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Environment and host species identity shape gut microbiota diversity in sympatric herbivorous mammals.

ABSTRACT: The previous studies have reported that the mammalian gut microbiota is a physiological consequence; nonetheless, the factors influencing its composition and function remain unclear. In this study, to evaluate the contributions of the host and environment to the gut microbiota, we conducted a sequencing analysis of 16S rDNA and shotgun metagenomic DNA from plateau pikas and yaks, two sympatric herbivorous mammals, and further compared the sequences in summer and winter. The results revealed that both pikas and yaks harboured considerably more distinct communities between summer and winter. We detected the over-representation of Verrucomicrobia and Proteobacteria in pikas, and Archaea and Bacteroidetes in yaks. Firmicutes and Actinobacteria, associated with energy-efficient acquisition, significantly enriched in winter. The diversity of the microbial community was determined by the interactive effects between the host and season. Metagenomic analysis revealed that methane-metabolism-related pathway of yaks was significantly enriched in summer, while some pathogenic pathways were more abundant in pikas. Both pikas and yaks had a higher capacity for lipid degradation in winter. Pika and yak shared more OTUs when food shortage occurred in winter, and this caused a convergence in gut microbial composition and function. From winter to summer, the network module number increased from one to five in pikas, which was different in yaks. Our study demonstrates that the host is a dominant factor in shaping the microbial communities and that seasonality promotes divergence or convergence based on dietary quality across host species identity.

SUBMITTER: Fu H

PROVIDER: S-EPMC8313255 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundGut microbiota play a key role in the nutrition of many marine herbivorous fishes through hindgut fermentation of seaweed. Gut microbiota composition in the herbivorous fish Kyphosus sydneyanus (family Kyphosidae) varies between individuals and gut sections, raising two questions: (i) is community composition stable over time, especially given seasonal shifts in storage metabolites of dietary brown algae, and (ii) what processes influence community assembly in the hindgut?ResultsWe examined variation in community composition in gut lumen and mucosa samples from three hindgut sections of K. sydneyanus collected at various time points in 2020 and 2021 from reefs near Great Barrier Island, New Zealand. 16S rRNA gene analysis was used to characterize microbial community composition, diversity and estimated density. Differences in community composition between gut sections remained relatively stable over time, with little evidence of temporal variation. Clostridia dominated the proximal hindgut sections and Bacteroidia the most distal section. Differences were detected in microbial composition between lumen and mucosa, especially at genus level.ConclusionsHigh variation in community composition and estimated bacterial density among individual fish combined with low variation in community composition temporally suggests that initial community assembly involved environmental selection and random sampling/neutral effects. Community stability following colonisation could also be influenced by historical contingency, where early colonizing members of the community may have a selective advantage. The impact of temporal changes in the algae may be limited by the dynamics of substrate depletion along the gut following feeding, i.e. the depletion of storage metabolites in the proximal hindgut. Estimated bacterial density, showed that Bacteroidota has the highest density (copies/mL) in distal-most lumen section V, where SCFA concentrations are highest. Bacteroidota genera Alistipes and Rikenella may play important roles in the breakdown of seaweed into useful compounds for the fish host.

Project description:The development of Leishmania parasites within sand fly vectors occurs entirely in the insect gut lumen, in the presence of symbiotic and commensal bacteria. The impacts of host species and environment on the gut microbiome are currently poorly understood. We employed MiSeq sequencing of the V3-16S rRNA gene amplicons to characterize and compare the gut microbiota of field-collected populations of Phlebotomus kandelakii, P. perfiliewi, P. alexandri, and P. major, the primary or secondary vectors of zoonotic visceral leishmaniasis (ZVL) in three distinct regions of Iran where ZVL is endemic. In total, 160,550 quality-filtered reads of the V3 region yielded a total of 72 operational taxonomic units (OTUs), belonging to 23 phyla, 47 classes, 91 orders, 131 families, and 335 genera. More than 50% of the bacteria identified were Proteobacteria, followed by Firmicutes (22%), Deinococcus-Thermus (9%), Actinobacteria (6%), and Bacteroidetes (5%). The core microbiome was dominated by eight genera: Acinetobacter, Streptococcus, Enterococcus, Staphylococcus, Bacillus, Propionibacterium, Kocuria, and Corynebacterium. Wolbachia were found in P. alexandri and P. perfiliewi, while Asaia sp. was reported in P. perfiliewi. Substantial variations in the gut bacterial composition were found between geographically distinct populations of the same sand fly species, as well as between different species at the same location, suggesting that sand fly gut microbiota is shaped by both the host species and geographical location. Phlebotomus kandelakii and P. perfiliewi in the northwest, and P. alexandri in the south, the major ZVL vectors, harbor the highest bacterial diversity, suggesting a possible relationship between microbiome diversity and the capacity for parasite transmission. In addition, large numbers of gram-positive human or animal pathogens were found, suggesting that sand fly vectors of ZVL could pose a potential additional threat to livestock and humans in the region studied. The presence of Bacillus subtilis, Enterobacter cloacae, and Asaia sp suggests that these bacteria could be promising candidates for a paratransgenesis approach to the fight against Leishmaniasis.

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Environment and host species identity shape gut microbiota diversity in sympatric herbivorous mammals.

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