Importance of Probiotics in Fish Aquaculture: Towards the Identification and Design of Novel Probiotics
Abstract
:1. Introduction
2. Probiotics
2.1. Probiotics in Aquaculture
Species/Size | Bacteria/Prebiotic | Pathogen (Challenge) | Oral Doses | Effects | Ref. |
---|---|---|---|---|---|
Pike-perch (S. lucioperca)/Juvenile (Larvae) | L. paracasei BGHN14 L. rhamnosus BGT10 L. reuteri BGGO6–55 L. salivarius BGHO1, OTOHIME fish diet Artemia nauplii | Fish diet: non-enriched A. nauplii per 5 day (300 nauplii per larvae per day) + 14 days of enriched diets (8 to 14 g per tank per day, 80 L/tank). Groups:
| ↗ Better skeletal development. ↗ Higher trypsin to chymotrypsin activity ratio values. ↘ Lower levels of Aeromonas and Mycobacterium spp. | [23] | |
Turbot (Scophthalmus maximus)/95.8 ± 17.7 g |
| Fish diet: Hand fed twice daily for 84 days A basal low fish meal (FM; 32%) diet supplemented with:
| ↘ Reduction of cholesterol levels. No changes in innate immune response. No changes in lysozyme activity in plasma. | [24] | |
Rohu (L. rohita)/ 43 ± 1.07 g | B. subtilis VSG1, Pseudomonas aeruginosa VSG2, and L. plantarum VSG3 | A. hydrophila | Immunized intraperitoneally: 0.1 mL phosphate buffer solution (PBS) containing 0.1 mg of any of the following cellular components: intercellular products (ICPs) of B. subtilis VSG1, ICPs of L. plantarum VSG3, and heat-killed whole cell products of P. aeruginosa VSG2 | ↗ Intercellular products of L. plantarum VSG3. ↗ Higher post challenge relative percent survival (83.32%). ↗ Increase in ACP activity and induction of IL-1β and TNF-α expression. | [25] |
Nile tilapia (O. niloticus)/3.83 ± 0.03 g | B. licheniformis | Streptococcus iniae | B. licheniformis (0%, 0.02%, 0.04%, 0.06%, 0.08% and 0.1% of AlCare®, containing live germ 2 × 1010 CFU/g)/twice daily fed for 10 weeks | ↗ Improve the growth performance, enhance immunity by ↗ increasing the content of complement C3 in serum and lysozyme activity. | [26] |
Turbot (S. maximus L.)/1.98 ± 0.17 g | L. mesenteroides subsp. cremoris SMM69 and W. cibaria P71 | V. splendidus CECT528 V. splendidus ATCC25914 and V. splendidus DMC-1 | Bathed with suspensions of bacteria at 1 × 109 CFU/mL during 1 h at 18 °C twice: 0 and 24 h. | ↗ Strong antimicrobial activity against T. maritimum and V. splendidus. Different adhesion ability to skin mucus. ↗ Inhibit the adhesion of turbot pathogens to mucus. ↗ Stimulation of genes encoding IL-1β, TNF-α, lysozyme, C3, MHC-Iα and MHC-IIα in five organs (head-kidney, spleen, liver, intestine and skin). | [29] |
European Sea bass (Dicentrarchus labrax)/13.23 ± 0.18 g | Organic acids and natural identical compounds providing 25% citric acid, 16.7% sorbic acid, 1.7% thymol and 1% vanillin in a matrix of hydrogenated fats. | Feed was provided by hand/twice a day/6 days a week. | ↗ Stimulation of the development of beneficial bacteria taxa such as Lactobacillus, Leuconostoc, and Bacillus spp. ↗ Dose-dependent upregulation of IL-8, IL-10 and TGF-β. | [32] | |
Atlantic salmon (S. salar)/~32 g | 1,3/1,6-beta glucans, mannan-oligosaccharides, nucleic acids, nucleotides, medium chain fatty acids and single chain fatty acid. | Fed by hand 4 times/day, during 0, 6 and 12 weeks. Experimental blend containing prebiotics at 0, 0.5, 1, 2 g/kg in fish formulation. | Changes in gut and skin microbial community of salmon. ↗ Enrichment of Bacillus and Mycoplasma spp. species. | [33] | |
Nile tilapia (O. niloticus)/9.2 ± 0.1 g | β-glucans | Groups 1. 30 days of standard diet + 15 days of β-glucan. 2. 15 days of standard diet + 30 days of β-glucan diet. 3. 45 days of 0.1% β-glucan. Endpoint: 7 and 14 days post-feeding trial. | ↗ Improvement of lysozyme activity in plasma, liver and intestine. | [34] | |
Nile tilapia (O. niloticus)/27.15 ± 0.2 g | A. oryzae and β-glucan | Fed 60 days 1. Standard diet 2. A. oryzae (1 g/kg) 3. β-glucan (1 g/kg) 4. 0.5 g/kg of A. oryzae + 0.5 g/kg of β-glucan | ↗ Fish growth improvement ↗ Enhanced immune response by increase of IgM and lysozyme activities. | [36] | |
Nile tilapia (O. niloticus)/16.57 ± 0.14 g | Dietary watermelon rind powder (WMRP) and L. plantarum CR1T5 (LP) | S. agalactiae | Fish diets: 1. Standard diet 2. 40 g/kg of WMRP 3. 108 CFU/g of LP 4. 40 g/kg of WMRP plus 108 CFU/g of LP. Fish were hand-fed ad libitum twice daily during 8 weeks. | ↗ Higher lysozyme and peroxidase elevation in skin mucus and serum. ↗ Phagocytosis and alternative complement (ACH50) activities. ↗ The relative percent survival of 68% in S. agalactiae challenge. | [38] |
Nile tilapia (O. niloticus)/15–20 g | Bacillus subps. NP5 | S. agalactiae | Fed 3 times/day/14 days before challenge. Diet: 1 g of probiotic (Bacillus NP5 at 1 × 106 CFU/mL) and 2 g of prebiotic per 100 g of feed (oligosaccharides from sweet potatoes var. sukuh). | ↗ Fish survival rate of 85.19% (control fed 18.52%). ↘ Level of damage by S. agalactiae in kidney and liver. | [39] |
Red tilapia (Oreochromis spp.)/14.05 ± 0.42 g | Jerusalem artichoke (H. tuberosus) and L. rhamnosus GG (LGG) | A. veronii | Fish diet: Fish were hand-fed/twice day/30 days. 1. Standard diet. 2. 10 g/kg of Jerusalem artichoke (H. tuberosus) + 108 CFU/g LGG). | ↗ Growth performance by 106%. ↗ Enhanced blood glucose, total protein and total cholesterol levels. ↗ Enhanced intestinal parameters (villous height, absorptive area and globet cells) No changes of survival rate in A. veronii challenge. | [40] |
2.2. Microbial Metabolites Produced by Probiotics and Intestinal Microbiota
2.3. Fish Microbiota and Natural Anti-α-Gal Antibodies Induced by Probiotics
3. Recombinant Probiotics in Aquaculture
4. Future Perspectives of Recombinant Probiotics in Aquaculture
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
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Species/Size | Bacteria | Vector (a,b,c) | Immunostimulant Peptide | Pathogen | Oral Dosis | Effects | Ref. |
---|---|---|---|---|---|---|---|
Rainbow trout (O. mykiss)/100 g | L. casei ATCC 393 | pG1-VP2 (Pxyl a, ssUSP b, pgsA c), pG2-VP2 (Pxyl a, ssUSP b) pG1-VP3 (Pxyl a, ssUSP b, pgsA c), pG2-VP3 (Pxyl a, ssUSP b) | VP2, VP3 | IPNV | 5 × 108 CFU (once) | Anti-IPNV IgM increased 5 to 10-fold 31 days post immunization. Presence of neutralizing antibodies in serum 63 days post immunization. Up to 40-fold reduction of viral load in the spleen 10 days post-challenge. The challenge was performed on day 66 post-immunization. | [125] |
Rainbow trout (O. mykiss)/100 g | L. casei ATCC 393 | pG1-VP2-3 (Pxyl a, ssUSP b, pgsA c), pG2-VP2-3 (Pxyl a, ssUSP b) | VP2-VP3 fusion | IPNV | 5 × 108 (once) | Presence of neutralizing antibodies in serum on day 63 post immunization. Anti-IPNV IgM increased 6- to 10-fold 31 days post immunization. Up to 10-fold reduction of viral load in the spleen 10 days post-challenge. The challenge was performed on day 66 post-immunization. | [126] |
Rainbow trout (O. mykiss)/11.5 g | L. casei ATCC 393 | pPG-612-CK6-VP2 (Constitutive a, ssUSP b) | CK6-VP2 | IPNV | 1 × 1010 (once) | CK6 expressed in Lactobacillus is biologically functional in vitro, increasing lymphocyte migration, inducing expression of IL-8, IL-1β and TNF-α. In vivo pPG-612-CK6-VP2 increase expression of IL-8, IL-1β, TNF-α, β-defensin, Mx, MHC-II, and CK6 in the first four days after administration. Increase in IgT and IgM titer by up to 10 times 31 days post immunization. Increase in neutralizing antibodies against IPNV. | [127] |
Rainbow trout (O. mykiss)/10 g | L. casei ATCC 393 | pPG-612-AHA1-CK6-VP2 (Pxyl a, ssUSP b) | AHA1-CK6-VP2 | IPNV | 2 × 109 for 3 days, then booster on days 31, 32 and 33 | AHA1-CK6 is biologically functional in vitro, increasing lymphocyte migration, inducing expression of IL-8, IL-1β and TNF-α. In vivo pPG- 612- AHA1-CK6-VP2 increase expression of IL-8, IL-1β, TNF-α, β-defensin, Mx, MHC-II, and CK6 in the first four days after administration. Increase in IgT and IgM titer by up to 15 times 31 days post immunization. Increase in neutralizing antibodies against IPNV. Reduced IPNV load. | [128] |
Rainbow trout (O. mykiss)/15 g | L. casei ATCC 393 | pPG-612-CK6-VP2-eGFP (Pxyl a, ssUSP b) | CK6-VP2-eGFP | IPNV | 2 × 109 for 3 days, then booster on days 31, 32 and 33 | Increase in IgT and IgM titer by up to 5 times 15 days post primary immunization. Increase in neutralizing antibodies against IPNV. Reduced IPNV load | [129] |
Rainbow trout (O. mykiss)/7 ± 0.65 g | L. lactis NZ3900 | pNZ8148-G (pNZ8148 Pnis a) | VHSV G | VHSV | Fed 3% daily. 108 to 1010 CFU/g of feed for seven days and then boosted for one week in the third week | Induce IFN-α in the second week. Increase in IgM in serum after two weeks. Titers remain high until day 60. Reduced mortality by around 3-fold (from 60% to 20%). Reduced viral load in spleen and head-kidney. Increase the percent of weight gain (PWG) and reduced food conversion rate (FCR) | [130] |
Olive flounder (P. olivaceus)/35 ± 5 g | L. lactis NZ9000 | pSLC-G (pNZ8148, Pnis a, SP-Usp45 b, acmA c) | HIRRV-G gene | HIRRV | 1.0 × 109 CFU/g diet, fed 1–2% each day. Supplemented food was administered for 7 days during weeks 1 and 5. | Increase in IgM titer against HIRRV in serum (after 4 weeks) and gut mucus (after 2 weeks). Serum IgM requires booster. Reduced viral load. Duplicated survival after challenge (70% vs. 35% in control). | [131] |
Common carp (C. carpio)/56 ± 1 g | L. casei CC16 (Strain isolated from the common carp gut microbiota) | pPG1(Pxyl a, ssUSP b, pgsA c) pPG2 (Pxyl a, ssUSP b) | OmpW | A. veronii | Fed daily at 1%. 1 × 109 CFU/g of feed for three days, and then booster of another 3 days after two weeks | Increase in OmpW-specific IgM antibody two weeks post immunization. Increase in lysozyme, acid phosphatase, alkaline phosphatase, and superoxide dismutase activity in blood. Increase in phagocytic activity in serum. Induced expression of IL-1β, IL-10, IFN-γ, and TNF-α in spleen, head-kidney and gut. Increase in survival from 0 to 50% after challenge with A. veroni TH0426 | [132] |
Common carp (C. carpio)/50 ± 1 g | L. casei CC16 (Strain isolated from the common carp gut microbiota) | pPG1(Pxyl a, ssUSP b, pgsA c) pPG2 (Pxyl a, ssUSP b) | OmpAI | A. veronii TH0426 | Feeding rate 1% body weight. Immunization with 2 × 109 CFU/g of feed for three days starting on day 1 and 31 (booster) | Increase in OmpAI-specific IgM antibodies in serum and skin mucose 15 days post immunization. Increase in lysozyme, acid phosphatase, alkaline phosphatase, and superoxide dismutase activity in blood after booster. Induced expression of IL-10, TNF-α in spleen, head-kidney and intestine. Induced expression of IL-1β, IFN-γ in spleen, head-kidney, gills, and intestine. Increase in survival from 0 to 50–70% after challenge with A. veroni TH0426 | [133] |
Common carp (C. carpio)/~60 g | L. casei CC16 (Strain isolated from the common carp gut microbiota) | pPG-Aha1 (Pxyl a, ssUSP b, pgsA c) pPG-Aha1-CTB (Pxyl a, ssUSP b, pgsA c) | Aha1 CTB (Cholera toxin B-subunit) Aha-CTB | A. veronii TH0426 | 1 × 109 CFU/g, days 1–3, 1st booster days 15–17, 2nd booster days 29–31. Challenge day 36 | Recombinant strains stimulate IgM, acid phosphatase (ACP), alkaline phosphatase (AKP), C3, C4, lysozyme (LZM), Lectin and superoxide dismutase (SOD). Upregulate expression of: Interleukin-10 (IL-10), Interleukin-1β (IL-1β), Tumor Necrosis Factor-α (TNF-α), immunoglobulin Z1 (IgZ1) and immunoglobulin Z2 (IgZ2). Colonization of fish intestine. Confers protection against A. veronii infection; pPG-Aha1-CTB/Lc CC16 and pPG-Aha1/Lc CC16 shows relative percent survival (RPS) of 64.29% and 53.57%, respectively. | [134] |
Common carp (C. carpio)/250 ± 2.5 g | L. casei CC16 (Strain isolated from the common carp gut microbiota) | pPG-Aha1, (Pxyl a, ssUSP b, pgsA c) pPG-Aha1-LTB (Pxyl a, ssUSP b, pgsA c) | Aha1 LTB (E. coli intolerant enterotoxin B subunit) Aha1-LTB | A. veronii TH0426 | Carps were immunized orally by feeding fish food (2%) twice daily for three days, then booster at day 14. | Increase in specific IgM in serum, and in activities of ACP, AKP, SOD, LYS, C3, C4, and lectin. Increase in expression of IL-10, IL-1β, TNF-α, IgZ1, and IgZ2 in the liver, spleen, kidney, intestines, and gill tissues. Improved survival in fish challenged with A. veronii (60.71%). | [135] |
Common carp (C. carpio)/50 ± 0.1 g | L. casei CC16 (Strain isolated from the common carp gut microbiota) | pPG1-Aha1 (Pxyl a, ssUSP b, pgsA c) pPG2-Aha1 (Pxyl a, ssUSP b, pgsA c) | Aha1 (A. hydrophila) | A. hydrophila BSK-10 | Feeds containing 1 × 109 CFU/g. The fish were orally immunized on day 1 to day 3, and reinforced posterior to 14 days (i.e., day 18–20). | Stimulate level of antibodies and AKP, ACP, SOD, LZM, C3, C4 in serum. Upregulate IL-10, IL-1β, TNF-α, IFN-γ in the livers, spleens, HK, and intestines. Increase in phagocytosis and survival rate (60–50%) after challenge with A. hydrophila. | [136] |
Common carp (C. carpio)/200 ± 20 g | L. plantarum | pYG | SVCV-G | SVCV | Immunization with 1 × 109 CFU/g of fed for three days on day 1, 10 (booster I) and 28 (booster II). Covered with alginate | Increase in anti-SVCV-G specific IgM antibodies in serum 14 days post primary immunization. Increase in survival from 0 to 80% in challenge assays. Increase in neutralizing antibodies | [137] |
Common carp (C. carpio)/500 ± 50 g | L. plantarum | pYG-G (pYG301 derived, Pxyl a, wall anchor motif from Streptococcus pyogenes M6 protein c) | SVCV-G and KHV ORF81 | SVCV KHV | Immunization with 3 × 109 CFU/g of feed for three days on day 1, 14 (booster I) and 28 (booster II) | Increase in anti-SVCV-G IgM and anti-KHV-ORF81 IgM levels 14 days post primary immunization. Increase in neutralizing antibodies against SVCV and KHV. Reduced mortality caused by SVCV and KHV by 10% respect to fish fed with L. plantarum | [138] |
Common carp (C. carpio)/5.05 ± 0.53 g | L. lactis NZ9000 | pNZ-UGA (pNZ8148, Pnis a, SP-Usp45 b, acmA c) | SVCV glycoprotein | SVCV | Intramuscular injection of 5 µg protein from culture | Induced IgM in serum 7 days post immunization. Induced TNF-α, IL-6b, IL-1β, Cxcr-1, IFN-γ, IFN-α and IgM. Increase in survival 8–9-fold. Reduced viral load | [139] |
Crucian carp (C. carassius)/50 ± 1 g | L. casei CC16 (Strain isolated from the common carp gut microbiota) | pPG1(Pxyl a, ssUSP b, pgsA c) pPG2 (Pxyl a, ssUSP b) | OmpAI-C5-I | A. veronii TH0426 | Feeding rate 1% body weight. Immunization with 2 × 109 CFU/g of fed for three days starting on day 1 and 31 (booster) | Increase in OmpAI-C5-I specific IgM antibodies in serum 16 days post immunization. Increase in lysozyme, acid phosphatase, alkaline phosphatase, and superoxide dismutase activity in blood after booster. Increase in phagocytic activity in serum. Induced expression of IL-10 in liver, spleen, kidney and intestine, Induced IL-1β, TNF-α, and IFN-γ in heart, liver spleen, kidney and intestine. Increased survival from 0 to 65–75% after challenge with A. veroni TH0426. | [140] |
Goldfish (C. auratus)/50 ± 5 g | L. casei ATCC393 | pPG-OmpK, (Pxyl a, ssUSP b, pgsA c) pPG-OmpK-CTB (Pxyl a, ssUSP b, pgsA c) | OmpK CTB (Cholera toxin B-subunit) OmpK-CTB | V. mimicus Hsy0531-k | 108 CFU/mL, mixed with commercial fish food First oral vaccination days 1–3, 2nd vaccination days 15–17, and 3rd vaccination days 29–31. | Lc-pPG-OmpK-CTB stimulated levels of IgM, and activity of acid phosphatase (ACP), alkaline phosphatase (AKP), superoxide dismutase (SOD), lysozyme (LYS), lectin, C3, and C4. Increase in expression of interleukin-1β (IL-1β), interleukin-10 (IL-10), tumor necrosis factor-α (TNF-α), and transforming growth factor-β (TGF-β) in the liver, spleen, head kidney, hind intestine and gills. Colonization of the intestine and increase in survival after challenge (58.33%). | [141] |
Crucian carp (C. carassius)/65 ± 4 g | L. plantarum Lp-095 | pPG-Malt-pgsA (Pxyl a, ssUSP b, pgsA c) | Malt (Maltoporin) | A. hydrophila | Food supplemented with 109 CFU/g. Fish were fed twice daily for 28 days without interruption. | Enhanced IgM level and phagocytic activity. Increase in expression of IL-10, IL-1β, TNF-α, IFN-γ in liver, spleen, head kidney and hind intestine. Increase in RPS of fish challenged intraperitoneal with A. hydrophila (55%). | [142] |
Nile tilapia (O. niloticus)/15 ± 2 g | L. lactis NZ9000 | pNZ8148-sip (pNZ8148 Pnis a) | Surface immunogenicity protein (Sip) | S. agalactiae | 2 × 108–2 × 1010 CFU/fish | Increase in Sip specific IgM antibodies in serum 16 days post primary immunization. Increase in survival from 5 to 60% in challenge assays. Induced expression of IgT, IgM, CD8a and C3 in liver, spleen, intestine and thymus | [143] |
Goldfish (C. auratus) | L. plantarum NC8 | pSIP409-IAG-52X (pSIP409, Pspp a) | IAG-52X | I. multifiliis | Fed 1% with 106 CFU/g of feed, for 4 weeks | Increase in Ig in serum and skin after four weeks of feed. Increase in survival from 40 to 60% in challenge assays. Induced C3, IgM and MHC-I after 2 weeks of feed. | [144] |
Rainbow trout (O. mykiss)/25 g | L. lactis NZ3900 | pNZ8149 (Pnis a, Usp45 b) | Interferon II (Atlantic salmon) | F. psychrophilum | 1 × 107 CFU/fish each day for one week | Induced expression of IFN-γ, IP10, IL-6, STAT1 and IL-1β Increase in serum lysozyme activity Increase in survival from 50% to 80% in challenge assays | [145] |
Atlantic salmon (S. salar)/10 g | L. lactis NZ3900 | pNZ8149 (Pnis a, Usp45 b) | Interferon Ia (Atlantic salmon) | IPNV | 1 × 107 CFU/fish each day for one week | Induced expression of Mx and PKR in spleen and head kidney. Reduced viral load in spleen and head kidney | [146] |
Nile tilapia (O. niloticus)/~100 g | Bacillus isolate B29 (Related to Bacillus subtilis) | pBESOn-CC (P aprE a, AprE SP b) | CC-Chemokine (Nile tilapia) | 1 × 108 CFU/kg of feed. Fish were fed ad libitum twice daily for 30 days | Increase in immunoglobulin, complement and lysozyme activity. Improved phagocytic activity. | [147] | |
Zebrafish (D. rerio)/50 mg | L. lactis ZHY1 | pMG36e-usp45-AcmA-AM (P32 a, Usp45 b, acmA c) | pili-like protein Amuc_1100 | High-fat diet 108 CFU/g. The zebrafish were fed two times a day at 6% of body weight, for 4 weeks | Reduced hepatic steatosis in zebrafish. Downregulated expression of the lipogenesis [peroxisome-proliferator-activated receptors (PPARγ), sterol regulatory element-binding proteins-1c (SREBP-1c), fatty acid synthase (FAS), and acetyl-CoA carboxylase 1 (ACC1)] and lipid transport genes (CD36 and FABP6) in the liver. Reduced serum aspartate aminotransferase (AST) and alanine aminotransferase (ALT) levels. Decrease in expression of tumor necrosis factor (TNF)-α and interleukin (IL)-6 in the liver. Increase in expression of intestinal tight junction (TJ) proteins (TJP1a, claudina, claudin7, claudin7b, claudin11a, claudin12, and claudin15a. Reduced Proteobacteria and Fusobacteria. | [148] | |
Zebrafish (D. rerio)/0.082 ± 0.002 g | B. subtilis wt55 | pDG364-N-AIO6 (CotC a,b,c) | AiiO-AIO6 (Lactonase) | A. veronii Hm091 | 108 CFU/g feed. Fish were fed at 6% of body weight per day, increased by 1% after a week, for two weeks. | Improved survival rate. Reduced number of invasive A. veronii in gut after challenge. Reduced intestinal alkaline phosphatase activity. Reduced expression of nuclear factor kappa-B (NF-κB) and proinflammatory cytokine interleukin-1β (IL-1β). Increase in expression of lysozyme gene. | [149] |
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Torres-Maravilla, E.; Parra, M.; Maisey, K.; Vargas, R.A.; Cabezas-Cruz, A.; Gonzalez, A.; Tello, M.; Bermúdez-Humarán, L.G. Importance of Probiotics in Fish Aquaculture: Towards the Identification and Design of Novel Probiotics. Microorganisms 2024, 12, 626. https://doi.org/10.3390/microorganisms12030626
Torres-Maravilla E, Parra M, Maisey K, Vargas RA, Cabezas-Cruz A, Gonzalez A, Tello M, Bermúdez-Humarán LG. Importance of Probiotics in Fish Aquaculture: Towards the Identification and Design of Novel Probiotics. Microorganisms. 2024; 12(3):626. https://doi.org/10.3390/microorganisms12030626
Chicago/Turabian StyleTorres-Maravilla, Edgar, Mick Parra, Kevin Maisey, Rodrigo A. Vargas, Alejandro Cabezas-Cruz, Alex Gonzalez, Mario Tello, and Luis G. Bermúdez-Humarán. 2024. "Importance of Probiotics in Fish Aquaculture: Towards the Identification and Design of Novel Probiotics" Microorganisms 12, no. 3: 626. https://doi.org/10.3390/microorganisms12030626