Allometry and Ecology of the Bilaterian Gut Microbiome.

Scott Sherrill-Mix,Deus Mjungu,Joyslin I Bushman,Beatrice H Hahn,Celeste Gaughan,Abigail Lauder,Frederic D Bushman,Paco Bertolani,Laurie Zimmerman,Sheri Speede,Aubrey Bailey,Kyle Bittinger,Ronald G Collman,Kevin Mccormick,Martin N Muller,Ella Schmidt,Christelle Colin,Yingying Li,Debby Cox,Rebeca Atencia,Joe Roman,Alexander V Georgiev,Volker Sommer,Jean-Bosco N Django,John Hart ,Térese B Hart ,David Morgan ,Gary D Wu ,John K Carlson ,Heather Marshall Rose ,J.h.l Taylor ,Rudolf P Bohm ,Paul S Schmidt ,Crickette Sanz ,Alex K Piel ,Fiona Stewart

doi:10.1128/mbio.00319-18

Abstract

ABSTRACTClassical ecology provides principles for construction and function of biological communities, but to what extent these apply to the animal-associated microbiota is just beginning to be assessed. Here, we investigated the influence of several well-known ecological principles on animal-associated microbiota by characterizing gut microbial specimens from bilaterally symmetrical animals (Bilateria) ranging from flies to whales. A rigorously vetted sample set containing 265 specimens from 64 species was assembled. Bacterial lineages were characterized by 16S rRNA gene sequencing. Previously published samples were also compared, allowing analysis of over 1,098 samples in total. A restricted number of bacterial phyla was found to account for the great majority of gut colonists. Gut microbial composition was associated with host phylogeny and diet. We identified numerous gut bacterial 16S rRNA gene sequences that diverged deeply from previously studied taxa, identifying opportunities to discover new bacterial types. The number of bacterial lineages per gut sample was positively associated with animal mass, paralleling known species-area relationships from island biogeography and implicating body size as a determinant of community stability and niche complexity. Samples from larger animals harbored greater numbers of anaerobic communities, specifying a mechanism for generating more-complex microbial environments. Predictions for species/abundance relationships from models of neutral colonization did not match the data set, pointing to alternative mechanisms such as selection of specific colonists by environmental niche. Taken together, the data suggest that niche complexity increases with gut size and that niche selection forces dominate gut community construction.

Highlights

Classical ecology provides principles for construction and function of biological communities, but to what extent these apply to the animal-associated microbiota is just beginning to be assessed
We carried out 16S quantitative PCR analysis of all samples studied and analyzed only samples where at least 1,000 16S rRNA gene copies could be introduced into PCRs for library preparation
Samples with extensive representation of lineages found in negative controls typically contained low starting copy numbers of bacterial DNA and were among those excluded by our quantitative PCR (qPCR) criteria

Summary

Introduction

Classical ecology provides principles for construction and function of biological communities, but to what extent these apply to the animal-associated microbiota is just beginning to be assessed. The number of bacterial lineages per gut sample was positively associated with animal mass, paralleling known species-area relationships from island biogeography and implicating body size as a determinant of community stability and niche complexity. IMPORTANCE The intestinal microbiome of animals is essential for health, contributing to digestion of foods, proper immune development, inhibition of pathogen colonization, and catabolism of xenobiotic compounds How these communities assemble and persist is just beginning to be investigated. We interrogated a set of gut samples from a wide range of animals to investigate the roles of selection and random processes in microbial community construction. Nonselective processes enable specific predictions for community structure, but our samples did not match the predictions of the neutral model These findings highlight the importance of niche selection in community construction and suggest mechanisms of niche diversification. Another study, which used a DNA fingerprinting method to characterize bacterial gut communities, concluded that richness increased for animals of larger sizes [5]

Methods

Results

Conclusion