Next Article in Journal
Effects of IGF1 and IGF2 on In Vitro Ovarian Follicle Maturation in Rainbow Trout, Oncorhynchus mykiss
Previous Article in Journal
Conservation Genetics of Clinch Dace Chrosomus sp. cf. saylori
Previous Article in Special Issue
Effect of the Potential Probiotic Vibrio proteolyticus DCF12.2 on the Immune System of Solea senegalensis and Protection against Photobacterium damselae subsp. piscicida and Vibrio harveyi
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Fishes
Volume 8
Issue 7
10.3390/fishes8070366
fishes-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Effect of Bacillus Probiotics on the Immunological Responses of Nile Tilapia (Oreochromis niloticus): A Review

by
Vicent Michael Shija
1,2,3,
Kwaku Amoah
1,2,3 and
Jia Cai
1,2,3,4,5,6,*
1
College of Fishery, Guangdong Ocean University, Zhanjiang 524088, China
2
Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, Zhanjiang 524088, China
3
Guangdong Key Laboratory of Control for Diseases of Aquatic Economic Animals, Zhanjiang 524088, China
4
Southern Marine Science and Engineering Guangdong Laboratory, Zhanjiang 524002, China
5
Guangxi Key Laboratory for Marine Natural Products and Combinational Biosynthesis Chemistry, Nanning 530200, China
6
Guangxi Beibu Gulf Marine Research Centre, Guangxi Academy of Sciences, Nanning 530007, China
*
Author to whom correspondence should be addressed.
Fishes 2023, 8(7), 366; https://doi.org/10.3390/fishes8070366
Submission received: 16 June 2023 / Revised: 6 July 2023 / Accepted: 11 July 2023 / Published: 13 July 2023
(This article belongs to the Special Issue Potential Application of Probiotics for Sustainable Aquaculture)
Browse Figures
Review Reports Versions Notes

Abstract

:
The use of antibiotics and therapeutics for Nile tilapia has increased along with its increased production and intensification. Probiotics have been studied as an alternative to the excessive use of antibiotics in fish diets. Studies have demonstrated that dietary Bacillus probiotic inclusion promotes faster growth and disease resistance in farmed fish species. Despite advances in research, there is still uncertainty about the mechanisms controlling the immune response of fish. In this review, we summarize and discuss recent research on the immune responses of Nile tilapia to Bacillus probiotics. Through the use of immunological information including phagocytosis, lysozyme activity, respiratory activity, antioxidant proteins, complement activity, and immune-related gene expression, researchers hope to develop effective strategies for successfully using Bacillus probiotics in Oreochromis niloticus farming.
Keywords:
Nile tilapia; Bacillus probiotics; gut microbiota; immune response
Key Contribution: The key aspect highlighted in the review is the effects of Bacillus probiotics on Nile tilapia’s immune system.

Graphical Abstract

1. Introduction

Over the last few decades, aquaculture has grown in popularity as a method of producing seafood for human consumption [1]. It has been a key part of many regions of the world’s food supply and has been rising tremendously as the demand for seafood increases [2]. However, in recent years, aquaculture has been plagued by a variety of infections, resulting in massive economic losses [3].
The use of antibiotics in commercial aquaculture has been a common practice for many years. While this practice has been effective in combating infectious diseases, it has also caused several significant problems [4,5]. In recent years, indiscriminate pesticide and antibiotic usage has led to the emergence of antibiotic-resistant bacteria, and residual antibiotics can be detected in aquatic products. Using pesticides and antibiotics to control disease outbreaks is no longer encouraged due to their detrimental effects on the environment, including the creation of mutagenic microbial strains and harming fish, including Nile tilapia [6,7].
As a result, the use of environmentally acceptable feed additives, such as probiotics, to improve the physiology, growth performance, and immune responses of aquaculture-related species has grown in popularity in recent years [8,9]. It is known that live bacteria, also known as probiotics, can have a variety of physiological effects on the hosts [10]. One of the primary benefits of Bacillus probiotics is their ability to regulate mucosal and systemic immunity, thus reducing inflammation and improving the body’s ability to fight off infection [11,12].
Bacillus probiotics have been found to help improve the absorption of vitamins and minerals from food and help break down proteins, carbohydrates, and fats to ensure that the body is obtaining the nutrients it needs for optimal health [13,14]. However, choosing the right probiotics is crucial because the wrong ones can negatively impact nutrient metabolism, immunomodulation, colonization resistance, and pathogen resistance. Critical considerations include the ability to be cultured on a larger scale and survive until reaching the gastrointestinal tract (GIT) of the host by being able to resist acidic conditions in the stomach [14].
Incorporating Bacillus probiotics, such as B. coagulans ATCC 7050 and B. subtilis WB60, into aquatic animals’ diets has improved their development, growth, immunity, and disease resistance [15,16]. As a result, Bacillus probiotic supplementation has been noted to be effective in improving fish health, including Nile tilapia [17,18].
Although Bacillus probiotics have gained increased attention, their mechanism of action, optimal dosage, and administration techniques remain poorly understood [19,20]. The Nile tilapia is a species of freshwater fish that is widely farmed throughout the world. Its hardiness, fast growth rate, and high nutritional value make it an attractive choice for farmers, and its efficient farming systems make it a more sustainable option for the environment. With landings of farmed Nile tilapia reaching an all-time high, it is clear that this species will continue to be an important part of the aquaculture industry for years to come [21,22,23].
Extensive Nile tilapia farming has been a profitable agricultural activity for many years. However, in recent years, the sector has been challenged by several disease outbreaks caused by pathogenic bacteria, resulting in a high rate of Nile tilapia mortality and morbidity [24,25]. The immunomodulatory activity of Bacillus probiotic (Bacillus cereus) administered to Nile tilapia is essential [26]. This is because Bacillus probiotics can assist in boosting the fish’s immune system, minimize disease risk, and reduce the number of antibiotics used in farming [27,28,29,30,31]. Therefore, this review emphasized recently discovered information concerning the immunomodulatory activity of recent Bacillus probiotics studies that influence the immunomodulatory potency via Nile tilapia diets. The reasonable identification of knowledge gaps in this field has emphasized the necessity for future research on efficient fish health management systems and advancing the aquaculture sectors.

2. Common Bacillus Probiotics Used in Nile Tilapia Rearing and Farming

Several Bacillus species have been identified as potential probiotics for aquaculture (including B. subtilis, B. clausii, B. velezensis, B. cereus, B. coagulans, B. licheniformis, B. pumilus, B. mojavensis, and B. megaterium) [32,33,34,35]. Using Bacillus species in tilapia farming is common and effective, primarily as feed or water additives [36,37,38,39]. The most common way to give fish probiotics is through the use of feed.
Encapsulating the probiotic in feed allows it to be released slowly over a more extended period, creating a sustained-release effect. This allows the probiotic to remain in the fish’s intestines longer, interacting with the immune system and developing a positive effect [30,40,41]. Probiotics are administered to fish through live food, either by packaging the probiotic in the live food or by adding it to the water where the live feed is grown.
Because the probiotic is included in the live feed, it may be promptly and directly absorbed by the fish, having an immediate impact [41]. To increase their benefits, Bacillus probiotics can be combined with prebiotics or other substances (fructooligosaccharide combined with B. licheniformis, Astragalus extracts combined with B. subtilis) [42,43,44]. Prebiotics are non-digestible food elements that promote the growth and activity of beneficial bacteria in the gut and can aid in boosting probiotic effectiveness [45]. In addition, vitamins, minerals, and enzymes can also be added to the probiotic to enhance its benefits.
As a result, the carrier may influence immune system regulation [46]. Nile tilapia have been discovered to benefit from Bacillus probiotics (B. safensis, B. subtilis, B. licheniformis) which offer several health advantages [20,47,48]. Bacillus probiotics can contribute to the health and growth of Nile tilapia by encouraging the growth of beneficial bacteria in the gut, enhancing feed conversion effectiveness, and increasing disease resistance [49,50]. Nile tilapia have been reported to benefit from Bacillus probiotics, although the exact method of action and dosage may vary from fish to fish [51,52,53].

3. Bacillus Probiotics and Gut Microbiota

The gut microbiota consists of bacteria found in the gastrointestinal tracts of humans and other animals that live in symbiotic relationships with them [54]. The gut microbiota of Nile tilapia has been noted to be primarily dominated by the phyla Fusobacteria, Proteobacteria, and Bacteroidetes [55,56]. Nile tilapia’s skin, eggs, gills, and digestive system are home to numerous natural kinds of bacteria [57].
The gut microbiome controls the intestinal epithelium’s morphology, function, host physiology, and immunological responses, which significantly impact digestion and homeostasis [58,59]. Adeoye et al. [60] studied the effects of Bacillus probiotics (B. subtilis, B. licheniformis, and B. pumilus) on the gut microbiota of Nile tilapia.
Adding Bacillus probiotics to Nile tilapia feed increased the levels of beneficial bacteria, such as Lactobacillus and Bifidobacterium, while decreasing the levels of pathogenic bacteria. Han et al. [20] investigated the effects of Bacillus probiotics (B. licheniformis) on Nile tilapia growth performances. Bacillus probiotics were found to increase the growth rate of Nile tilapia when added to their feed. Hence, Bacillus probiotics may benefit Nile tilapia, as they can help improve the gut microbiota. Magda et al. [61] investigated the viability of Bacillus probiotics in influencing immunity in Nile tilapia. Their study found that adding Bacillus subtilis to the Nile tilapia diet significantly improves the immune system.
Studies have shown that using Bacillus probiotics can significantly increase the number of beneficial bacteria in the gut of Nile tilapia. These beneficial bacteria can help promote better digestion and absorption of nutrients and reduce the risk of disease [62]. For example, dietary administration of a Bacillus probiotic (Bacillus cereus) increased beneficial bacteria such as Lactobacillus, Bifidobacterium, and Enterococcus species and decreased pathogenic bacteria such as Aeromonas and Vibrio species [26], as well as several immune-related genes, such as interleukin-1β, tumor necrosis factor-α, and interferon-γ.
As shown in a study by Wu et al. [48], Bacillus safensis NPUST1 supplementation appears to be effective in regulating the gut microbiota within Nile tilapia. It provides a potential solution to aluminum-induced imbalances within the gut microbiota of Nile tilapia. In addition, Bacillus probiotics (B. velezensis, B. cereus,) increased the production of short-chain fatty acids, which are beneficial for gut health [63]. Based on the data provided by Hassaan et al. [64], Bacillus pumilus significantly enhanced Nile tilapia growth, immunity, and gut microbiota. A probiotic Bacillus strain improved Nile tilapia’s growth performance significantly. Results showed that the fish gained weight, were more fed, and had a higher specific growth rate. Additionally, the use of Bacillus probiotics (B. coagulans) significantly improved the total serum protein level, lysozyme activity, and total immunoglobulin E (IgE) level in Nile tilapia [11].
Similarly, Yaqub et al. [65] found that dietary supplementation with Bacillus licheniformis SB3086 improved growth performance, immunological parameters, intestinal morphology, and resistance to challenge infections in Oreochromis mossambicus. The growth performance, immunological parameters, intestinal morphology, and resistance of O. mossambicus were significantly improved by B. licheniformis SB3086.
The colonization dynamics of the gut microbiota in Nile tilapia are largely determined by environmental factors (such as temperature, pH, and salinity) [66,67,68,69]. It has been shown that Nile tilapia’s diet also influences gut microbiota colonization dynamics [70,71,72].
Also, certain dietary components, including carbohydrates, proteins, lipids, and vitamins, may influence gut microbiome composition [66,73]. Fish’s age, diet, and health status also affect the colonization dynamics of their gut microbiota, with some bacteria becoming more abundant as they age [56,74].
The composition of the gut microbiome of Nile tilapia may also be influenced by environmental toxins, such as heavy metals [75].

4. Mode of Action of Bacillus Probiotics in Nile Tilapia

Bacillus probiotics (B. subtilis) have the potential to protect the intestines against diseases, make the environment inhospitable for pathogens, compete for vital nutrients, restrict epithelial adhesion sites, and alter immune responses at the physiological and molecular levels (Figure 1) [76].
Probiotics from the genus can be consumed in various ways, including as food supplements, bio-encapsulated Bacillus particles, and water additives [77]. Bacillus probiotics (such as B. amyloliquefaciens) are known to create both organic acids and short-chain fatty acids, which can enhance the operation of the digestive system to aid in food digestion (proteins, carbohydrates, and lipids) [78,79].
As a result of enhancing the production of digestive enzymes, such as lipase, amylase, and protease, Bacillus probiotics (B. subtilis and B. licheniformis) improve feed digestibility [80]. Two host-associated Bacillus species (B. amyloliquefaciens and B. licheniformis) were fed to Nile tilapia, and high lipase activity was seen in B. subtilis in their intestines [49,50].
Bacillus probiotics (such as Bacillus sp. KUAQ1 and Bacillus sp. KUAQ2, B. subtilis C-3102, B. subtilis, and B. velezensis LF01) have been shown to compete for adhesion sites with pathogens on the gastrointestinal epithelium of Nile tilapia [81,82,83,84].
According to Bidhan et al. [30], Bacillus clausii produces several inhibitory substances (proteases) that can aid in the inhibition of pathogen adherence to the mucosal epithelium.
A range of Bacillus species, including B. cereus, B. subtilis, and B. amyloliquefaciens, can compete with pathogens for adhesion sites, protecting Nile tilapia from diseases [85]. For instance, Vibrio sp. (V. harveyi and V. parahaemolyticus, V. alginolyticus) and Mycobacterium species were suppressed from growing in Nile tilapia when B. pumilus, B. firmus, B. subtilis, and B. cereus were utilized as probiotics [86].
By inhibiting intestinal absorption and hepatic accumulation of aluminum, Bacillus probiotic bacteria like Bacillus cereus and Bacillus subtilis can alleviate aluminum-induced oxidative stress and tissular damage caused by aluminum [87].
Among the most commonly used aquaculture probiotics, Bacillus subtilis promotes multiple protective mechanisms such as synergistic mechanisms, antagonistic mechanisms, competitive exclusion, and immune stimulation [88]. Intestinal cell and microvillus density were boosted by adding B. subtilis and B. cereus to tilapia’s diet, boosting disease resistance via changes in the intestinal microbiota [17].
Kuebutornye et al. [50] reported that the increase in density of microvilli in fish intestines could minimize pathogenic microorganisms’ colonization rate. Microvilli are minute, finger-like protrusions that line the surface of the intestines, and their density has been found to influence the intestine’s absorptive surface area [89].
A higher density of microvilli enhances the absorptive surface area, allowing for better absorption of nutrients and other substances. Because there are fewer surfaces for the pathogenic microbes to attach and colonize as a result of the increased absorptive surface area, the rate at which they cling and colonize also decreases [90].
Activating and altering the fish’s immune response with dietary Bacillus probiotics has been found to increase the resistance of Nile tilapia to various infections (Table 1) [91].

5. Bacillus Probiotics and Fish Immunological Response

The Nile tilapia is an important species of fish due to its well-developed innate immune system [101]; this system is composed of physical barriers, humoral components, and cellular components [102]. The physical barriers of the Nile tilapia include the skin made up of several layers of cells that provide a protective barrier against infection. The mucus layer of the fish helps trap any foreign particles that may enter the body [103]. The humoral components of the Nile tilapia’s immune system are made up of proteins and other molecules that are produced by the fish’s body to fight off any potential pathogens [92,104]. The cellular components of the Nile tilapia’s immune system are composed of several different types of cells that are responsible for recognizing and attacking any foreign particles that may enter the body [105,106].
Epithelial cells are a type of cell that forms the outer layer (skin, mouth, digestive tract, respiratory system) of tissue in organs and other structures of the body; these cells are important for protection, absorption, secretion, and transport [107]. In addition to protecting the body from infection and disease, mucous secretions are made up of immune system cells (mucosa-associated lymphoid tissue (MALT)). Based on its location, MALT can be divided into three types: gill-associated lymphoid tissue (GALT), skin-associated lymphoid tissue (SALT), and gut-associated lymphoid tissue (GALT) [108].
In the gut mucosa, probiotic organisms interact with numerous immune-competent cells [109]. Pathogen pattern recognition receptors (PRRs) are gene-encoded proteins that detect molecular patterns of pathogens and inform the host whether or not the pathogen is pathogenic [110]. Bacillus probiotic species (B. amyloliquefaciens, B. subtilis) interact with several immune-competent cells in the gut mucosa of the host (Nile tilapia). A host can identify pathogenic bacteria using pathogen pattern recognition receptors (PRRs), which are germ-line encoded proteins that recognize pathogen-specific molecular patterns [95,111]. Molecular patterns associated with damage or pathogens (PAMPs or DAMPs) recognized by PRRs include lipopolysaccharides, lipoic acid, peptidoglycan, and viral intracellular signatures.
The host recognizes microbe-associated molecular patterns (MAMPs) found in pathogens and nonpathogenic microorganisms. Bacillus probiotics (B. subtilis, B. fragilis) are examples of PAMPs on nonpathogenic microorganisms [112,113]. In response to pathogens, the innate immune system is alerted by signaling molecules generated when MAMPs and PRRs interact on host cells [38,96]. MAMPs from Bacillus licheniformis HGA8B interacted with PRRs of antigen-presenting cells and epithelial cells via toll-like receptors (TLRs) and nucleotide oligomerization domain receptors (NLRs), increasing complement activity in Nile tilapia fed diets containing Bacillus licheniformis HGA8B [96].
MAMPs, such as peptidoglycans, are found in the cell walls of Bacillus species (B. subtilis) and other bacteria [114,115]. MAMPs increase the transcription of pro-inflammatory cytokines and chemokines, which recruit innate immune cells when Bacillus probiotics (B. subtilis) interact with the immune system [71,115]. Several studies have shown that Bacillus probiotics (B. velezensis TPS3N, B. subtilis TPS4, B. amyloliquefaciens TPS17) can improve tilapia’s local and systemic immunity (Figure 2 summarizes the effects of Bacillus probiotics on fish immunological responses) [39,49,50].

5.1. Bacillus Probiotics Improve Immune Response

Several types of immune system cells can interact with probiotic bacteria (Bacillus subtilis). These cells include monocytes, macrophages, lymphocytes, granulocytes, neutrophils, and natural killer cells [116]. Through signaling from the cell surface pattern recognition receptors or by activating lymphoid cells, Nile tilapia can enhance their innate immune response to threats as a result of etiological agents [117].
Activation of immune cells by Bacillus probiotics (B. coagulans, B. licheniformis, and B. subtilis) can alter the intestinal mucosa by detecting DAMPs contained in stressed or wounded cells’ biomolecules [10,118]. Opiyo et al. [119] found that Bacillus subtilis can increase white blood cells in Nile tilapia when administered as a probiotic. For instance, a study of Nile tilapia fed Bacillus pumilus-containing diets showed greater peripheral blood leukocyte counts [53]. Acidophilic granulocytes and intraepithelial lymphocyte proliferation were increased in Nile tilapia fed diets containing Bacillus subtilis and Bacillus licheniformis [120].
In Reda and Selim’s study, the use of Bacillus amyloliquefaciens in fish feed improved intestinal function and mucosal immunity in Nile tilapia by increasing villous height in the proximal and middle intestines [121]. In fish and higher vertebrates, serum immunoglobulins are a crucial component of the humoral immune system and help to provide disease resistance. B lymphocytes create antibodies that bind to an antigen when it is encountered.
This binding procedure aids in preventing disease-causing antigens from entering the body [61]. Several Bacillus probiotics such as B. amyloliquefaciens and Lactobacillus sp., B. velezensis TPS3N, B. subtilis TPS4, and B. amyloliquefaciens TPS1, whether administered separately or in combination, have been shown to increase immunoglobulin levels and leukocyte counts [49,50,122].

5.2. Bacillus Probiotics Modulate Phagocytic Activity

The innate immune system acts as the first line of defense against infection [123], and Bacillus probiotics (B. amyloliquefaciens, B. subtilis, B. licheniformis, and B. pumilus) have been shown to enhance phagocytosis in Nile tilapia [124]. Bacillus subtilis probiotics ameliorated Nile tilapia’s phagocytic index despite the fish being raised at high stocking density, demonstrating that Bacillus probiotics can relieve the stress associated with intensive rearing [47].
In the study conducted by Fath El-Bab et al. [125], it was found that feeding Bacillus coagulans-containing diets increased phagocytic activity in Nile tilapia farming. Pei-Shan Wu et al. [48] also observed an increase in phagocytosis in Nile tilapia fed diets containing Bacillus safensis NPUST1 against Aeromonas hydrophila. In addition, another study by Telli et al. [47] discovered that adding Bacillus probiotics to fish feed caused Nile tilapia to increase phagocytic activity. Similarly, adding Enterococcus faecium to the tilapia diet increased immunity when exposed to A. hydrophila, indicating an immunological resistance [126].

5.3. Bacillus Probiotics Regulate Lysozyme Activity

Bacillus amyloliquefaciens and Bacillus subtilis have both demonstrated lysozyme stimulation in Nile tilapia [52,92,100]. Saurabh et al. [101] suggest that the increased lysozyme levels in Nile tilapia could be attributed to an increase in phagocytes that secrete lysozyme or an increase in lysozyme-producing cells. The type, quantity, and time of Bacillus probiotics (B. velezensis H3.1) that are administered may affect lysozyme activity [59]. In Nile tilapia exposed to the pathogenic bacteria Streptococcus agalactiae, Bacillus amyloliquefaciens was found to increase lysozyme levels [52]. Lysozyme is a multifunctional enzyme present in many animals, plants, and microbes; lysozyme, on the other hand, attacks chitin, a significant component of fungal cell walls [101].
In Nile tilapia challenged with hypoxic conditions, Bacillus pumilus administered as a probiotic significantly improved various humoral and cellular immune activities, including lysozyme activity [92]. Furthermore, Bacillus subtilis controls lysozyme activity and reduces the negative effects of salinity stress on Nile tilapia [127].

5.4. Bacillus Probiotics Modulate the Respiratory Burst Process

Bacillus probiotics can modify the respiratory burst process in Nile tilapia; the respiratory burst process is a natural defense mechanism used by fish to defend themselves against pathogens and other environmental stressors [82]. Bacillus probiotics can influence the respiratory burst process in Nile tilapia by generating antioxidant molecules.
These molecules help to reduce reactive oxygen species (ROS) production by cells, hence minimizing the amount of oxidative damage that occurs [52]. Compared to the control group, Nile tilapia fed a diet containing Bacillus subtilis strain NZ86 for 51 days displayed increased respiratory burst activity [37]. However, the period of Bacillus probiotic feeding required to boost particular immunological parameters varies between Bacillus probiotic strains and aquatic species. When tilapia juveniles were fed Bacillus pumilus AQAHBS01 (1 × 107–109) for 14 days, respiratory burst activity was significantly enhanced [53], but no differences were found during feeding with Bacillus safensis NPUST1 strains for 8 weeks [48].
Furthermore, Liu et al. [92] found that no significant differences in respiratory burst activity were detected between two strains of Bacillus subtilis and Bacillus licheniformis during the feeding of Nile tilapia over 4 weeks. To decide the optimal feeding duration for Nile tilapia probiotics, further research is required to determine the benefits of short- and long-term administration, as well as the attributes and dosage of cultured strains.

5.5. Bacillus Probiotics Improve Complement Activity

Complement activity is a type of immune response triggered when the body detects the presence of a foreign substance, such as a virus or pathogenic bacteria [128,129]. In Nile tilapia, Bacillus probiotics have been found to improve complement activity by increasing the production of proteins (complement factors), which help to identify and target foreign substances [130]. Nile tilapia diet containing B. amyloliquefaciens, B. licheniformis, B. pumilus AQAHBS01, and Pediococcus pentosaceus PKWA-1 and B. subtilis BA04 showed increased complement-mediated hemolysis [20,82].
In multiple investigations, tilapia fed diets containing B. amyloliquefaciens, B. licheniformis, Bacillus pumilus AQAHBS01, and Pediococcus pentosaceus PKWA-1 and B. subtilis BA04 showed higher complement-mediated hemolytic activity [53]. Nevertheless, feeding Bacillus subtilis O14VRQ and Bacillus spp. KUAQ1 to Nile tilapia failed to increase serum complement levels [37,82].
A two-experiment study by Ridha and Azad [131] found that only adult Nile tilapia had high serum complement activity after consumption of Bacillus subtilis in the diet; thus, divergent findings highlight the value of thoroughly investigating how probiotics affect Nile tilapia’s immune response and growth.

5.6. Bacillus Probiotics Stimulate Immune-Related Gene Expression

The effects of Bacillus probiotics on the expression of immune-related genes in Nile tilapia have been studied in various studies [98]. A significant increase in cytokine and chemokine expression was observed in Nile tilapia fish treated with Bacillus probiotics (B. amyloliquefaciens, B. subtilis, and B. licheniformis) [132,133,134]. Nile tilapia express immune-related genes in response to multiple pathogens, including pro-inflammatory and anti-inflammatory cytokines such as interleukin-1 (IL-1), interleukin-8 (IL-8), interferon (IFN), tumor necrosis factor (TNF), and interleukin-10 (IL-10) [99,135]. Pro-inflammatory and anti-inflammatory cytokines are proteins released by various cells in the fish parts that contribute to defense in the presence of bacteria colonization or invasion.
The balance of cytokine expression is a major component in determining the immune response to Bacillus probiotics [135]. In Nile tilapia fed diets containing both B. subtilis and B. licheniformis, C-lysozyme, heat shock protein 70 (HSP70), transforming growth factor beta (TGF-), defensin and small body size decapentaplegic homolog 3 (SMAD3) were upregulated in the mid-intestine and head kidney [54,103,136,137].
DAMPs also promote the host’s defense mechanisms, as shown by elevated HSP70, IL-1, IFN-gamma, and tumor necrosis factor (TNF) expression in Nile tilapia fed diets containing Bacillus subtilis WB60 or Lactococcus lactosis [100]. In Nile tilapia diets containing Bacillus licheniformis HGA8B, IL-10 demonstrated anti-inflammatory effects, suggesting that the host may have developed tolerance to the probiotic as it is not perceived as a threat [99].
A study in Nile tilapia showed increased cytokine IL-10 in the intestine after administration of Bacillus probiotics (B. licheniformis and B. subtilis) [51,54,135]. As molecular chaperones, heat shock proteins (HSPs) (HSP60, HSP70, and HSP90 families) interact with proteins to prevent them from aggregating, refold polypeptides, and repair or denature proteins in altered or denatured states [10,138]. In aquatic species, HSP70s are considered the most helpful biomarkers of infection due to their wide range of expression [139].
During stressful conditions, fish secrete significant amounts of HSP70, which may boost protein integrity and reduce apoptosis [81,98,138]. Fish have been found to express less HSP70 in some studies, but Nile tilapia exhibit the opposite trend in numerous in-vivo studies. In general, suppression of HSP70 gene expression by probiotics is associated with a reduction in growth rate and survival [137,140].

6. Bacillus Probiotics Regulate Antioxidant Enzyme Activity

Bacillus probiotics (such as B. subtilis) have been proven to help regulate the antioxidant enzyme activity of Nile tilapia farm operations. The antioxidant enzymes in fish help break down the hazardous compounds in the water and prevent the detrimental effects of free radicals (Table 1) [141]. It has been shown that Bacillus probiotics can significantly reduce oxidative stress in various health problems that are exacerbated by oxidative stress [142].
Many aerobic cellular functions generate reactive oxygen species, and their concentration is determined by their synthesis and elimination by the antioxidant system [143]. Numerous antioxidants are found in cells and are involved in maintaining ROS levels at low levels, preventing oxidative damage, and preventing the onset of several diseases [144]. A variety of fish species, including Nile tilapia, contain antioxidant enzymes like superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPx) [100,145]. Antioxidant enzyme activities are frequently utilized as functional criteria for assessing Nile tilapia immune responses [26].
Bacillus subtilis, Bacillus coagulans [139], and Bacillus cereus [26] added to Nile tilapia rearing systems increased SOD activity. A similar rise in SOD activity was seen when Bacillus paralicheniformis SO1 was added to tilapia diets [140]. In the fish’s liver and intestines, SOD, CAT, and GPx levels are increased, indicating an enhanced ability to fight disease. Fish probiotics, including Bacillus spp., have been linked to an increase in antioxidant enzymes in various fish, including tilapia [99,142,146,147,148].

7. Conclusions and Future Perspectives

This review summarizes current knowledge about the beneficial effects of Bacillus probiotics on Nile tilapia (Oreochromis niloticus) immunity at various life stages, highlighting several areas in need of further investigation. This review provides compelling evidence that the administration of Bacillus probiotics can alter Nile tilapia’s immunity by strengthening the gut barrier’s defense mechanisms, thereby preventing the development of several diseases. According to the findings, probiotic bacteria can modify and strengthen Nile tilapia’s immune system through a variety of mechanisms. Academicians, scientists, producers, and fish industry owners must investigate the specific aspects of bacteria–host interactions conferring favorable changes in diverse immune responses to offer clinically effective, bacteria-based strategies to support aquaculture’s health, production, and economic growth. There is also potential for future research to investigate the co-administration of Bacillus probiotics with prebiotics, multiple-species probiotics, pulse-feeding tactics, and encapsulating techniques to preserve Bacillus probiotics throughout treatment.

Author Contributions

Conceptualization, methodology, validation, writing—original draft preparation, V.M.S.; methodology, software, validation, writing—review and editing, visualization, supervision, K.A.; validation, resources, writing—review and editing, project administration, funding acquisition, J.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (U20A2065, 32002426, 32073006), Natural Science Foundation of Guangdong Province (2021A1515010532, 2022A1515010553), and Zhanjiang Science and Technology Plan Project (2022A01012, 2022A01006).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We are grateful to Jia Cai (Guangdong Ocean University) for his support in writing this paper. The authors are appreciative to all the laboratory members for the support. We are also grateful to the Editor and Reviewers for their constructive criticisms and suggestions, making this study a genuine one.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Mohapatra, S.; Chakraborty, T.; Kumar, V.; DeBoeck, G.; Mohanta, K.N. Aquaculture and stress management: A review of probiotic intervention. J. Anim. Physiol. Anim. Nutr. 2013, 97, 405–430. [Google Scholar] [CrossRef] [PubMed]
  2. Boyd, C.E.; McNevin, A.A.; Davis, R.P. The contribution of fisheries and aquaculture to the global protein supply. Food Secur. 2022, 14, 805–827. [Google Scholar] [CrossRef] [PubMed]
  3. Bouwmeester, M.M.; Goedknegt, M.A.; Poulin, R.; Thieltges, D.W. Collateral diseases: Aquaculture impacts on wildlife infections. J. Appl. Ecol. 2021, 58, 453–464. [Google Scholar] [CrossRef]
  4. Akanmu, O.A. Probiotics, an Alternative Measure to Chemotherapy in Fish Production. In Probiotics-Current Knowledge and Future Prospects; IntechOpen: London, UK, 2018; Volume 1, pp. 9–12. [Google Scholar]
  5. Hoseinifar, S.H.; Sun, Y.-Z.; Wang, A.; Zhou, Z. Probiotics as Means of Diseases Control in Aquaculture, a Review of Current Knowledge and Future Perspectives. Front. Microbiol. 2018, 9, 2429. [Google Scholar] [CrossRef] [PubMed]
  6. Okocha, R.C.; Olatoye, I.O.; Adedeji, O.B. Food safety impacts of antimicrobial use and their residues in aquaculture. Public Health Rev. 2018, 39, 21. [Google Scholar] [CrossRef] [PubMed]
  7. Zorriehzahra, M.J.; Delshad, S.T.; Adel, M.; Tiwari, R.; Karthik, K.; Dhama, K.; Lazado, C.C. Probiotics as beneficial microbes in aquaculture: An update on their multiple modes of action: A review. Vet. Q. 2016, 36, 228–241. [Google Scholar] [CrossRef]
  8. Goh, J.X.H.; Tan, L.T.H.; Law, J.W.F.; Ser, H.L.; Khaw, K.Y.; Letchumanan, V.; Lee, L.H.; Goh, B.H. Harnessing the potentialities of probiotics, prebiotics, synbiotics, paraprobiotics, and postbiotics for shrimp farming. Rev. Aquac. 2022, 14, 1478–1557. [Google Scholar] [CrossRef]
  9. Merrifield, D.L.; Dimitroglou, A.; Foey, A.; Davies, S.J.; Baker, R.T.; Bøgwald, J.; Castex, M.; Ringø, E. The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 2010, 302, 1–18. [Google Scholar] [CrossRef]
  10. Nayak, S. Probiotics and immunity: A fish perspective. Fish Shellfish Immunol. 2010, 29, 2–14. [Google Scholar] [CrossRef]
  11. Patel, S.; Shukla, R.; Goyal, A. Probiotics in valorization of innate immunity across various animal models. J. Funct. Foods 2015, 14, 549–561. [Google Scholar] [CrossRef]
  12. Marco, M.L.; Pavan, S.; Kleerebezem, M. Towards understanding molecular modes of probiotic action. Curr. Opin. Biotechnol. 2006, 17, 204–210. [Google Scholar] [CrossRef]
  13. Kuebutornye, F.K.A.; Abarike, E.D.; Sakyi, M.E.; Lu, Y.; Wang, Z. Modulation of nutrient utilization, growth, and immunity of Nile tilapia, Oreochromis niloticus: The role of probiotics. Aquac. Int. 2020, 28, 277–291. [Google Scholar] [CrossRef]
  14. Olmos Soto, J. Bacillus Probiotic Enzymes: External Auxiliary Apparatus to Avoid Digestive Deficiencies, Water Pollution, Diseases, and Economic Problems in Marine Cultivated Animals, 1st ed.; Advances in Food and Nutrition Research; Elsevier Inc.: Amsterdam, The Netherlands, 2017; Volume 80, pp. 15–35. [Google Scholar]
  15. Amoah, K.; Huang, Q.-C.; Tan, B.-P.; Zhang, S.; Chi, S.-Y.; Yang, Q.-H.; Liu, H.-Y.; Dong, X.-H. Dietary supplementation of probiotic Bacillus coagulans ATCC 7050, improves the growth performance, intestinal morphology, microflora, immune response, and disease confrontation of Pacific white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol. 2019, 87, 796–808. [Google Scholar] [CrossRef]
  16. Lee, S.; Katya, K.; Hamidoghli, A.; Hong, J.; Kim, D.-J.; Bai, S.C. Synergistic effects of dietary supplementation of Bacillus subtilis WB60 and mannanoligosaccharide (MOS) on growth performance, immunity and disease resistance in Japanese eel, Anguilla japonica. Fish Shellfish Immunol. 2018, 83, 283–291. [Google Scholar] [CrossRef]
  17. Xia, Y.; Wang, M.; Gao, F.; Lu, M.; Chen, G. Effects of dietary probiotic supplementation on the growth, gut health and disease resistance of juvenile Nile tilapia (Oreochromis niloticus). Anim. Nutr. 2020, 6, 69–79. [Google Scholar] [CrossRef]
  18. Addo, S.; Carrias, A.A.; Williams, M.A.; Liles, M.R.; Terhune, J.S.; Davis, D.A. Effects of Bacillus subtilis strains and the prebiotic Previda® on growth, immune parameters and susceptibility to Aeromonas hydrophila infection in Nile tilapia, Oreochromis niloticus. Aquac. Res. 2017, 48, 4798–4810. [Google Scholar] [CrossRef]
  19. Arora, M.; Baldi, A. Selective Identification and Characterization of Potential Probiotic Strains: A Review on Comprehensive Polyphasic Approach. Appl. Clin. Res. Clin. Trials. Regul. Aff. 2017, 4, 60–76. [Google Scholar] [CrossRef]
  20. Han, B.; Long, W.-Q.; He, J.-Y.; Liu, Y.-J.; Si, Y.-Q.; Tian, L.-X. Effects of dietary Bacillus licheniformis on growth performance, immunological parameters, intestinal morphology and resistance of juvenile Nile tilapia (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol. 2015, 46, 225–231. [Google Scholar] [CrossRef]
  21. Richardson, K.; Wilcox, C.; Vince, J.; Hardesty, B.D. Challenges and misperceptions around global fishing gear loss estimates. Mar. Policy 2021, 129, 104522. [Google Scholar] [CrossRef]
  22. Pilling, D.; Bélanger, J.; Hoffmann, I. Declining biodiversity for food and agriculture needs urgent global action. Nat. Food 2020, 1, 144–147. [Google Scholar] [CrossRef]
  23. Zhang, L. Global Fisheries Management and Community Interest. Sustainability 2021, 13, 8586. [Google Scholar] [CrossRef]
  24. Thanh, H.; Viet, V.; Dinh, H.; Sangsuriya, P.; Jitrakorn, S. Naturally concurrent infections of bacterial and viral pathogens in disease outbreaks in cultured Nile tilapia (Oreochromis niloticus) farms. Aquaculture 2015, 448, 427–435. [Google Scholar]
  25. Fitzsimmons, K. From Africa to the world—The journey of Nile tilapia. Rev. Aquac. 2023, 15, 6–21. [Google Scholar]
  26. Wang, M.; Liu, G.; Lu, M.; Ke, X.; Liu, Z.; Gao, F.; Cao, J.; Zhu, H.; Yi, M.; Yu, D. Effect of Bacillus cereus as a water or feed additive on the gut microbiota and immunological parameters of Nile tilapia. Aquac. Res. 2017, 48, 3163–3173. [Google Scholar] [CrossRef]
  27. Van Hai, N. Research findings from the use of probiotics in tilapia aquaculture: A review. Fish Shellfish Immunol. 2015, 45, 592–597. [Google Scholar]
  28. Elkamel, A. Immunomodulation of Nile Tilapia, Oreochromis niloticus, by Nigella sativa and Bacillus subtilis. J. Aquac. Res. Dev. 2018, 19, 3–6. [Google Scholar]
  29. Van Doan, H.; Hossein, S.; Tapingkae, W. Combined administration of low molecular weight sodium alginate boosted immunomodulatory, disease resistance and growth-enhancing effects of Lactobacillus plantarum in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 2016, 58, 678–685. [Google Scholar] [CrossRef]
  30. Meena, D.K.; Behera, B.K.; Das, P. Probiotics in fish and shellfish culture: Immunomodulatory and ecophysiological responses Probiotics in fish and shellfish culture: Immunomodulatory and ecophysiological responses. Fish Physiol. Biochem. 2014, 1, 4–38. [Google Scholar]
  31. Nathanailides, C.; Kolygas, M.; Choremi, K.; Mavraganis, T.; Gouva, E.; Vidalis, K.; Athanassopoulou, F. Probiotics Have the Potential to Significantly Mitigate the Environmental Impact of Freshwater Fish Farms. Fishes 2021, 6, 76. [Google Scholar] [CrossRef]
  32. Buruiană, C.T.; Profir, A.G.; Vizireanu, C. Effects of probiotic Bacillus species in aquaculture—An overview. Ann. Univ. Dunarea Jos Galati. Fascicle VI-Food Technol. 2014, 38, 9–17. [Google Scholar]
  33. Emam, A.M.; Dunlap, C.A. Genomic and phenotypic characterization of Bacillus velezensis AMB-y1; a potential probiotic to control pathogens in aquaculture. Antonie Leeuwenhoek 2020, 113, 2041–2052. [Google Scholar] [CrossRef]
  34. Ya, X.L.; Li, L.J. Isolation and characterization of Bacillus spp. antagonistic to Vibrio parahaemolyticus for use as probiotics in aquaculture. J. Microbiol. Biotechnol. 2015, 2, 2–7. [Google Scholar]
  35. Soto, J.O. Feed intake improvement, gut microbiota modulation and pathogens control by using Bacillus species in shrimp aquaculture. World J. Microbiol. Biotechnol. 2021, 37, 28. [Google Scholar] [CrossRef]
  36. Aly, S.M.; Ahmed, Y.A.-G.; Ghareeb, A.A.-A.; Mohamed, M.F. Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol. 2008, 25, 128–136. [Google Scholar] [CrossRef]
  37. Galagarza, O.A.; Smith, S.A.; Drahos, D.J.; Eifert, J.D.; Williams, R.C.; Kuhn, D.D. Modulation of innate immunity in Nile tilapia (Oreochromis niloticus) by dietary supplementation of Bacillus subtilis endospores. Fish Shellfish Immunol. 2018, 83, 171–179. [Google Scholar] [CrossRef]
  38. Opiyo, M.A.; Jumbe, J.; Ngugi, C.C.; Charo-Karisa, H. Dietary administration of probiotics modulates non-specific immunity and gut microbiota of Nile tilapia (Oreochromis niloticus) cultured in low input ponds. Int. J. Vet. Sci. Med. 2019, 7, 1–9. [Google Scholar] [CrossRef]
  39. Cavalcante, R.B.; Telli, G.S.; Tachibana, L.; Dias, D.D.C.; Oshiro, E.; Natori, M.M.; da Silva, W.F.; Ranzani-Paiva, M.J. Probiotics, Prebiotics and Synbiotics for Nile tilapia: Growth performance and protection against Aeromonas hydrophila infection. Aquac. Rep. 2020, 17, 100343. [Google Scholar] [CrossRef]
  40. Ramos, E.A.; Relucio, J.L.V.; Torres-villanueva, C.A.T. Orginial Articles Gene Expression in Tilapia Following Oral Delivery of Chitosan-Encapsulated Plasmid DNA Incorporated into Fish Feeds. Mar Biotechnol. 2005, 7, 89–94. [Google Scholar] [CrossRef]
  41. Bakhrouf, A. Inhibitory activity and adhesive ability of potential probiotic Bacillus species to confer protection for Artemia gnotobiotic culture against pathogenic Vibrio spp. Inhibitory activity and adhesive ability of potential probiotic Bacillus species to confer. Turk. J. Vet. Sci. 2011, 35, 227–233. [Google Scholar]
  42. Zhang, C.N.; Li, X.F.; Xu, W.N.; Jiang, G.Z.; Lu, K.L.; Wang, L.N.; Liu, W.B. Combined effects of dietary fructooligosaccharide and Bacillus licheniformis on innate immunity, antioxidant capability and disease resistance of triangular bream (Megalobrama terminals). Fish Shellfish Immunol. 2013, 2, 1380–1386. [Google Scholar] [CrossRef]
  43. Liang, W.; Li, H.; Zhou, H.; Wang, M.; Zhao, X.; Sun, X.; Li, C.; Zhang, X. Effects of Taraxacum and Astragalus extracts combined with probiotic Bacillus subtilis and Lactobacillus on Escherichia coli—Infected broiler chickens. Poult. Sci. 2021, 100, 101007. [Google Scholar] [CrossRef] [PubMed]
  44. Shehata, A.A.; Yalçın, S.; Latorre, J.D.; Basiouni, S.; Attia, Y.A.; El-Wahab, A.A.; Visscher, C.; El-Seedi, H.R.; Huber, C.; Hafez, H.M.; et al. Probiotics, Prebiotics, and Phytogenic Substances for Optimizing Gut Health in Poultry. Microorganisms 2022, 10, 395. [Google Scholar] [CrossRef] [PubMed]
  45. Ogueke, C.; Owuamanam, C.; Ihediohanm, N.; Iwouno, J. Probiotics and Prebiotics: Unfolding Prospects for Better Human Health. Pak. J. Nutr. 2010, 9, 833–843. [Google Scholar] [CrossRef]
  46. Nayak, S.; Swain, P.; Mukherjee, S. Effect of dietary supplementation of probiotic and vitamin C on the immune response of Indian major carp, Labeo rohita (Ham.). Fish Shellfish Immunol. 2007, 23, 892–896. [Google Scholar] [CrossRef]
  47. Telli, G.S.; Ranzani-Paiva, M.J.T.; Dias, D.D.C.; Sussel, F.R.; Ishikawa, C.M.; Tachibana, L. Dietary administration of Bacillus subtilis on hematology and non-specific immunity of Nile tilapia Oreochromis niloticus raised at different stocking densities. Fish Shellfish. Immunol. 2014, 39, 305–311. [Google Scholar] [CrossRef]
  48. Wu, P.S.; Liu, C.H.; Hu, S.Y. Probiotic Bacillus safensis NPUST1 administration improves growth performance, gut microbiota, and innate immunity against Streptococcus iniae in nile tilapia (Oreochromis niloticus). Microorganisms 2021, 9, 2494. [Google Scholar] [CrossRef]
  49. Kuebutornye, F.K.; Tang, J.; Cai, J.; Yu, H.; Wang, Z.; Abarike, E.D.; Lu, Y.; Li, Y.; Afriyie, G. In vivo assessment of the probiotic potentials of three host-associated Bacillus species on growth performance, health status and disease resistance of Oreochromis niloticus against Streptococcus agalactiae. Aquaculture 2020, 527, 735440. [Google Scholar] [CrossRef]
  50. Kuebutornye, F.K.A.; Wang, Z.W.; Lu, Y.S.; Abarike, E.D.; Sakyi, M.E.; Li, Y.; Xie, C.X.; Hlordzi, V. Effects of three host-associated Bacillus species on mucosal immunity and gut health of Nile tilapia, Oreochromis niloticus and its resistance against Aeromonas hydrophila infection. Fish Shellfish Immunol. 2020, 97, 83–95. [Google Scholar] [CrossRef]
  51. Sciences, M. Dietary administration of a commercial mixed-species probiotic improves growth performance and modulates the intestinal immunity of tilapia, Oreochromis niloticus. Fish Shellfish Immunol. 2016, 1, 5–24. [Google Scholar]
  52. Saputra, F.; Shiu, Y.L.; Chen, Y.C.; Puspitasari, A.W.; Danata, R.H.; Liu, C.H.; Hu, S.Y. Dietary supplementation with xylanase-expressing B. amyloliquefaciens R8 improves growth performance and enhances immunity against Aeromonas hydrophila in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 2016, 58, 397–405. [Google Scholar] [CrossRef]
  53. Srisapoome, P.; Areechon, N. Efficacy of viable Bacillus pumilus isolated from farmed fish on immune responses and increased disease resistance in Nile tilapia (Oreochromis niloticus): Laboratory and on-farm trials. Fish Shellfish Immunol. 2017, 67, 199–210. [Google Scholar] [CrossRef]
  54. Ghanbari, M.; Kneifel, W.; Domig, K.J. A new view of the fish gut microbiome: Advances from next-generation sequencing. Aquaculture 2015, 448, 464–475. [Google Scholar] [CrossRef]
  55. Egerton, S.; Culloty, S.; Whooley, J.; Stanton, C.; Ross, R.P. The Gut Microbiota of Marine Fish. Front. Microbiol. 2018, 9, 873. [Google Scholar] [CrossRef]
  56. Yu, L.; Qiao, N.; Li, T.; Yu, R.; Zhai, Q.; Tian, F.; Zhao, J.; Zhang, H.; Chen, W. Dietary supplementation with probiotics regulates gut microbiota structure and function in Nile tilapia exposed to aluminum. PeerJ 2019, 7, e6963. [Google Scholar] [CrossRef]
  57. Li, X.; Ringø, E.; Hoseinifar, S.H.; Lauzon, H.L.; Birkbeck, H.; Yang, D. The adherence and colonization of microorganisms in the fish gastrointestinal tract. Rev. Aquac. 2019, 11, 603–618. [Google Scholar] [CrossRef]
  58. Tarnecki, A.; Burgos, F.; Ray, C.; Arias, C. Fish intestinal microbiome: Diversity and symbiosis unravelled by metagenomics. J. Appl. Microbiol. 2017, 123, 2–17. [Google Scholar] [CrossRef]
  59. Butt, R.L.; Volkoff, H. Gut Microbiota and Energy Homeostasis in Fish. Front. Endocrinol. 2019, 10, 9. [Google Scholar] [CrossRef]
  60. Adeoye, A.A.; Yomla, R.; Jaramillo-Torres, A.; Rodiles, A.; Merrifield, D.L.; Davies, S.J. Combined effects of exogenous enzymes and probiotics on Nile tilapia (Oreochromis niloticus) growth, intestinal morphology, and microbiome. Aquaculture 2016, 463, 61–70. [Google Scholar] [CrossRef]
  61. El-Ezabi, M.; Serafy, S.E.; Essa, M.; Daboor, S.; Esmael, N. The viability of probiotics as a factor influencing the immune response in the Nile tilapia, Oreochromis niloticus. Egypt. J. Aquat. Biol. Fish. 2011, 15, 105–124. [Google Scholar] [CrossRef]
  62. Jahangiri, L.; Esteban, M. Administration of Probiotics in the Water in Finfish Aquaculture Systems: A Review. Fishes 2018, 3, 33. [Google Scholar] [CrossRef]
  63. Chen, M.; Chen, X.-Q.; Tian, L.-X.; Liu, Y.-J.; Niu, J. Improvement of growth, intestinal short-chain fatty acids, non-specific immunity and ammonia resistance in Pacific white shrimp (Litopenaeus vannamei) fed dietary water-soluble chitosan and mixed probiotics. Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol. 2020, 236, 108791. [Google Scholar] [CrossRef] [PubMed]
  64. Hassaan, M.S.; Mohammady, E.Y.; Soaudy, M.R.; Elashry, M.A.; Moustafa, M.M.; Wassel, M.A.; El-Garhy, H.A.; El-Haroun, E.R.; Elsaied, H.E. Synergistic effects of Bacillus pumilus and exogenous protease on Nile tilapia (Oreochromis niloticus) growth, gut microbes, immune response and gene expression fed plant protein diet. Anim. Feed. Sci. Technol. 2021, 275, 114892. [Google Scholar] [CrossRef]
  65. Yaqub, A.; Awan, M.N.; Kamran, M.; Majeed, I. Evaluation of potential applications of dietary probiotic (Bacillus licheniformis SB3086): Effect on growth, digestive enzyme activity, hematological, biochemical, and immune response of Tilapia (Oreochromis mossambicus). Turk. J. Fish. Aquat. Sci. 2022, 223, 5. [Google Scholar] [CrossRef]
  66. Giatsis, C.; Sipkema, D.; Smidt, H.; Verreth, J.; Verdegem, M. The Colonization Dynamics of the Gut Microbiota in Tilapia Larvae. PLoS ONE 2014, 9, e103641. [Google Scholar]
  67. Deng, Y.; Verdegem, M.C.; Eding, E.; Kokou, F. Effect of rearing systems and dietary probiotic supplementation on the growth and gut microbiota of Nile tilapia (Oreochromis niloticus) larvae. Aquaculture 2022, 546, 737297. [Google Scholar] [CrossRef]
  68. Bereded, N.K.; Curto, M.; Domig, K.J.; Abebe, G.B.; Fanta, S.W.; Waidbacher, H.; Meimberg, H. Metabarcoding Analyses of Gut Microbiota of Nile Tilapia (Oreochromis niloticus) from Lake Awassa and Lake Chamo, Ethiopia. Microorganisms 2020, 8, 1040. [Google Scholar] [CrossRef]
  69. Payne, C.J.; Turnbull, J.F.; MacKenzie, S.; Crumlish, M. Investigating the Effect of an Oxytetracycline Treatment on the Gut Microbiome and Antimicrobial Resistance Gene Dynamics in Nile Tilapia (Oreochromis niloticus). Antibiotics 2021, 10, 1213. [Google Scholar] [CrossRef]
  70. Zhai, Q.; Yu, L.; Li, T.; Zhu, J.; Zhang, C.; Zhao, J.; Zhang, H.; Chen, W. Effect of dietary probiotic supplementation on intestinal microbiota and physiological conditions of Nile tilapia (Oreochromis niloticus) under waterborne cadmium exposure. Antonie van Leeuwenhoek Int. J. Gen. Mol. Microbiol. 2017, 110, 501–513. [Google Scholar] [CrossRef]
  71. Mannan, M.; Islam, S.R.; Osman, M.H.; Rahman, M.K.; Uddin, M.N.; Kamal, M.; Reza, S. Antibacterial activity of oxytetracycline on the microbial ecology of Nile tilapia (Oreochromis niloticus) gastrointestinal tract under laboratory conditions. Aquac. Res. 2020, 51, 2125–2133. [Google Scholar] [CrossRef]
  72. Van Doan, H.; Hoseinifar, S.H.; Naraballobh, W.; Jaturasitha, S.; Tongsiri, S.; Chitmanat, C.; Ringø, E. Dietary inclusion of Orange peels derived pectin and Lactobacillus plantarum for Nile tilapia (Oreochromis niloticus) cultured under indoor biofloc systems. Aquaculture 2019, 508, 98–105. [Google Scholar] [CrossRef]
  73. Conlon, M.A.; Bird, A.R. The Impact of Diet and Lifestyle on Gut Microbiota and Human Health. Nutrients 2015, 7, 17. [Google Scholar] [CrossRef]
  74. Wang, A.R.; Ran, C.; Ringø, E.; Zhou, Z.G. Progress in fish gastrointestinal microbiota research. Rev. Aquac. 2018, 10, 626–640. [Google Scholar] [CrossRef]
  75. Li, J.; Liu, G.; Li, C.; Deng, Y.; Tadda, M.A.; Lan, L.; Zhu, S.; Liu, D. Effects of different solid carbon sources on water quality, biofloc quality and gut microbiota of Nile tilapia (Oreochromis niloticus) larvae. Aquaculture 2018, 495, 919–931. [Google Scholar] [CrossRef]
  76. Thirabunyanon, M.; Thongwittaya, N. Protection activity of a novel probiotic strain of Bacillus subtilis against Salmonella Enteritidis infection. Res. Vet. Sci. 2012, 93, 74–81. [Google Scholar] [CrossRef]
  77. Kumar, V.; Roy, S.; Meena, D.K.; Sarkar, U.K. Application of Probiotics in Shrimp Aquaculture: Importance, Mechanisms of Action, and Methods of Administration. Rev. Fish. Sci. Aquac. 2016, 24, 342–368. [Google Scholar] [CrossRef]
  78. Maas, R.M.; Deng, Y.; Dersjant-Li, Y.; Petit, J.; Verdegem, M.C.J.; Schrama, J.W.; Kokou, F. Exogenous enzymes and probiotics alter digestion kinetics, volatile fatty acid content and microbial interactions in the gut of Nile tilapia. Sci. Rep. 2021, 11, 8221. [Google Scholar] [CrossRef]
  79. Cai, G.; Wu, D.; Li, X.; Lu, J. Levan from Bacillus amyloliquefaciens JN4 acts as a prebiotic for enhancing the intestinal adhesion capacity of Lactobacillus reuteri JN101. Int. J. Biol. Macromol. 2020, 146, 482–487. [Google Scholar] [CrossRef]
  80. Yang, J.; Huang, K.; Wang, J.; Wu, D.; Liu, Z.; Yu, P.; Wei, Z.; Chen, F. Combined Use of Bacillus subtilis yb-114,246 and Bacillus licheniformis yb-214,245 Improves Body Growth Performance of Chinese Huainan Partridge Shank Chickens by Enhancing Intestinal Digestive Profiles. Probiotics Antimicrob. Proteins 2020, 13, 327–342. [Google Scholar] [CrossRef]
  81. He, S.; Zhang, Y.; Xu, L.; Yang, Y.; Marubashi, T.; Zhou, Z.; Yao, B. Effects of dietary Bacillus subtilis C-3102 on the production, intestinal cytokine expression, and autochthonous bacteria of hybrid tilapia Oreochromis niloticus Fishes 08 00366 i001 × Oreochromis aureus Fishes 08 00366 i002. Aquaculture 2013, 412–413, 125–130. [Google Scholar] [CrossRef]
  82. Sookchaiyaporn, N.; Srisapoome, P.; Unajak, S.; Areechon, N. Efficacy of Bacillus spp. isolated from Nile tilapia Oreochromis niloticus Linn. on its growth and immunity, and control of pathogenic bacteria. Fish. Sci. 2020, 86, 353–365. [Google Scholar] [CrossRef]
  83. Eladawy, M.M. Characterization of probiotic Bacillus subtilis isolated from Nile tilapia (Oreochromis niloticus) digestive tract and evaluation its positive impact on health and immunity. Egypt. J. Aquac. 2019, 9, 1–26. [Google Scholar] [CrossRef]
  84. Zhang, D.; Gao, Y.; Ke, X.; Yi, M.; Liu, Z.; Han, X.; Shi, C.; Lu, M. Bacillus velezensis LF01: In vitro antimicrobial activity against fish pathogens, growth performance enhancement, and disease resistance against streptococcosis in Nile tilapia (Oreochromis niloticus). Appl. Microbiol. Biotechnol. 2019, 103, 9023–9035. [Google Scholar] [CrossRef] [PubMed]
  85. Tabassum, T.; Sofi Uddin Mahamud, A.G.M.; Acharjee, T.K.; Hassan, R.; Akter Snigdha, T.; Islam, T.; Alam, R.; Khoiam, U.; Akter, F.; Azad, R.; et al. Probiotic supplementations improve the growth, water quality, hematology, gut microbiota, and intestinal morphology of Nile tilapia. Aquac Rep. 2021, 21, 100972. [Google Scholar] [CrossRef]
  86. Das, S.; Ward, L.R.; Burke, C. Screening of marine Streptomyces spp. for potential use as probiotics in aquaculture. Aquaculture 2010, 305, 32–41. [Google Scholar] [CrossRef]
  87. Arun, K.; Madhavan, A.; Sindhu, R.; Emmanual, S.; Binod, P.; Pugazhendhi, A.; Sirohi, R.; Reshmy, R.; Awasthi, M.K.; Gnansounou, E.; et al. Probiotics and gut microbiome—Prospects and challenges in remediating heavy metal toxicity. J. Hazard. Mater. 2021, 420, 126676. [Google Scholar] [CrossRef]
  88. Nayak, S.K. Multifaceted applications of probiotic Bacillus species in aquaculture with special reference to Bacillus subtilis. Rev. Aquac. 2021, 13, 862–906. [Google Scholar] [CrossRef]
  89. Al Masri, S.; Hünigen, H.; Al Aiyan, A.; Rieger, J.; Zentek, J.; Richardson, K.; Plendl, J. Influence of age at weaning and feeding regimes on the postnatal morphology of the porcine small intestine. J. Swine. Health Prod. 2015, 23, 186–203. [Google Scholar]
  90. Shim, K.-Y.; Lee, D.; Han, J.; Nguyen, N.-T.; Park, S.; Sung, J.H. Microfluidic gut-on-a-chip with three-dimensional villi structure. Biomed. Microdevices 2017, 19, 37. [Google Scholar] [CrossRef]
  91. Vallejos-Vidal, E.; Reyes-López, F.; Teles, M.; MacKenzie, S. The response of fish to immunostimulant diets. Fish Shellfish Immunol. 2016, 56, 34–69. [Google Scholar] [CrossRef]
  92. Liu, H.; Wang, S.; Cai, Y.; Guo, X.; Cao, Z.; Zhang, Y.; Liu, S.; Yuan, W.; Zhu, W.; Zheng, Y.; et al. Dietary administration of Bacillus subtilis HAINUP40 enhances growth, digestive enzyme activities, innate immune responses and disease resistance of tilapia, Oreochromis niloticus. Fish Shellfish Immunol. 2017, 60, 326–333. [Google Scholar] [CrossRef]
  93. Panase, A.; Thirabunyanon, M.; Promya, J.; Chitmanat, C. Influences of Bacillus subtilis and fructooligosaccharide on growth performances, immune responses, and disease resistance of Nile tilapia, Oreochromis niloticus. Front. Vet. Sci. 2023, 9, 1094681. [Google Scholar] [CrossRef]
  94. Ismail, T.; Hegazi, E.; Nassef, E.; Habotta, O.A.; Gewaily, M.S. The optimized inclusion level of Bacillus subtilis fermented Azolla pinnata in Nile tilapia (Oreochromis niloticus) diets: Immunity, antioxidative status, intestinal digestive enzymes and histomorphometry, and disease resistance. Fish Physiol. Biochem. 2022, 48, 767–783. [Google Scholar] [CrossRef]
  95. Al-deriny, S.H.; Dawood, M.A.O.; Abou, A.A.; El-tras, W.F.; Ahamad, B.; Van Doan, H.; Mohamed, R.A. The synergistic effects of Spirulina platensis and Bacillus amyloliquefaciens on the growth performance, intestinal histomorphology, and immune response of Nile tilapia (Oreochromis niloticus). Aquac. Rep. 2020, 17, 100390. [Google Scholar] [CrossRef]
  96. Midhun, S.J.; Neethu, S.; Arun, D.; Vysakh, A.; Divya, L.; Radhakrishnan, E.; Jyothis, M. Dietary supplementation of Bacillus licheniformis HGA8B improves growth parameters, enzymatic profile and gene expression of Oreochromis niloticus. Aquaculture 2019, 505, 289–296. [Google Scholar] [CrossRef]
  97. Sutthi, N.; Van Doan, H. Saccharomyces crevices and Bacillus spp. effectively enhance the health tolerance of Nile tilapia under transportation stress. Aquaculture 2020, 528, 735527. [Google Scholar] [CrossRef]
  98. Van Doan, H.; Hoseinifar, S.H.; Khanongnuch, C.; Kanpiengjai, A.; Unban, K.; Van Kim, V.; Srichaiyo, S. Host-associated probiotics boosted mucosal and serum immunity, disease resistance, and growth performance of Nile tilapia (Oreochromis niloticus). Aquaculture 2018, 491, 94–100. [Google Scholar] [CrossRef]
  99. Wang, M.; Yi, M.M.; Lu, M.X.; Gao, F.Y.; Liu, Z.G.; Huang, Q.B.; Li, Q.Y.; Zhu, D.X. Effects of probiotics Bacillus cereus NY5 and Alcaligenes faecalis Y311 used as water additives on the microbiota and immune enzyme activities in three mucosal tissues in Nile tilapia Oreochromis niloticus reared in outdoor tanks. Aquac. Rep. 2020, 17, 100309. [Google Scholar] [CrossRef]
  100. Won, S.; Hamidoghli, A.; Choi, W.; Park, Y.; Jang, W.J.; Kong, I.S.; Bai, S.C. Effects of Bacillus subtilis wb60 and Lactococcus lactis on growth, immune responses, histology and gene expression in nile tilapia, Oreochromis niloticus. Microorganisms 2020, 8, 68. [Google Scholar] [CrossRef]
  101. Saurabh, S.; Sahoo, P.K. Lysozyme: An important defense molecule of the fish’s innate immune system. Aquac. Res. 2008, 39, 223–239. [Google Scholar] [CrossRef]
  102. Gómez, G.D.; Balcázar, J.L. A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol. Med. Microbiol. 2008, 52, 145–154. [Google Scholar] [CrossRef]
  103. Mohammadi, M.; Imani, A.; Farhangi, M.; Gharaei, A.; Hafezieh, M. Replacement of fishmeal with processed canola meal in diets for juvenile Nile tilapia (Oreochromis niloticus): Growth performance, mucosal innate immunity, hepatic oxidative status, liver and intestine histology. Aquaculture 2020, 518, 734824. [Google Scholar] [CrossRef]
  104. Pirarat, N.; Pinpimai, K.; Endo, M.; Katagiri, T.; Ponpornpisit, A.; Chansue, N.; Maita, M. Modulation of intestinal morphology and immunity in nile tilapia (Oreochromis niloticus) by Lactobacillus rhamnosus GG. Res. Vet. Sci. 2011, 91, e92–e97. [Google Scholar] [CrossRef] [PubMed]
  105. Van Doan, H.; Hoseinifar, S.H.; Sringarm, K.; Jaturasitha, S.; Yuangsoi, B.; Dawood, M.A.; Esteban, M.; Ringø, E.; Faggio, C. Effects of Assam tea extract on growth, skin mucus, serum immunity and disease resistance of Nile tilapia (Oreochromis niloticus) against Streptococcus agalactiae. Fish Shellfish. Immunol. 2019, 93, 428–435. [Google Scholar] [CrossRef] [PubMed]
  106. Mokhtar, D.M.; Zaccone, G.; Alesci, A.; Kuciel, M.; Hussein, M.T.; Sayed, R.K.A. Main Components of Fish Immunity: An Overview of the Fish Immune System. Fishes 2023, 8, 93. [Google Scholar] [CrossRef]
  107. Monteiro, S.M.; Fontainhas-Fernandes, A.; Sousa, M. An immunohistochemical study of gill epithelium cells in the Nile tilapia, Oreochromis niloticus. Folia Histochem. Cytobiol. 2010, 48, 112–121. [Google Scholar] [CrossRef]
  108. Lazado, C.C.; Marlowe, C.; Caipang, A. Mucosal immunity and probiotics in fish. Fish Shellfish Immunol. 2014, 39, 78–89. [Google Scholar] [CrossRef]
  109. Rinaldi, E.; Consonni, A.; Guidesi, E.; Elli, M.; Mantegazza, R.; Baggi, F. Gut microbiota and probiotics: Novel immune system modulators in myasthenia gravis? Ann. N. Y. Acad. Sci. 2018, 1413, 49–58. [Google Scholar] [CrossRef]
  110. Wang, X.; Zhang, Y.; Zhang, R.; Zhang, J. The diversity of pattern recognition receptors (PRRs) involved with insect defense against pathogens. Curr. Opin. Insect Sci. 2019, 33, 105–110. [Google Scholar] [CrossRef]
  111. Iwashita, M.K.P.; Nakandakare, I.B.; Terhune, J.S.; Wood, T.; Ranzani-Paiva, M.J.T. Dietary supplementation with Bacillus subtilis, Saccharomyces cerevisiae and Aspergillus oryzae enhance immunity and disease resistance against Aeromonas hydrophila and Streptococcus iniae infection in juvenile tilapia Oreochromis niloticus. Fish Shellfish Immunol. 2015, 43, 60–66. [Google Scholar] [CrossRef]
  112. Akhter, N.; Wu, B.; Memon, A.M.; Mohsin, M. Probiotics and prebiotics associated with aquaculture: A review. Fish Shellfish Immunol. 2015, 45, 733–741. [Google Scholar] [CrossRef]
  113. Chu, H.; Mazmanian, S.K. Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nat. Immunol. 2013, 14, 668–675. [Google Scholar] [CrossRef]
  114. Wolf, A.J.; Underhill, D.M. Peptidoglycan recognition by the innate immune system. Nat. Rev. Immunol. 2018, 18, 243–254. [Google Scholar] [CrossRef]
  115. Irazoki, O.; Hernandez, S.B.; Cava, F. Peptidoglycan Muropeptides: Release, Perception, and Functions as Signaling Molecules. Front. Microbiol. 2019, 10, 500. [Google Scholar] [CrossRef]
  116. Ashraf, R.; Shah, N.P. Immune System Stimulation by Probiotic Microorganisms. Crit. Rev. Food Sci. Nutr. 2014, 54, 938–956. [Google Scholar] [CrossRef]
  117. Roayaei, M.; Mansouri-Tehrani, H.-A.; Rabbani-Khorasgani, M.; Hosseini, S.M.; Mokarian, F.; Mahdavi, H. Effect of supplements: Probiotics and probiotic plus honey on blood cell counts and serum IgA in patients receiving pelvic radiotherapy. J. Res. Med Sci. 2015, 20, 679–683. [Google Scholar] [CrossRef]
  118. Smith, N.C.; Rise, M.L.; Christian, S.L. A Comparison of the Innate and Adaptive Immune Systems in Cartilaginous Fish, Ray-Finned Fish, and Lobe-Finned Fish. Front. Immunol. 2019, 10, 2292. [Google Scholar] [CrossRef] [PubMed]
  119. Opiyo, M.A.; Jumbe, J.; Ngugi, C.C.; Charo-Karisa, H. Different levels of probiotics affect growth, survival and body composition of Nile tilapia (Oreochromis niloticus) cultured in low input ponds. Sci. Afr. 2019, 4, e00103. [Google Scholar] [CrossRef]
  120. Tachibana, L.; Telli, G.S.; de Dias, D.C.; Gonçalves, G.S.; Guimarães, M.C.; Ishikawa, C.M.; Cavalcante, R.B.; Natori, M.M.; Alarcon, M.F.F.; Tapia-Paniagua, S.; et al. Bacillus subtilis and Bacillus licheniformis in diets for Nile tilapia (Oreochromis niloticus): Effects on growth performance, gut microbiota modulation, and innate immunology. Aquac Res. 2021, 52, 1630–1642. [Google Scholar] [CrossRef]
  121. Reda, R.M.; Selim, K.M. Evaluation of Bacillus amyloliquefaciens on the growth performance, intestinal morphology, hematology and body composition of Nile tilapia, Oreochromis niloticus. Aquac. Int. 2015, 23, 203–217. [Google Scholar] [CrossRef]
  122. Ridha, M.T.; Azad, I.S. Preliminary evaluation of growth performance and immune response of Nile tilapia Oreochromis niloticus supplemented with two putative probiotic bacteria. Aquac. Res. 2012, 43, 843–852. [Google Scholar] [CrossRef]
  123. Cruvinel, W.M.; Júnior, D.M.; Araújo, J.A.P.; Catelan, T.T.T.; de Souza, A.W.S.; da Silva, N.P.; da Silva, N.P.; Andrade, L.E.C. Immune system—Part I fundamentals of innate immunity with emphasis on molecular and cellular mechanisms of inflammatory response. Rev. Bras. Reumatol. 2010, 50, 443–461. [Google Scholar]
  124. Ghalwash, H.R.; Salah, A.S.; El-Nokrashy, A.M.; Abozeid, A.M.; Zaki, V.H.; Mohamed, R.A. Dietary supplementation with Bacillus species improves growth, intestinal histomorphology, innate immunity, antioxidative status, and expression of growth and appetite-regulating genes of Nile tilapia fingerlings. Aquac Res. 2022, 53, 1378–1394. [Google Scholar] [CrossRef]
  125. Fath El-Bab, A.F.; Majrashi, K.A.; Sheikh, H.M.; Shafi, M.E.; El-Ratel, I.T.; Neamat-Allah, A.N.F.; El-Raghi, A.A.; Elazem, A.Y.A.; Abd-Elghany, M.F.; Abdelnour, S.A.; et al. Dietary supplementation of Nile tilapia (Oreochromis niloticus) with β-glucan and/or Bacillus coagulans: Synergistic impacts on performance, immune responses, redox status and expression of some related genes. Front Vet. Sci. 2022, 9, 4–9. [Google Scholar] [CrossRef]
  126. Tachibana, L.; Telli, G.S.; Dias, D.D.C.; Gonçalves, G.S.; Ishikawa, C.M.; Cavalcante, R.B.; Natori, M.M.; Ben Hamed, S.; Ranzani-Paiva, M.J.T. Effect of feeding strategy of probiotic Enterococcus faecium on growth performance, hematologic, biochemical parameters and non-specific immune response of Nile tilapia. Aquac. Rep. 2020, 16, 100277. [Google Scholar] [CrossRef]
  127. Mahboob, S. Environmental pollution of heavy metals as a cause of oxidative stress in fish: A review. Life Sci. J. 2013, 10, 336–347. [Google Scholar]
  128. Parkin, J.; Cohen, B. An overview of the immune system. Immunology 2001, 357, 1777–1787. [Google Scholar] [CrossRef]
  129. Giang, J.; Seelen, M.A.J.; Van Doorn, M.B.A.; Rissmann, R.; Prens, E.P.; Damman, J. Complement Activation in Inflammatory Skin Diseases. Front. Immunol. 2018, 9, 639. [Google Scholar] [CrossRef]
  130. Mohammadi, G.; Adorian, T.J.; Federal, U.; Maria, D.S.; Rafiee, G. Beneficial effects of Bacillus subtilis on water quality, growth, immune responses, endotoxemia and protection against lipopolysaccharide-induced damages in Oreochromis niloticus under biofloc technology system. Aquac. Nutr. 2020, 26, 1476–1492. [Google Scholar] [CrossRef]
  131. Ridha, M.T.; Azad, I.S. Effect of autochthonous and commercial probiotic bacteria on growth, persistence, immunity and disease resistance in juvenile and adult Nile tilapia Oreochromis niloticus. Aquac Res. 2015, 47, 2757–2767. [Google Scholar] [CrossRef]
  132. Ismail, T.; Hegazi, E.; Nassef, E.; El-Din, M.T.S.; Dawood, M.A.; Abdo, S.E.; Gewaily, M.S. Gut immune-related gene expression, histomorphometry and hematoimmunological assays in Nile tilapia (Oreochromis niloticus) fed Aspergillus oryzae fermented olive cake. Fish Shellfish Immunol. 2021, 117, 299–310. [Google Scholar] [CrossRef]
  133. Di, J.; Chu, Z.; Zhang, S.; Huang, J.; Du, H.; Wei, Q. Evaluation of the potential probiotic Bacillus subtilis isolated from two ancient sturgeons on growth performance, serum immunity and disease resistance of Acipenser dabryanus. Fish Shellfish. Immunol. 2019, 93, 711–719. [Google Scholar] [CrossRef]
  134. Tan, H.Y.; Chen, S.-W.; Hu, S.-Y. Improvements in the growth performance, immunity, disease resistance, and gut microbiota by the probiotic Rummelii Bacillus stabekisii in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 2019, 92, 265–275. [Google Scholar] [CrossRef] [PubMed]
  135. Foysal, J.; Alam, M.; Kawser, A.Q.M.R.; Hasan, F.; Rahman, M.; Tay, C.; Prodhan, M.S.H.; Gupta, S.K. Meta-omics technologies reveals beneficiary effects of Lactobacillus plantarum as dietary supplements on gut microbiota, immune response and disease resistance of Nile tilapia (Oreochromis niloticus) J. Aquac. 2020, 734974. [Google Scholar] [CrossRef]
  136. Pérez-sánchez, T.; Luis, J.; Merri, D.L.; Carnevali, O.; Gioacchini, G.; De Blas, I.; Ruiz-Zarzuela, I. Expression of immune-related genes in rainbow trout (Oncorhynchus mykiss) induced by probiotic bacteria during Lactococcus garvieae infection. Fish Shellfish Immunol. 2011, 31, 196–201. [Google Scholar] [CrossRef]
  137. Huang, L.; Ran, C.; He, S.; Ren, P.; Hu, J.; Zhao, X.; Zhou, Z. Effects of dietary Saccharomyces cerevisiae culture or live cells with Bacillus amyloliquefaciens spores on growth performance, gut mucosal morphology, hsp70 gene expression, and disease resistance of juvenile common carp (Cyprinus carpio). Aquaculture 2015, 438, 33–38. [Google Scholar] [CrossRef]
  138. Ran, C.; Huang, L.; Hu, J.; Tacon, P.; He, S.; Li, Z.; Xu, L.; Yang, Y.; Zhou, Z. Effects of dietary live and heat-inactive baker’s yeast on growth, gut health, and disease resistance of Nile tilapia under high rearing density. Fish Shellfish Immunol. 2016, 56, 263–271. [Google Scholar] [CrossRef]
  139. Sung, Y.Y.; MacRae, T.H. Heat Shock Proteins and Disease Control in Aquatic Organisms Heat Shock Proteins and Disease Control in Aquatic Organisms. Aquac. Res. Dev. 2015, s2, 2–5. [Google Scholar]
  140. Avella, M.A.; Olivotto, I.; Silvi, S.; Place, A.R.; Carnevali, O. Effect of dietary probiotics on clownfish: A molecular approach to define how lactic acid bacteria modulate development in a marine fish. Am. J. Physiol. Soc. 2010, 298, R359–R371. [Google Scholar] [CrossRef]
  141. Tang, S.; Liu, S.; Zhang, J.; Zhou, L.; Wang, X.; Zhao, Q.; Weng, W.; Qin, J.G.; Chen, L.; Li, E. Relief of hypersaline stress in Nile tilapia Oreochromis niloticus by dietary supplementation of a host-derived Bacillus subtilis strain. Aquaculture 2020, 528, 735542. [Google Scholar] [CrossRef]
  142. Bakhrouf, A.; Mahdhi, A. Effect of dietary supplementation of probiotics and palm fruits extracts on the antioxidant enzyme gene expression in the mucosae of gilthead seabream (Sparus aurata L). Fish Shellfish Immunol. 2014, 39, 532–540. [Google Scholar]
  143. Weydert, C.J.; Cullen, J.J. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat. Protoc. 2009, 5, 51–66. [Google Scholar] [CrossRef] [PubMed]
  144. Article, R.; Bratovcic, A. Antioxidant Enzymes and their Role in Preventing Cell Damage. Acta Sci. Nutr. Health 2020, 4, 1–7. [Google Scholar]
  145. Dawood, M.A.O.; Eweedah, N.M.; Moustafa, E.; Farahat, E.M. Probiotic effects of Aspergillus oryzae on the oxidative status, heat shock protein, and immune-related gene expression of Nile tilapia (Oreochromis niloticus) under hypoxia challenge. Aquaculture 2019, 520, 734669. [Google Scholar] [CrossRef]
  146. Zhou, X.; Tian, Z.; Wang, Y. Effect of treatment with probiotics as water additive on tilapia (Oreochromis niloticus) growth performance and immune response Effect of treatment with probiotics as water additives on tilapia (Oreochromis niloticus) growth performance and immune res. Fish Physiol. Biochem. 2009, 36, 501–509. [Google Scholar] [CrossRef]
  147. Makled, S.O.; Hamdan, A.M.; Fattah, A.; El Sayed, M. Effects of dietary supplementation of a marine thermotolerant bacterium, SO - 1, on growth performance and immune responses of Nile tilapia, Oreochromis niloticus. Aquac. Nutr. 2019, 25, 817–827. [Google Scholar] [CrossRef]
  148. Li, W.; Zhang, X. Effects of Bacillus preparations on immunity and antioxidant activities in grass carp (Ctenopharyngodon idellus). Fish Physiol. Biochem. 2015, 38, 1585–1592. [Google Scholar]
Fishes 08 00366 g001 550
Figure 1. Scheme demonstrating the Bacillus probiotics’ mode of action, Bacillus probiotics protect the intestines against diseases, by making the environment inhospitable for pathogens, compete for vital nutrients and restrict epithelial adhesion sites.
Figure 1. Scheme demonstrating the Bacillus probiotics’ mode of action, Bacillus probiotics protect the intestines against diseases, by making the environment inhospitable for pathogens, compete for vital nutrients and restrict epithelial adhesion sites.
Fishes 08 00366 g001
Fishes 08 00366 g002 550
Figure 2. Interactions between host and microbe in the fish mucosal immune system, host recognizes microbe-associated molecular patterns (MAMPs) found in pathogens and nonpathogenic microorganisms, innate immune signaling molecules generated when MAMPs and PRRs interact on host cells.
Figure 2. Interactions between host and microbe in the fish mucosal immune system, host recognizes microbe-associated molecular patterns (MAMPs) found in pathogens and nonpathogenic microorganisms, innate immune signaling molecules generated when MAMPs and PRRs interact on host cells.
Fishes 08 00366 g002
Table
Table 1. The effect of different Bacillus probiotics on the immune response in Nile tilapia.
Table 1. The effect of different Bacillus probiotics on the immune response in Nile tilapia.
Probiotic NameProbiotic SourceDose (CFU/g) Feeding Duration (Days)Immunological Effects Country of InvestigationReference
B. subtilis HAINUP40Natural pond water10856LYZ (↑ after 2 weeks), RB (↑ after 2 weeks), SOD (↑ after 14 weeks), T-AOC (↑ after 14 weeks)Hainan, China[92]
B. subtilis NZ86 CommercialIndividual 10751LYZ (↓), PG (↔), RB (↔), IL-1β (↔), TNF-α (↔), AH50 (↑ NZ86), LYZ (↑ NZ86)Miami, IL, USA[37]
Bacillus spp.O. niloticus gastrointestinal tract10828NO (↑), IgM (↑), LYZ (↑), AKP (↑), CAT (↑), SOD (↑)Gaozhou, China[49,50]
B. velezensis TPS3N, B. subtilis TPS4, B. amyloliquefaciens TPS17O. niloticus gastrointestinal tract108 individual, 108 + 108 + 108 combined28NO (↑), IgM (↑), LYZ (↑), AKP (↑), ACP (↑), SOD (↑), CAT (↑), MDA (↓)Gaozhou, China [49,50]
B. subtilisCommercial 1 × 108 and 1 × 1010 CFU/kg56IL-1β, TNF-α, IFN-γ, and hsp-70 in the live (↑)Greentech Aquaculture Co. Ltd., Nonthaburi, Thailand[93]
B. subtilis E20Culture collection strain0.3 mL of
108
cells/mL		95Non-specific immunity parameters including LYZ, PG (↑)Cairo, Egypt[94]
B. subtilisCommercial1010 individual180Serum TP (↑), WBCs (↑), LYZ (↑)Sagana, Kenya[38]
B. amyloliquefaciensCulture collection strain2.1×10960LYZ (↑), RB (↑), PG (↑), SOD (↔)Pingtung, Taiwan[52]
B. pumilusO. niloticus107–109120Peripheral blood leukocyte (↑), RB (↑), PG (↑)Bangkok, Thailand[53]
B. subtilisCommercial3 g kg−142TLR-2 (↑), TNF-α (↑), IL-1β (↑), IL-10 (↑), TGFβ (↑), HSP70 (↑)Plymouth, UK[51]
B. amyloliquefaciensCommercial 10960Blood TP (↑), IgM (↑), TNF-α (↑), HSP70 (↓), SOD (↔)Kafr El-Sheikh farm, Kafr al-Shaykh, Egypt[95]
B. licheniformis HGA8BAnabas testudineus gastrointestinal tract106, 10860 MUC 2 (↑), SOD (↑), TLR-2 (↑), IL-10 (↑), TNF-α (↔), IL-8 (↔) GSH-Px (↑), CAT (↑), MPO (↑)Panagad, Kerala, India[96]
B. cereusO. niloticus intestinal tract107, 108 via water42LYZ (↑), peroxidase activity (↑), ACP (↑), SOD (↑)Guangzhou, China[26]
B. subtilis, B. megaterium, and B. licheniformisCulture collection strain106120TNF-α (↑), HSP70 (↑), LYZ (↔)Khon Kaen, Thailand[97]
B. velezensis H3.1O. niloticus intestinal tract10815LYZ (↑ mucus) (↔ serum)Chiang Mai, Thailand [98]
B. cereus NY5O. niloticus intestinal tract104 CFU mL−1 individual via water90SOD (↑ skin)Guangzhou, China[99]
B. subtilis WB60Anguilla japonica intestine108 individual56LYZ (↑), SOD (↑), HSP70 (↑), MPO (↑), IL-1β (↑), IFN-γ (↑), TNF-α (↑)Busan, Republic of Korea[100]
CFU: colony forming unit, LYZ: lysozyme, RB: respiratory burst, SOD: superoxide dismutase, PG: phagocytic activity, NO: nitric oxide, IgM: immunoglobulin M, AKP: alkaline phosphatase, CAT: catalase, ACP: acid phosphatase, MDA: malondialdehyde, WBCs: white blood cells, serum TP: serum protein, blood TP: blood total protein, GHS-Px: glutathione peroxidase, MPO: myeloperoxidase. Symbols are used to explain whether or not the immunological activities were highly significant; i.e., ↑: significant increase, ↓: significant decrease, ↔: no significant changes.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Shija, V.M.; Amoah, K.; Cai, J. Effect of Bacillus Probiotics on the Immunological Responses of Nile Tilapia (Oreochromis niloticus): A Review. Fishes 2023, 8, 366. https://doi.org/10.3390/fishes8070366

AMA Style

Shija VM, Amoah K, Cai J. Effect of Bacillus Probiotics on the Immunological Responses of Nile Tilapia (Oreochromis niloticus): A Review. Fishes. 2023; 8(7):366. https://doi.org/10.3390/fishes8070366

Chicago/Turabian Style

Shija, Vicent Michael, Kwaku Amoah, and Jia Cai. 2023. "Effect of Bacillus Probiotics on the Immunological Responses of Nile Tilapia (Oreochromis niloticus): A Review" Fishes 8, no. 7: 366. https://doi.org/10.3390/fishes8070366

Article Metrics

Back to TopTop