Sequence variant analysis reveals poor correlations in microbial taxonomic abundance between humans and mice after gnotobiotic transfer

Fouladi, Farnaz; Glenny, Elaine M.; Bulik-Sullivan, Emily C.; Tsilimigras, Matthew C. B.; Sioda, Michael; Thomas, Stéphanie; Wang, Yunfei; Djukic, Zorka; Tang, Quyen; Tarantino, Lisa M.; Bulik, Cynthia M.; Fodor, Anthony A.; Carroll, Ian M.

doi:10.1038/s41396-020-0645-z

Cited by 36 publications

(35 citation statements)

References 37 publications

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“…Fecal materials, the excreted residue of the digestive tract, fail to capture the overall variation in bacterial colonization along the entire GI-tract because of the absence of the SI microbiota. In many previous studies using humanized mice, microbes successfully colonizing the recipient intestine also primarily originated from the largeintestinal microbiome of donors, such as Lachnospiraceae, Prevotellaceae, and Ruminococcaceae, with few smallintestinal microbes colonized [72][73][74][75]. These outcomes are in line with our study and indicate the missing effects of the small-intestinal microbiota of donors in these FMT studies.…”

Section: Niche-specific Colonization Of Exogenous Microbiota Across Dsupporting

confidence: 89%

Spatial heterogeneity of bacterial colonization across different gut segments following inter-species microbiota transplantation

Zuo

Huang

et al. 2020

Microbiome

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Background The microbiota presents a compartmentalized distribution across different gut segments. Hence, the exogenous microbiota from a particular gut segment might only invade its homologous gut location during microbiota transplantation. Feces as the excreted residue contain most of the large-intestinal microbes but lack small-intestinal microbes. We speculated that whole-intestinal microbiota transplantation (WIMT), comprising jejunal, ileal, cecal, and colonic microbiota, would be more effective for reshaping the entire intestinal microbiota than conventional fecal microbiota transplantation fecal microbiota transplantation (FMT). Results We modeled the compartmentalized colonization of the gut microbiota via transplanting the microbiota from jejunum, ileum, cecum, and colon, respectively, into the germ-free mice. Transplanting jejunal or ileal microbiota induced more exogenous microbes’ colonization in the small intestine (SI) of germ-free mice rather than the large intestine (LI), primarily containing Proteobacteria, Lactobacillaceae, and Cyanobacteria. Conversely, more saccharolytic anaerobes from exogenous cecal or colonic microbiota, such as Bacteroidetes, Prevotellaceae, Lachnospiraceae, and Ruminococcaceae, established in the LI of germ-free mice that received corresponding intestinal segmented microbiota transplantation. Consistent compartmentalized colonization patterns of microbial functions in the intestine of germ-free mice were also observed. Genes related to nucleotide metabolism, genetic information processing, and replication and repair were primarily enriched in small-intestinal communities, whereas genes associated with the metabolism of essential nutrients such as carbohydrates, amino acids, cofactors, and vitamins were mainly enriched in large-intestinal communities of germ-free mice. Subsequently, we compared the difference in reshaping the community structure of germ-free mice between FMT and WIMT. FMT mainly transferred LI-derived microorganisms and gene functions into the recipient intestine with sparse SI-derived microbes successfully transplanted. However, WIMT introduced more SI-derived microbes and associated microbial functions to the recipient intestine than FMT. Besides, WIMT also improved intestinal morphological development as well as reduced systematic inflammation responses of recipients compared with FMT. Conclusions Segmented exogenous microbiota transplantation proved the spatial heterogeneity of bacterial colonization along the gastrointestinal tract, i.e., the microbiota from one specific location selectively colonizes its homologous gut region. Given the lack of exogenous small-intestinal microbes during FMT, WIMT may be a promising alternative for conventional FMT to reconstitute the microbiota across the entire intestinal tract.

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Section: Niche-specific Colonization Of Exogenous Microbiota Across Dsupporting

confidence: 89%

Spatial heterogeneity of bacterial colonization across different gut segments following inter-species microbiota transplantation

Zuo

Huang

et al. 2020

Microbiome

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“…However, antibiotic doses used in mice experiments create an almost germ-free environment after treatment, which is unlikely to apply to the human gut with clinical use of antibiotics. Furthermore, the mice gut microbiome and human gut microbiome differ considerably [41][42][43]. For example, many Firmicutes spp., which represent major colonizers of the human gut, cannot efficiently colonize the murine gut.…”

Section: Discussionmentioning

confidence: 99%

Antibiotics create a shift from mutualism to competition in human gut communities with a longer-lasting impact on fungi than bacteria

et al. 2020

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Background Antibiotic treatment has a well-established detrimental effect on the gut bacterial composition, but effects on the fungal community are less clear. Bacteria in the lumen of the gastrointestinal tract may limit fungal colonization and invasion. Antibiotic drugs targeting bacteria are therefore seen as an important risk factor for fungal infections and induced allergies. However, antibiotic effects on gut bacterial-fungal interactions, including disruption and resilience of fungal community compositions, were not investigated in humans. We analysed stool samples collected from 14 healthy human participants over 3 months following a 6-day antibiotic administration. We integrated data from shotgun metagenomics, metatranscriptomics, metabolomics, and fungal ITS2 sequencing. Results While the bacterial community recovered mostly over 3 months post treatment, the fungal community was shifted from mutualism at baseline to competition. Half of the bacterial-fungal interactions present before drug intervention had disappeared 3 months later. During treatment, fungal abundances were associated with the expression of bacterial genes with functions for cell growth and repair. By extending the metagenomic species approach, we revealed bacterial strains inhibiting the opportunistic fungal pathogen Candida albicans. We demonstrated in vitro how C. albicans pathogenicity and host cell damage might be controlled naturally in the human gut by bacterial metabolites such as propionate or 5-dodecenoate. Conclusions We demonstrated that antibacterial drugs have long-term influence on the human gut mycobiome. While bacterial communities recovered mostly 30-days post antibacterial treatment, the fungal community was shifted from mutualism towards competition.

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“…Although no PCL gyrB sequence was detected in mouse gut bacterial gene catalog, which was generated from common laboratory mice (non-humanized) (60), a recent study verified the reliable transmission of Prevotellaceae from human feces to germfree mice (61). Our investigation on the PCL members in captive mammals suggested that these bacteria recently originated from sympatric human hosts and potentially experienced niche selection, e.g., g8 of P. copri in bovines and pigs.…”

Section: Non-strict Biogeography and Host For Pcl Members Suggest Limmentioning

confidence: 70%

Panoramic Insights into the Microevolution and Macroevolution ofPrevotella copri-containing Lineage in Primate Guts

Meier‐Kolthoff

et al. 2020

Preprint

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Prevotella copri and related taxa are widely detected in mammalian gut microbiomes and have been linked with one human enterotype. However, their microevolution and macroevolution among hosts are poorly characterized. In this study, extensively collected marker genes and genomes were analyzed to trace their evolutionary history, host specificity, and biogeographic distribution. Investigations based on 16S rRNA gene, gyrB, and genomes suggested that a multi-specific P. copri-containing lineage (PCL) harbors diverse species in higher primates. Firstly, P. copri is the dominant species of PCL in the human gut and consists of multiple groups exhibiting high genomic divergence and conspicuous but non-strict biogeographic pattern. Most African strains with high genomic divergence from other strains were phylogenetically placed near the species root, indicating the co-evolutionary history of P. copri and Homo sapiens. Secondly, although long-term co-evolution between PCL and higher primates was revealed, sporadic signals of co-speciation and extensive host jumping of PCL members were observed among higher primates. Metagenomic and phylogenetic analyses indicated that P. copri and other PCL species found in captive mammals have been recently transmitted from humans. Thirdly, strong evidence was found on the extensively horizontal transfer of genes (e.g., carbohydrate-active enzyme encoding genes) among sympatric P. copri groups and PCL species in the same primate host. Our study provides panoramic insights into the complex effects of vertical and horizontal transmission, and potential niche adaption on speciation, host, and biogeographical distribution spanning microevolutionary and macroevolutionary history for a certain gut bacterial lineage.ImportancePrevotella copri and its related taxa, which we designated as Prevotella copri-containing lineage (PCL) in the present study, are widely detected in guts of human, non-human primates and many captive mammals, showing positive or negative correlation to some human diseases. However, a comprehensive understanding on its microevolutionary (within P. copri) and macroevolutionary (among PCL members) history across host species and host biogeography is still lacking. According to our analysis based on 16S rRNA gene, gyrB and genomes, we provided the panoramic insights into the putative effects of vertical transfer, horizontal transmission and potential niche selection on host and biogeographical distribution of this gut bacterial lineage and P. copri. To our knowledge, it is the first time that a gut bacterial lineage was studied at both micro- and macroevolutionary levels, which can aid our systematic understanding on the host-microbe co-evolutionary interactions.

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Sequence variant analysis reveals poor correlations in microbial taxonomic abundance between humans and mice after gnotobiotic transfer

Cited by 36 publications

References 37 publications

Spatial heterogeneity of bacterial colonization across different gut segments following inter-species microbiota transplantation

Spatial heterogeneity of bacterial colonization across different gut segments following inter-species microbiota transplantation

Antibiotics create a shift from mutualism to competition in human gut communities with a longer-lasting impact on fungi than bacteria

Panoramic Insights into the Microevolution and Macroevolution ofPrevotella copri-containing Lineage in Primate Guts

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