The Microbial Population of the Gastrointestinal Tract of Animals: Impacts on Host Physiology

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Gut Microbiota".

Deadline for manuscript submissions: closed (20 November 2022) | Viewed by 35074

Special Issue Editors


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Guest Editor
Department of Animal and Dairy Science, University of Georgia, Athens, GA, USA
Interests: microbial ecology; microbial physiology; preharvest food safety; gastrointestinal microbiology; antimicrobial resistance; rumen microbiome

E-Mail Website
Guest Editor
Department of Animal and Dairy Science, University of Georgia, Athens, GA, USA
Interests: animal science; bioinformatics; biostatistics; metagenomics; microbiome; nutrition; ruminants

Special Issue Information

Dear Colleagues,

The gastrointestinal microbial ecosystem of food animals is very diverse, complex, and interdependent and can include bacteria, protozoa, fungi, and viral members that act as a consortium to degrade digesta and produce end products that have significant impacts on host energetic status and can include toxins and vitamins that can impact host health. Some microbial effects on host physiology can impact animal production and production efficiency, but the microbial ecosystem can lead to changes in the host that might lead to increased multiplication and penetration of potential pathogens that impact animal health, as well as food safety. Next-generation sequencing and bioinformatics approaches have allowed us to determine the microbial population of the gut of animals more precisely, but we have not developed a complete picture of the interactions between the microbiome and host physiology. This Special Issue of Microorganisms is designed to bring knowledge of how the microbial population (and their end products) can impact host animal physiology and how that impacts animal (and human) health, growth, production, and ultimately safety.

Dr. Todd Callaway
Dr. Jeferson M. Lourenco
Guest Editors

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Published Papers (12 papers)

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Editorial

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3 pages, 166 KiB  
Editorial
Editorial: Impact of Special Issue “The Microbial Population of the Gastrointestinal Tract of Animals: Impacts on Host Physiology”
by Jeferson M. Lourenco and Todd R. Callaway
Microorganisms 2024, 12(5), 859; https://doi.org/10.3390/microorganisms12050859 - 25 Apr 2024
Viewed by 561
Abstract
In recent years, there has been an exponential increase in the number of papers that have investigated the microbiome of animals and humans [...] Full article

Research

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17 pages, 3475 KiB  
Article
Metagenomic Sequencing Reveals the Taxonomic and Functional Characteristics of Rumen Micro-organisms in Gayals
by Huan Gao, Ye Yu, Yaqi Lv, Deao Wang, Haonan Li, Zhe Li, Yuchen Zhang, Lan Chen and Jing Leng
Microorganisms 2023, 11(5), 1098; https://doi.org/10.3390/microorganisms11051098 - 22 Apr 2023
Cited by 1 | Viewed by 1642
Abstract
As a semi-wild breed, Gayals have a strong fiber degradation capacity, which is unique to the microbial structure and function of their rumen. In this study, the unique rumen microbial composition and function of Gayals were investigated by metagenomic sequencing, with the Yunnan [...] Read more.
As a semi-wild breed, Gayals have a strong fiber degradation capacity, which is unique to the microbial structure and function of their rumen. In this study, the unique rumen microbial composition and function of Gayals were investigated by metagenomic sequencing, with the Yunnan yellow cattle as the control. We compared the differences in rumen micro-organisms between Gayals and the Yunnan Yellow cattle, and the results showed that there were differences in bacteria, archaea and fungi between Gayals and the Yunnan Yellow cattle, while no significant abundance changes were observed in the protozoa. In addition, the ratio of Firmicutes to Bacteroidetes (1.06) in Gayals was higher than that of the Yunnan Yellow cattle (0.66). Three enzymes (PTA, ACH and FTHFS) related to the acetate production pathway and five enzymes (BHBD, THL, PTB, BK and BCACT) involved in butyric acid production were annotated in this study. The CAZymes search results showed that the abundance of GH5, GH26, GH94, CBM11 and CBM63 in Gayals was higher than in the Yunnan Yellow cattle (p < 0.05). Furthermore, this research constructed a model of rumen micro-organisms degrading fibers according to the characteristics and differences in the rumen microbiota structures and functions of the two breeds. This study expands our knowledge of the rumen microbiota and the mechanisms of fiber degradation in Gayals. Full article
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10 pages, 1587 KiB  
Article
Establishment of the Bacterial Microbiota in a Lab-Reared Model Teleost Fish, the Medaka Oryzias latipes
by Charlotte Duval, Benjamin Marie, Pierre Foucault and Sébastien Duperron
Microorganisms 2022, 10(11), 2280; https://doi.org/10.3390/microorganisms10112280 - 17 Nov 2022
Cited by 6 | Viewed by 1904
Abstract
Oryzias latipes is an important model organism for physiology, genetics, and developmental studies, and has also emerged as a relevant vertebrate model for aquatic ecotoxicology. Knowledge regarding its associated microbiota on the other hand is still scarce and limited to adults, despite the [...] Read more.
Oryzias latipes is an important model organism for physiology, genetics, and developmental studies, and has also emerged as a relevant vertebrate model for aquatic ecotoxicology. Knowledge regarding its associated microbiota on the other hand is still scarce and limited to adults, despite the relevance of the associated microbiome to the host’s biology. This study provides the first insights into the establishment of bacterial microbiota during early developmental stages of laboratory-reared medaka using a 16S-rRNA-sequencing-based approach. Major shifts in community compositions are observed, from a Proteobacteria-dominated community in larvae and juveniles to a more phylum-diverse community towards adulthood, with no obvious difference between female and male specimens. Major bacterial taxa found in adults, including genera Cetobacterium and ZOR0006, establish progressively and are rare during early stages. Dominance shifts are comparable to those documented in another major model teleost, the zebrafish. Results from this study provide a basis for future work investigating the influence of medaka-associated bacteria during host development. Full article
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14 pages, 2384 KiB  
Article
Comparative Analyses of the Exopalaemon carinicauda Gut Bacterial Community and Digestive and Immune Enzyme Activity during a 24-Hour Cycle
by Shumin Xie, Runyao Liu, Huiling Zhang, Fei Yu, Tingting Shi, Jiawei Zhu, Xinlei Zhou, Binlun Yan, Huan Gao, Panpan Wang and Chaofan Xing
Microorganisms 2022, 10(11), 2258; https://doi.org/10.3390/microorganisms10112258 - 14 Nov 2022
Cited by 1 | Viewed by 1527
Abstract
The change in life activities throughout a cycle of approximately 24 h is called the circadian rhythm. Circadian rhythm has an important impact on biological metabolism, digestion, immunity, and other physiological activities, but the circadian rhythm of crustaceans has rarely been studied. In [...] Read more.
The change in life activities throughout a cycle of approximately 24 h is called the circadian rhythm. Circadian rhythm has an important impact on biological metabolism, digestion, immunity, and other physiological activities, but the circadian rhythm of crustaceans has rarely been studied. In this study, the activity of digestive enzymes (α-amylase, trypsin, and lipase) and immune enzymes (superoxide dismutase, lysozyme, and catalase), as well as the circadian rhythm of the intestinal bacterial community of Exopalaemon carinicauda, were studied. The results showed that the digestive and immune enzyme activities of E. carinicauda changed significantly (p < 0.05) at four time points throughout the day by one-way ANOVA analysis, with the highest value at 24:00 and the lowest value at 12:00. The highest values of alpha diversity and richness were observed in the 24:00 samples, which were significantly higher than those in the other groups (p < 0.05). The principal coordinate analysis (PCoA) results obviously showed that the samples from the same sampling time had higher similarity in the bacterial community structure. Candidatus hepatoplasma had the highest abundance among the intestinal microorganisms at 24:00, and Marinomonas had the highest abundance at 12:00. This study contributed to the understanding of digestive enzyme activity, immune enzyme activity, and the circadian rhythm of the intestinal bacterial community structure in E. carinicauda. It will play an important role in optimizing feeding times and improving digestion and nutrient utilization for E. carinicauda. The results of this study provide a basis for further study on the physiological mechanism of diurnal variation of intestinal flora in crustaceans. Full article
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19 pages, 2827 KiB  
Article
Genomic and Biochemical Characterization of Bifidobacterium pseudocatenulatum JCLA3 Isolated from Human Intestine
by Raquel González-Vázquez, Eduardo Zúñiga-León, Edgar Torres-Maravilla, Martha Leyte-Lugo, Felipe Mendoza-Pérez, Natalia C. Hernández-Delgado, Ricardo Pérez-Pastén-Borja, Alejandro Azaola-Espinosa and Lino Mayorga-Reyes
Microorganisms 2022, 10(11), 2100; https://doi.org/10.3390/microorganisms10112100 - 22 Oct 2022
Cited by 6 | Viewed by 2326
Abstract
Bifidobacteria have been investigated due to their mutualistic microbe–host interaction with humans throughout their life. This work aims to make a biochemical and genomic characterization of Bifidobacterium pseudocatenulatum JCLA3. By multilocus analysis, the species of B. pseudocatenulatum JCLA3 was established as pseudocatenulatum. [...] Read more.
Bifidobacteria have been investigated due to their mutualistic microbe–host interaction with humans throughout their life. This work aims to make a biochemical and genomic characterization of Bifidobacterium pseudocatenulatum JCLA3. By multilocus analysis, the species of B. pseudocatenulatum JCLA3 was established as pseudocatenulatum. It contains one circular genome of 2,369,863 bp with G + C content of 56.6%, no plasmids, 1937 CDSs, 54 tRNAs, 16 rRNAs, 1 tmRNA, 1 CRISPR region, and 401 operons predicted, including a CRISPR-Cas operon; it encodes an extensive number of enzymes, which allows it to utilize different carbohydrates. The ack gene was found as part of an operon formed by xfp and pta genes. Two genes of ldh were found at different positions. Chromosomally encoded resistance to ampicillin and cephalothin, non-hemolytic activity, and moderate inhibition of Escherichia coli ATCC 25922 and Staphylococcus aureus ATCC 6538 were demonstrated by B. pseudocatenulatum JCLA3; it can survive 100% in simulated saliva, can tolerate primary and secondary glyco- or tauro-conjugated bile salts but not in a mix of bile; the strain did not survive at pH 1.5–5. The cbh gene coding to choloylglycine hydrolase was identified in its genome, which could be related to the ability to deconjugate secondary bile salts. Intact cells showed twice as much antioxidant activity than debris. B. pseudocatenulatum JCLA3 showed 49% of adhesion to Caco-2 cells. The genome and biochemical analysis help to elucidate further possible biotechnological applications of B. pseudocatenulatum JCLA3. Full article
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13 pages, 636 KiB  
Article
Plasma Gut Microbe-Derived Metabolites Associated with Peripheral Artery Disease and Major Adverse Cardiac Events
by Karen J. Ho, Joel L. Ramirez, Rohan Kulkarni, Katharine G. Harris, Irene Helenowski, Liqun Xiong, C. Keith Ozaki and S. Marlene Grenon
Microorganisms 2022, 10(10), 2065; https://doi.org/10.3390/microorganisms10102065 - 19 Oct 2022
Cited by 11 | Viewed by 2413
Abstract
Cardiovascular diseases are associated with gut dysbiosis, but the role of microbe-derived metabolites as biomarkers or modulators of cardiovascular disease are not well understood. This is a targeted metabolomics study to investigate the association of nine microbe-derived metabolites with lower extremity peripheral artery [...] Read more.
Cardiovascular diseases are associated with gut dysbiosis, but the role of microbe-derived metabolites as biomarkers or modulators of cardiovascular disease are not well understood. This is a targeted metabolomics study to investigate the association of nine microbe-derived metabolites with lower extremity peripheral artery disease (PAD), a form of atherosclerosis, and major adverse cardiac events (MACE). The study cohort consists of individuals with intermittent claudication and ankle-brachial index (ABI) < 0.9 (N = 119) and controls without clinically-apparent atherosclerosis (N = 37). The primary endpoint was MACE, a composite endpoint of myocardial infarction, coronary revascularization, stroke, transient ischemic attack, or cardiac-related death. Plasma metabolite concentrations differed significantly between the PAD and control groups. After adjustment for traditional atherosclerosis risk factors, kynurenine, hippuric acid, indole-3-propionic acid (IPA), and indole-3-aldehyde (I3A) concentrations were negatively associated with PAD, whereas indoxyl sulfate and 3-hydroxyanthranilic acid were positively associated. Hippuric acid, IPA, and I3A correlated with ABI, a surrogate for atherosclerotic disease burden. Those in the highest I3A concentration quartile had significantly improved freedom from MACE during follow-up compared to those in the lowest quartile. This study identifies specific indole- and phenyl-derived species impacted by gut microbial metabolic pathways that could represent novel microbiome-related biomarkers of PAD. Full article
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13 pages, 1609 KiB  
Article
Partial Replacement of Oat Hay with Whole-Plant Hydroponic Barley Seedlings Modulates Ruminal Microbiota and Affects Growth Performance of Holstein Heifers
by Peng Ren, Mengmeng Deng, Juan Feng, Ruocheng Li, Xiaojiao Ma, Jianxin Liu and Diming Wang
Microorganisms 2022, 10(10), 2000; https://doi.org/10.3390/microorganisms10102000 - 10 Oct 2022
Cited by 5 | Viewed by 1654
Abstract
The dairy industry is facing challenges in balancing forage supply and crop production. Therefore, forage supply based on a farm land-saving approach should be developed to overcome the human–livestock competition on farmland. The objective of this study was to learn the potential impact [...] Read more.
The dairy industry is facing challenges in balancing forage supply and crop production. Therefore, forage supply based on a farm land-saving approach should be developed to overcome the human–livestock competition on farmland. The objective of this study was to learn the potential impact of partially replacing oat hay with whole-plant hydroponic barley seedlings (HBS) produced via a land-saving hydroponic method on growth performance, digestibility, and rumen microbiota in Holstein dairy heifers. In total, 39 Holstein heifers were randomly divided into 13 blocks based on age and body weight for an 8-week experimental period. The heifers within each block were randomly allocated to one of three diets group: (1) 0% HBS and 16% oat hay (CON); (2) 4% HBS and 12% oat hay (25% HBS); and (3) 8% HBS and 8% oat hay (50% HBS). Compared to CON, feed intake, growth performance, and body N retention were similar to those in cows fed 25% HBS but lower in 50% HBS-fed animals (p < 0.05). Reduced digestibility (crude protein (CP) and organic matter (OM)) was observed in 50% HBS animals (p < 0.05). Compared to the control, the levels of Lachnospiraceae_XPB1014_group, Bacillus, and Colidextribacter were higher, but the levels of Sphaerochaeta and Ruminiclostridium were lower in 50% HBS animals (p < 0.05). Additionally, the digestibility of CP (p < 0.01, r = −0.61) and ether extract (EE) (p < 0.01, r = −0.58) was negatively correlated with Lachnospiraceae_XPB1014_group. The digestibility of OM (p = 0.01, r = −0.55), neutral detergent fiber (NDF) (p = 0.01, r = −0.56), acid detergent fiber (ADF) (p = 0.02, r = −0.52), and CP (p < 0.01, r = −0.61) was negatively correlated with Bacillus. The digestibility of NDF (p = 0.02, r = −0.52) and ADF (p = 0.03, r = −0.50) was negatively correlated with Colidextribacter. The digestibility of OM (p = 0.03, r = 0.50), NDF (p = 0.03, r = 0.50), and ADF (p = 0.03, r = 0.49) was positively correlated with Ruminiclostridium. The digestibility of OM (p = 0.04, r = 0.47), CP (p < 0.01, r = 0.58), and EE (p = 0.03, r = 0.49) was positively correlated with unclassified_f_Rikenellaceae. The digestibility of CP was positively correlated with Sphaerochaeta (p = 0.02, r = 0.53). In conclusion, the current study suggests that HBS could replace oat hay in a ratio-dependent manner. The reduced growth performance could be caused by lower feed intake and digestibility, which may be attributed to the alteration in the rumen’s microbial population. Further exploration of the inhibiting factors of HBS would broaden the application of hydroponic feed in the future. Full article
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10 pages, 1043 KiB  
Article
Fecal Microbiome Differences in Angus Steers with Differing Feed Efficiencies during the Feedlot-Finishing Phase
by Jeferson M. Lourenco, Christina B. Welch, Taylor R. Krause, Michael A. Wieczorek, Francis L. Fluharty, Michael J. Rothrock, T. Dean Pringle and Todd R. Callaway
Microorganisms 2022, 10(6), 1128; https://doi.org/10.3390/microorganisms10061128 - 31 May 2022
Cited by 8 | Viewed by 2164
Abstract
The gastrointestinal microbiota of cattle is important for feedstuff degradation and feed efficiency determination. This study evaluated the fecal microbiome of Angus steers with distinct feed efficiencies during the feedlot-finishing phase. Angus steers (n = 65), fed a feedlot-finishing diet for 82 [...] Read more.
The gastrointestinal microbiota of cattle is important for feedstuff degradation and feed efficiency determination. This study evaluated the fecal microbiome of Angus steers with distinct feed efficiencies during the feedlot-finishing phase. Angus steers (n = 65), fed a feedlot-finishing diet for 82 days, had growth performance metrics evaluated. Steers were ranked based upon residual feed intake (RFI), and the 5 lowest RFI (most efficient) and 5 highest RFI (least efficient) steers were selected for evaluation. Fecal samples were collected on 0-d and 82-d of the finishing period and microbial DNA was extracted and evaluated by 16S rRNA gene sequencing. During the feedlot trial, inefficient steers had decreased (p = 0.02) Ruminococcaceae populations and increased (p = 0.01) Clostridiaceae populations. Conversely, efficient steers had increased Peptostreptococcaceae (p = 0.03) and Turicibacteraceae (p = 0.01), and a trend for decreased Proteobacteria abundance (p = 0.096). Efficient steers had increased microbial richness and diversity during the feedlot period, which likely resulted in increased fiber-degrading enzymes in their hindgut, allowing them to extract more energy from the feed. Results suggest that cattle with better feed efficiency have greater diversity of hindgut microorganisms, resulting in more enzymes available for digestion, and improving energy harvest in the gut of efficient cattle. Full article
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12 pages, 1713 KiB  
Article
The Gut Microbiota May Affect Personality in Mongolian Gerbils
by Lin Gan, Tingbei Bo, Wei Liu and Dehua Wang
Microorganisms 2022, 10(5), 1054; https://doi.org/10.3390/microorganisms10051054 - 20 May 2022
Cited by 4 | Viewed by 2601
Abstract
The “gut–microbiota–brain axis” reveals that gut microbiota plays a critical role in the orchestrating behavior of the host. However, the correlation between the host personalities and the gut microbiota is still rarely known. To investigate whether the gut microbiota of Mongolian gerbils ( [...] Read more.
The “gut–microbiota–brain axis” reveals that gut microbiota plays a critical role in the orchestrating behavior of the host. However, the correlation between the host personalities and the gut microbiota is still rarely known. To investigate whether the gut microbiota of Mongolian gerbils (Meriones unguiculatus) differs between bold and shy personalities, we compared the gut microbiota of bold and shy gerbils, and then we transplanted the gut microbiota of bold and shy gerbils into middle group gerbils (individuals with less bold and shy personalities). We found a significant overall correlation between host boldness and gut microbiota. Even though there were no significant differences in alpha diversity and beta diversity of gut microbiota between bold and shy gerbils, the Firmicutes/Bacteroidetes phyla and Odoribacter and Blautia genus were higher in bold gerbils, and Escherichia_shigella genus was lower. Furthermore, the fecal microbiota transplantation showed that changes in gut microbiota could not evidently cause the increase or decrease in the gerbil’s boldness score, but it increased the part of boldness behaviors by gavaging the “bold fecal microbiota”. Overall, these data demonstrated that gut microbiota were significantly correlated with the personalities of the hosts, and alteration of microbiota could alter host boldness to a certain extent. Full article
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Review

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24 pages, 1590 KiB  
Review
Bovine Immunity and Vitamin D3: An Emerging Association in Johne’s Disease
by Taylor L. T. Wherry and Judith R. Stabel
Microorganisms 2022, 10(9), 1865; https://doi.org/10.3390/microorganisms10091865 - 18 Sep 2022
Viewed by 2521
Abstract
Mycobacterium avium subspecies paratuberculosis (MAP) is an environmentally hardy pathogen of ruminants that plagues the dairy industry. Hallmark clinical symptoms include granulomatous enteritis, watery diarrhea, and significant loss of body condition. Transition from subclinical to clinical infection is a dynamic process led by [...] Read more.
Mycobacterium avium subspecies paratuberculosis (MAP) is an environmentally hardy pathogen of ruminants that plagues the dairy industry. Hallmark clinical symptoms include granulomatous enteritis, watery diarrhea, and significant loss of body condition. Transition from subclinical to clinical infection is a dynamic process led by MAP which resides in host macrophages. Clinical stage disease is accompanied by dysfunctional immune responses and a reduction in circulating vitamin D3. The immunomodulatory role of vitamin D3 in infectious disease has been well established in humans, particularly in Mycobacterium tuberculosis infection. However, significant species differences exist between the immune system of humans and bovines, including effects induced by vitamin D3. This fact highlights the need for continued study of the relationship between vitamin D3 and bovine immunity, especially during different stages of paratuberculosis. Full article
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21 pages, 746 KiB  
Review
Utilizing the Gastrointestinal Microbiota to Modulate Cattle Health through the Microbiome-Gut-Organ Axes
by Christina B. Welch, Valerie E. Ryman, T. Dean Pringle and Jeferson M. Lourenco
Microorganisms 2022, 10(7), 1391; https://doi.org/10.3390/microorganisms10071391 - 10 Jul 2022
Cited by 26 | Viewed by 5509
Abstract
The microorganisms inhabiting the gastrointestinal tract (GIT) of ruminants have a mutualistic relationship with the host that influences the efficiency and health of the ruminants. The GIT microbiota interacts with the host immune system to influence not only the GIT, but other organs [...] Read more.
The microorganisms inhabiting the gastrointestinal tract (GIT) of ruminants have a mutualistic relationship with the host that influences the efficiency and health of the ruminants. The GIT microbiota interacts with the host immune system to influence not only the GIT, but other organs in the body as well. The objective of this review is to highlight the importance of the role the gastrointestinal microbiota plays in modulating the health of a host through communication with different organs in the body through the microbiome-gut-organ axes. Among other things, the GIT microbiota produces metabolites for the host and prevents the colonization of pathogens. In order to prevent dysbiosis of the GIT microbiota, gut microbial therapies can be utilized to re-introduce beneficial bacteria and regain homeostasis within the rumen environment and promote gastrointestinal health. Additionally, controlling GIT dysbiosis can aid the immune system in preventing disfunction in other organ systems in the body through the microbiome-gut-brain axis, the microbiome-gut-lung axis, the microbiome-gut-mammary axis, and the microbiome-gut-reproductive axis. Full article
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17 pages, 1742 KiB  
Review
Domestic Environment and Gut Microbiota: Lessons from Pet Dogs
by Juan Hernandez, Soufien Rhimi, Aicha Kriaa, Vincent Mariaule, Houda Boudaya, Amandine Drut, Amin Jablaoui, Héla Mkaouar, Amel Saidi, Vincent Biourge, Mohamed Ali Borgi, Moez Rhimi and Emmanuelle Maguin
Microorganisms 2022, 10(5), 949; https://doi.org/10.3390/microorganisms10050949 - 30 Apr 2022
Cited by 14 | Viewed by 7842
Abstract
Accumulating data show the involvement of intestinal microbiota in the development and maintenance of numerous diseases. Many environmental factors influence the composition and function of the gut microbiota. An animal model subjected to the same environmental constraints that will allow better characterization of [...] Read more.
Accumulating data show the involvement of intestinal microbiota in the development and maintenance of numerous diseases. Many environmental factors influence the composition and function of the gut microbiota. An animal model subjected to the same environmental constraints that will allow better characterization of the microbiota–host dialogue is awaited. The domestic dog has physiological, dietary and pathological characteristics similar to those of humans and shares the domestic environment and lifestyle of its owner. This review exposes how the domestication of dogs has brought them closer to humans based on their intrinsic and extrinsic similarities which were discerned through examining and comparing the current knowledge and data on the intestinal microbiota of humans and canines in the context of several spontaneous pathologies, including inflammatory bowel disease, obesity and diabetes mellitus. Full article
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