scholarly journals Predictable and host‐species specific humanization of the gut microbiota in captive primates

2021 ◽  
Author(s):  
Jennifer L. Houtz ◽  
Jon G. Sanders ◽  
Anthony Denice ◽  
Andrew H. Moeller
2020 ◽  
Author(s):  
Connie A. Rojas ◽  
Santiago A. Ramírez-Barahona ◽  
Kay E. Holekamp ◽  
Kevin. R. Theis

AbstractThe gut microbiota is critical for host function. Among mammals, host phylogenetic relatedness and diet are strong drivers of gut microbiota structure, but one factor may be more influential than the other. Here, we used 16S rRNA gene sequencing to determine the relative contributions of host phylogeny and host dietary guild in structuring the gut microbiotas of 11 herbivore species from 5 families living sympatrically in southwest Kenya. Herbivore species were classified as grazers, browsers, or mixed-feeders. We found that gut microbiotas were highly species-specific, and that host family accounted for more variation in the gut microbiota (35%) than did host dietary guild (14%). Overall, similarity among gut microbiotas increased with host phylogenetic relatedness (r=0.73), yet this relationship was not apparent among seven closely related Bovid host species (r=0.21 NS). In bovids, host dietary guild explained twice as much variation in the gut microbiota as did host species. Lastly, we found that the gut microbiotas of herbivores residing in southwest Kenya closely resemble those of conspecifics from central Kenya, suggesting that regardless of variability in host local habitat, hosts consistently provide microbes with similar niches for colonization. Overall, our findings suggest that host phylogeny may structure the gut microbiota at broad taxonomic scales, but that host ecology may be more influential in shaping the gut microbiotas of closely related host species.


Author(s):  
Jennifer Houtz ◽  
Jon Sanders ◽  
Anthony Denice ◽  
Andrew Moeller

Humans and non-human primates (NHPs) harbor complex gut microbial communities that affect phenotypes and fitness. The gut microbiotas of wild NHPs reflect their hosts’ phylogenetic histories and are compositionally distinct from those of humans, but in captivity the endogenous gut microbial lineages of NHPs can be lost or replaced by lineages found in humans. Despite its potential contributions to gastrointestinal dysfunction, this humanization of the gut microbiota has not been investigated systematically across captive NHP species. Here we show through comparisons of well-sampled wild and captive populations of apes and monkeys that the fraction of the gut microbiota humanized by captivity varies significantly between NHP species but is remarkably reproducible between captive populations of the same NHP species. Conspecific captive populations displayed significantly greater than expected overlap in the sets of bacterial 16S rRNA gene variants that were differentially abundant between captivity and the wild. This overlap was evident even between captive populations residing on different continents but was never observed between heterospecific captive populations. In addition, we developed an approach incorporating human gut microbiota data to rank NHPs’ gut microbial clades based on the propensity of their lineages to be lost or replaced by lineages found in humans in captivity. Relatively few microbial genera displayed reproducible degrees of humanization in different captive host species, but most microbial genera were reproducibly humanized or retained from the wild in conspecific pairs of captive populations. These results demonstrate that the gut microbiotas of captive NHPs display predictable, host-species specific responses to captivity.


2021 ◽  
Vol 3 (1) ◽  
Author(s):  
Connie A. Rojas ◽  
Santiago Ramírez-Barahona ◽  
Kay E. Holekamp ◽  
Kevin R. Theis

AbstractThe gut microbiota is critical for host function. Among mammals, host phylogenetic relatedness and diet are strong drivers of gut microbiota structure, but one factor may be more influential than the other. Here, we used 16S rRNA gene sequencing to determine the relative contributions of host phylogeny and host diet in structuring the gut microbiotas of 11 herbivore species from 5 families living sympatrically in southwest Kenya. Herbivore species were classified as grazers, browsers, or mixed-feeders and dietary data (% C4 grasses in diet) were compiled from previously published sources. We found that herbivore gut microbiotas were highly species-specific, and that host taxonomy accounted for more variation in the gut microbiota (30%) than did host dietary guild (10%) or sample month (8%). Overall, similarity in the gut microbiota increased with host phylogenetic relatedness (r = 0.74) across the 11 species of herbivores, but among 7 closely related Bovid species, dietary %C4 grass values more strongly predicted gut microbiota structure (r = 0.64). Additionally, within bovids, host dietary guild explained more of the variation in the gut microbiota (17%) than did host species (12%). Lastly, while we found that the gut microbiotas of herbivores residing in southwest Kenya converge with those of distinct populations of conspecifics from central Kenya, fine-scale differences in the abundances of bacterial amplicon sequence variants (ASVs) between individuals from the two regions were also observed. Overall, our findings suggest that host phylogeny and taxonomy strongly structure the gut microbiota across broad host taxonomic scales, but these gut microbiotas can be further modified by host ecology (i.e., diet, geography), especially among closely related host species.


2020 ◽  
Vol 375 (1808) ◽  
pp. 20190597 ◽  
Author(s):  
Andrew H. Moeller ◽  
Jon G. Sanders

Every mammalian species harbours a gut microbiota, and variation in the gut microbiota within mammalian species can have profound effects on host phenotypes. In this review, we summarize recent evidence that gut microbiotas have influenced the course of mammalian adaptation and diversification. Associations with gut microbiotas have: (i) promoted the diversification of mammalian species by enabling dietary transitions onto difficult-to-digest carbon sources and toxic food items; (ii) shaped the evolution of adaptive phenotypic plasticity in mammalian species through the amplification of signals from the external environment and from postnatal developmental processes; and (iii) generated selection for host mechanisms, including innate and adaptive immune mechanisms, to control the gut microbiota for the benefit of host fitness. The stability of specific gut microbiotas within host species lineages varies substantially across the mammalian phylogeny, and this variation may alter the ultimate evolutionary outcomes of relationships with gut microbiotas in different mammalian clades. In some mammalian species, including humans, relationships with host species-specific gut microbiotas appear to have led to the evolution of host dependence on the gut microbiota for certain functions. These studies implicate the gut microbiota as a significant environmental factor and selective agent shaping the adaptive evolution of mammalian diet, phenotypic plasticity, gastrointestinal morphology and immunity. This article is part of the theme issue ‘The role of the microbiome in host evolution’.


2021 ◽  
Vol 15 ◽  
Author(s):  
Dehuang Kong ◽  
Lidewij Schipper ◽  
Gertjan van Dijk

Accumulating evidence implicates gut-microbiota-derived metabolites as important regulators of host energy balance and fuel homeostasis, the underlying mechanisms are currently subject to intense research. In this review, the most important executors, short chain fatty acids, which both directly and indirectly fulfill the interactions between gut microbiota and host will be discussed. Distinct roles of individual short chain fatty acids and the different effects they exert on host metabolism have long been overlooked, which compromises the process of clarifying the sophisticated crosstalk between gut microbiota and its host. Moreover, recent findings suggest that exogenously administered short chain fatty acids affect host metabolism via different mechanisms depending on the routes they enter the host. Although these exogenous routes are often artificial, they may help to comprehend the roles of the short-chain-fatty-acid mechanisms and signaling sites, that would normally occur after intestinal absorption of short chain fatty acids. Cautions should be addressed of generalizing findings, since different results have appeared in different host species, which may imply a host species-specific response to short chain fatty acids.


2020 ◽  
Vol 375 (1808) ◽  
pp. 20190598 ◽  
Author(s):  
Laura Grieneisen ◽  
Amanda L. Muehlbauer ◽  
Ran Blekhman

Recent comparative studies have found evidence consistent with the action of natural selection on gene regulation across primate species. Other recent work has shown that the microbiome can regulate host gene expression in a wide range of relevant tissues, leading to downstream effects on immunity, metabolism and other biological systems in the host. In primates, even closely related host species can have large differences in microbiome composition. One potential consequence of these differences is that host species-specific microbial traits could lead to differences in gene expression that influence primate physiology and adaptation to local environments. Here, we will discuss and integrate recent findings from primate comparative genomics and microbiome research, and explore the notion that the microbiome can influence host evolutionary dynamics by affecting gene regulation across primate host species. This article is part of the theme issue ‘The role of the microbiome in host evolution’.


PeerJ ◽  
2019 ◽  
Vol 7 ◽  
pp. e6658 ◽  
Author(s):  
Bing Zhang ◽  
Jing Ren ◽  
Daode Yang ◽  
Shuoran Liu ◽  
Xinguo Gong

Background The gut microbiota plays an important role in host immunity and metabolic homeostasis. Although analyses of gut microbiotas have been used to assess host health and foster disease prevention and treatment, no comparative comprehensive study, assessing gut microbiotas among several species of farmed snake, is yet available. In this study, we characterized and compared the gut microbiotas of four species of farmed snakes (Naja atra, Ptyas mucosa, Elaphe carinata, and Deinagkistrodon acutus) using high-throughput sequencing of the 16S rDNA gene in southern China and tested whether there was a relationship between gut microbiotal composition and host species. Results A total of 629 operational taxonomic units across 22 samples were detected. The five most abundant phyla were Bacteroidetes, Proteobacteria, Firmicutes, Fusobacteria, and Actinobacteria, while the five most abundant genera were Bacteroides, Cetobacterium, Clostridium, Plesiomonas, and Paeniclostridium. This was the first report of the dominance of Fusobacteria and Cetobacterium in the snake gut. Our phylogenetic analysis recovered a relatively close relationship between Fusobacteria and Bacteroidetes. Alpha diversity analysis indicated that species richness and diversity were highest in the gut microbiota of D. acutus and lowest in that of E. carinata. Significant differences in alpha diversity were detected among the four farmed snake species. The gut microbiotas of conspecifics were more similar to each other than to those of heterospecifics. Conclusion This study provides the first comparative study of gut microbiotas among several species of farmed snakes, and provides valuable data for the management of farmed snakes. In farmed snakes, host species affected the species composition and diversity of the gut microbiota.


2008 ◽  
Vol 14 (4) ◽  
pp. 223-231 ◽  
Author(s):  
Regina Lizundia ◽  
Kay-Sara Sauter ◽  
Geraldine Taylor ◽  
Dirk Werling

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