Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography

Metagenomic methods provide an experimental approach to inform the relationships between hosts and their microbial inhabitants. Previous studies have provided the conceptual realization that microbiomes are dynamic among hosts and the intimacy of relation between micro‐ and macroorganisms. Here, we present an intestinal microflora community analysis for members of the order Chiroptera and investigate the relative influence of variables in shaping observed microbiome relationships. The variables ranged from those considered to have ancient and long‐term influences (host phylogeny and life history) to the relatively transient variable of host reproductive condition. In addition, collection locality data, representing the geographic variable, were included in analyses. Results indicate a complex influence of variables in shaping sample relationships in which signal for host phylogeny is recovered at broad taxonomic levels (family), whereas intrafamilial analyses disclosed various degrees of resolution for the remaining variables. Although cumulative probabilities of assignment indicated both reproductive condition and geography influenced relationships, comparison of ecological measures among groups revealed statistical differences between most variable classifications. For example, ranked ecological diversity was associated with host phylogeny (deeper coalescences among families were associated with more microfloral diversity), dietary strategy (herbivory generally retained higher diversity than carnivory) and reproductive condition (reproductively active females displayed more diverse microflora than nonreproductive conditions). Overall, the results of this study describe a complex process shaping microflora communities of wildlife species as well as provide avenues for future research that will further inform the nature of symbiosis between microflora communities and hosts.

[1]  D. Faith Conservation evaluation and phylogenetic diversity , 1992 .

[2]  Ted Dunning,et al.  Accurate Methods for the Statistics of Surprise and Coincidence , 1993, CL.

[3]  R. Knight,et al.  UniFrac: a New Phylogenetic Method for Comparing Microbial Communities , 2005, Applied and Environmental Microbiology.

[4]  S. O’Brien,et al.  A Molecular Phylogeny for Bats Illuminates Biogeography and the Fossil Record , 2005, Science.

[5]  C. De Simone,et al.  Probiotic lactobacilli: an innovative tool to correct the malabsorption syndrome of vegetarians? , 2005, Medical hypotheses.

[6]  M. Fondevila,et al.  The effect of lactating rabbit does on the development of the caecal microbial community in the pups they nurture , 2007, Journal of applied microbiology.

[7]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[8]  Olivier C. Martin,et al.  A congruence index for testing topological similarity between trees , 2007, Bioinform..

[9]  S. Salminen,et al.  Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. , 2008, The American journal of clinical nutrition.

[10]  R. Knight,et al.  Evolution of Mammals and Their Gut Microbes , 2008, Science.

[11]  Adam P. Arkin,et al.  FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix , 2009, Molecular biology and evolution.

[12]  Rob Knight,et al.  PyNAST: a flexible tool for aligning sequences to a template alignment , 2009, Bioinform..

[13]  O. von Helversen,et al.  Evolution of nectarivory in phyllostomid bats (Phyllostomidae Gray, 1825, Chiroptera: Mammalia) , 2010, BMC Evolutionary Biology.

[14]  R. Baker,et al.  TIMESCALE OF DIVERSIFICATION OF FEEDING STRATEGY AND MORPHOLOGY IN NEW WORLD LEAF-NOSED BATS ( PHYLLOSTOMIDAE ) : A PHYLOGENETIC PERSPECTIVE , 2010 .

[15]  R. Nelson,et al.  Photoperiod modulates gut bacteria composition in male Siberian hamsters (Phodopus sungorus) , 2010, Brain, Behavior, and Immunity.

[16]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[17]  S. Wisely,et al.  Microbial ecological response of the intestinal flora of Peromyscus maniculatus and P. leucopus to heavy metal contamination , 2010, Molecular ecology.

[18]  P. Hugenholtz,et al.  Evolutionary Relationships of Wild Hominids Recapitulated by Gut Microbial Communities , 2010, PLoS biology.

[19]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[20]  S. Dowd,et al.  Stressor Exposure Disrupts Commensal Microbial Populations in the Intestines and Leads to Increased Colonization by Citrobacter rodentium , 2010, Infection and Immunity.

[21]  Eunseog Youn,et al.  Black Box Chimera Check (B2C2): a Windows-Based Software for Batch Depletion of Chimeras from Bacterial 16S rRNA Gene Datasets , 2010, The open microbiology journal.

[22]  J. Clemente,et al.  Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans , 2011, Science.

[23]  L. Navarro,et al.  When did plants become important to leaf‐nosed bats? Diversification of feeding habits in the family Phyllostomidae , 2011, Molecular ecology.

[24]  C. Huttenhower,et al.  Host and gut microbiota symbiotic factors: lessons from inflammatory bowel disease and successful symbionts , 2011, Cellular microbiology.

[25]  R. Knight,et al.  Global patterns in the biogeography of bacterial taxa. , 2011, Environmental microbiology.

[26]  Gregg F. Gunnell,et al.  Evolutionary History of Bats: Fossils, Molecules and Morphology , 2012 .

[27]  R. Baker,et al.  Evolutionary History of Bats: Molecular time scale of diversification of feeding strategy and morphology in New World Leaf-Nosed Bats (Phyllostomidae): a phylogenetic perspective , 2012 .