Microbial communities exhibit host species distinguishability and phylosymbiosis along the length of the gastrointestinal tract

Abstract

Host-associated microbial communities consist of stable and transient members that can assemble through purely stochastic processes associated with the environment or by interactions with the host. Phylosymbiosis predicts that if host-microbiota interactions impact assembly patterns, then one conceivable outcome is concordance between host evolutionary histories (phylogeny) and the ecological similarities in microbial community structures (microbiota dendrogram). This assembly pattern has been demonstrated in several clades of animal hosts in laboratory and natural populations, but in vertebrates, it has only been investigated using samples from faeces or the distal colon. Here, we collected the contents of five gut regions from seven rodent species and inventoried the bacterial communities by sequencing the 16S rRNA gene. We investigated how community structures varied across gut regions and whether the pattern of phylosymbiosis was present along the length of the gut. Gut communities varied by host species and gut region, with Oscillospira and Ruminococcus being more abundant in the stomach and hindgut regions. Gut microbial communities were highly distinguishable by host species across all gut regions, with the strength of the discrimination increasing along the length of the gut. Last, the pattern of phylosymbiosis was found in all five gut regions, as well as faeces. Aspects of the gut environment, such as oxygen levels, production of antimicrobials or other factors, may shift microbial communities across gut regions. However, regardless of these differences, host species maintain distinguishable, phylosymbiotic assemblages of microbes that may have functional impacts for the host.

Comparative analysis of microbiota along the length of the gastrointestinal tract of two tree squirrel species (Sciurus aberti and S. niger) living in sympatry

“…Despite these limitations, our findings strengthen previous assertions that the high‐fiber diet of Abert's squirrels has shaped the evolution of the GI tract of this species (Murphy & Linhart, ). Moreover, our data corroborate previous research documenting distinct microbial communities in the upper and lower GI tract (Gu et al, ; Kohl, Dearing, et al, ; Lu et al, ; Suzuki & Nachman, ). Although few studies have compared microbial communities along the length of the GI tract in different species, our findings align with previous research suggesting the microbiota of the lower GI tract may be more divergent between species than microbial communities inhabiting the upper GI tract (Kohl, Dearing, et al, ).…”

“…Furthermore, most alpha ‐diversity measurements were higher in samples from the lower GI tract than the upper GI tract. These results parallel findings in several other rodent species where samples from the upper and lower GI tract are clearly delineated by community membership, and lower GI samples typically have higher diversity (Gu et al, ; Kohl, Dearing, et al, ; Lu et al, ; Suzuki & Nachman, ). Consistent with lower overall diversity in the upper GI tract, the core microbiota of upper GI samples were comprised of few species, which also indicates high individual heterogeneity in this community.…”

“…Factors such as pH, oxygen availability, and production of antimicrobial immune products vary along the length of the tract, and regions of the tract are functionally distinct (Donaldson, Lee, & Mazmanian, 2016). As expected, studies that have analyzed the microbiome of different gut regions have found considerable variation even within individuals (Gu et al, 2013;Kohl, Brun, et al, 2017;Kohl, Dearing, & Bordenstein, 2017;Kohl, Miller, et al, 2014;Lu et al, 2015;Suzuki & Nachman, 2016), but few studies have done this in a comparative framework across species.…”

Editorial 2019

“…The second section featured a number of manuscripts that investigated the structure of the microbiome in an attempt to understand the drivers of microbiota community assembly and turnover. Some contributions weighed in on the role of host phylogeny vs. ecology (Erlandson, Savage, Wei, Cavender‐Bares, & Peay, ; Ivens, Gadau, Kiers, & Kronauer, 2018; Hernandez‐Gomez, Briggler, & Williams, ; Kohl, Dearing, & Bordenstein, ; Nishida & Ochman, ; Roth‐Schulze et al., ; Schuelke, Pereira, Hardy, & Bik, ), others probed how the presence of hosts themselves alters the microbiota around them (Chen & Parfrey, ; Shukla, Vogel, Heckel, Vilcinskas, & Kaltenpoth, ), one investigated patterns of co‐infection (Rock et al, ) and one documented changes in microbiota during development (Prest, Kimball, Kueneman, & McKenzie, ). A few studies in this section studied the structure of the microbiome with manipulative experiments (e.g., Chen & Parfrey, ; Erlandson et al, ; Morella, Gomez, Wang, Leung, & Koskella, ; Raymann, Bobay, & Moran, ).…”

Introduction: The host‐associated microbiome: Pattern, process and function

“…However, in systems ranging from sponges (Thomas et al., ), trees (Kembel et al., ), amphibians (Bletz et al., ) and kelp (Lemay et al., ), host identity is a strong predictor of communities, but the signal disappears at broader phylogenetic levels (e.g., genus and above). Contributions in this issue test the importance of host phylogeny vs. ecology as predictors of microbiome composition by sampling closely related host taxa in controlled environments (Kohl, Dearing, & Bordenstein, ) (Erlandson, Savage, Wei, Cavender‐Bares, & Peay, ), related species with contrasting ecologies in uncontrolled, natural environments (Ivens, Gadau, Kiers, & Kronauer, ) and through broad phylogenetic sampling of animals with both divergent and convergent feeding ecologies (Nishida & Ochman, ; Schuelke, Pereira, Hardy, & Bik, ).…”