A Reverse Ecology Approach Based on a Biological Definition of Microbial Populations

Delineating ecologically meaningful populations among microbes is important for identifying their roles in environmental and host-associated microbiomes. Here, we introduce a metric of recent gene flow, which when applied to co-existing microbes, identifies congruent genetic and ecological units separated by strong gene flow discontinuities from their next of kin. We then develop a pipeline to identify genome regions within these units that show differential adaptation and allow mapping of populations onto environmental variables or host associations. Using this reverse ecology approach, we show that the human commensal bacterium Ruminococcus gnavus breaks up into sharply delineated populations that show different associations with health and disease. Defining populations by recent gene flow in this way will facilitate the analysis of bacterial and archaeal genomes using ecological and evolutionary theory developed for plants and animals, thus allowing for testing unifying principles across all biology.

[1]  Jan Krüger,et al.  acdc – Automated Contamination Detection and Confidence estimation for single-cell genome data , 2016, BMC Bioinformatics.

[2]  P. Donnelly,et al.  Recombination and Population Structure in Salmonella enterica , 2011, PLoS genetics.

[3]  A. Phillippy,et al.  High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries , 2017, Nature Communications.

[4]  R. Grunow,et al.  Population Structure of Francisella tularensis , 2006, Journal of bacteriology.

[5]  K. Schleifer,et al.  Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences , 2014, Nature Reviews Microbiology.

[6]  Katharina T. Huber,et al.  ape 3.0: New tools for distance-based phylogenetics and evolutionary analysis in R , 2012, Bioinform..

[7]  Pascal Lapierre,et al.  Estimating the size of the bacterial pan-genome. , 2009, Trends in genetics : TIG.

[8]  J. Lennon,et al.  Scaling laws predict global microbial diversity , 2016, Proceedings of the National Academy of Sciences.

[9]  B. Shapiro,et al.  Microbial Speciation. , 2015, Cold Spring Harbor perspectives in biology.

[10]  Andreas Tauch,et al.  The Pan-Genome of the Animal Pathogen Corynebacterium pseudotuberculosis Reveals Differences in Genome Plasticity between the Biovar ovis and equi Strains , 2013, PloS one.

[11]  Lawrence A. David,et al.  Reproducibility of Vibrionaceae population structure in coastal bacterioplankton , 2012, The ISME Journal.

[12]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[13]  E. Alm,et al.  Adaptive radiation by waves of gene transfer leads to fine-scale resource partitioning in marine microbes , 2016, Nature Communications.

[14]  Johannes Söding,et al.  MMseqs2: sensitive protein sequence searching for the analysis of massive data sets , 2017, bioRxiv.

[15]  S. Preheim,et al.  Merging Taxonomy with Ecological Population Prediction in a Case Study of Vibrionaceae , 2011, Applied and Environmental Microbiology.

[16]  Bas E. Dutilh,et al.  Microbial taxonomy in the post-genomic era: Rebuilding from scratch? , 2014, Archives of Microbiology.

[17]  N. Kashtan,et al.  Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus , 2014, Science.

[18]  Natalia N. Ivanova,et al.  Microbial species delineation using whole genome sequences , 2015, Nucleic acids research.

[19]  Eugene V. Koonin,et al.  Phylogenomics of Prokaryotic Ribosomal Proteins , 2012, PloS one.

[20]  D. Krizanc,et al.  Speedy speciation in a bacterial microcosm: new species can arise as frequently as adaptations within a species , 2013, The ISME Journal.

[21]  Silvio C. E. Tosatto,et al.  InterPro in 2017—beyond protein family and domain annotations , 2016, Nucleic Acids Res..

[22]  Lawrence A. David,et al.  Resource Partitioning and Sympatric Differentiation Among Closely Related Bacterioplankton , 2008, Science.

[23]  J. Majewski,et al.  Sexual isolation in bacteria. , 2001, FEMS microbiology letters.

[24]  H. Ochman,et al.  Biological Species Are Universal across Life’s Domains , 2017, Genome biology and evolution.

[25]  C. Pál,et al.  Adaptive evolution of bacterial metabolic networks by horizontal gene transfer , 2005, Nature Genetics.

[26]  Otto X. Cordero,et al.  Population Genomics of Early Events in the Ecological Differentiation of Bacteria , 2012, Science.

[27]  E. Wright,et al.  Exclusivity offers a sound yet practical species criterion for bacteria despite abundant gene flow , 2018, BMC Genomics.

[28]  Otto X. Cordero,et al.  Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global Vibrio cholerae Populations , 2011, mBio.

[29]  O. Gaggiotti,et al.  INVITED REVIEW: What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity , 2006, Molecular ecology.

[30]  M. Hahn,et al.  Microdiversification of a Pelagic Polynucleobacter Species Is Mainly Driven by Acquisition of Genomic Islands from a Partially Interspecific Gene Pool , 2016, Applied and Environmental Microbiology.

[31]  Doolittle Wf Phylogenetic Classification and the Universal Tree , 1999 .

[32]  R. Garrett,et al.  Horizontal Gene Transfer, Dispersal and Haloarchaeal Speciation , 2015, Life.

[33]  C. Fraser,et al.  Recombination and the Nature of Bacterial Speciation , 2007, Science.

[34]  A. Darling,et al.  Patterns of Gene Flow Define Species of Thermophilic Archaea , 2012, PLoS biology.

[35]  C. Fraser,et al.  Fuzzy species among recombinogenic bacteria , 2005, BMC Biology.

[36]  Tal Dagan,et al.  Trends and barriers to lateral gene transfer in prokaryotes. , 2011, Current opinion in microbiology.

[37]  Jenn-Kang Hwang,et al.  CELLO2GO: A Web Server for Protein subCELlular LOcalization Prediction with Functional Gene Ontology Annotation , 2014, PloS one.

[38]  S. Dongen A cluster algorithm for graphs , 2000 .

[39]  Ruth Hershberg,et al.  Gene Loss Dominates As a Source of Genetic Variation within Clonal Pathogenic Bacterial Species , 2015, Genome biology and evolution.

[40]  P. Bork,et al.  Accurate and universal delineation of prokaryotic species , 2013, Nature Methods.

[41]  Carl T. Bergstrom,et al.  The map equation , 2009, 0906.1405.

[42]  James Mallet,et al.  What Is Speciation? , 2016, PLoS genetics.

[43]  M. Yassour,et al.  A novel Ruminococcus gnavus clade enriched in inflammatory bowel disease patients , 2017, Genome Medicine.

[44]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[45]  E. Mayr Systematics and the Origin of Species from the Viewpoint of a Zoologist , 1943 .

[46]  Eric J. Alm,et al.  Sympatric Speciation: When Is It Possible in Bacteria? , 2013, PloS one.

[47]  M. Touchon,et al.  The chromosomal organization of horizontal gene transfer in bacteria , 2017, Nature Communications.

[48]  Steven Salzberg,et al.  Mugsy: fast multiple alignment of closely related whole genomes , 2010, Bioinform..

[49]  B. McDonald,et al.  The Accessory Genome as a Cradle for Adaptive Evolution in Pathogens , 2012, PLoS pathogens.

[50]  E. Rocha Neutral Theory, Microbial Practice: Challenges in Bacterial Population Genetics , 2018, Molecular biology and evolution.

[51]  Otto X. Cordero,et al.  Ecology drives a global network of gene exchange connecting the human microbiome , 2011, Nature.

[52]  Janice K. Wiedenbeck,et al.  Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. , 2011, FEMS microbiology reviews.

[53]  M. Touchon,et al.  Regulation of genetic flux between bacteria by restriction–modification systems , 2016, Proceedings of the National Academy of Sciences.

[54]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[55]  Eric J Alm,et al.  Horizontal gene transfer and the evolution of bacterial and archaeal population structure. , 2013, Trends in genetics : TIG.

[56]  Stephanie J. Spielman,et al.  Pyvolve: A Flexible Python Module for Simulating Sequences along Phylogenies , 2015, bioRxiv.

[57]  Eric J Alm,et al.  Looking for Darwin's footprints in the microbial world. , 2009, Trends in microbiology.

[58]  Daniel J. Wilson,et al.  ClonalFrameML: Efficient Inference of Recombination in Whole Bacterial Genomes , 2015, PLoS Comput. Biol..

[59]  Howard Ochman,et al.  The consequences of genetic drift for bacterial genome complexity. , 2009, Genome research.

[60]  Francisco M. Camas,et al.  Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations , 2015, mBio.

[61]  M. Polz,et al.  A Reverse Ecology Framework for Bacteria and Archaea , 2018 .

[62]  J. M. Smith,et al.  Detecting recombination from gene trees. , 1998, Molecular biology and evolution.

[63]  H. Ochman,et al.  Factors driving effective population size and pan-genome evolution in bacteria , 2018, BMC Evolutionary Biology.

[64]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[65]  V A Traag,et al.  Narrow scope for resolution-limit-free community detection. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[66]  M. Gelfand,et al.  Pangenomic Definition of Prokaryotic Species and the Phylogenetic Structure of Prochlorococcus spp. , 2018, Front. Microbiol..

[67]  Eugene V. Koonin,et al.  Theory of prokaryotic genome evolution , 2016, Proceedings of the National Academy of Sciences.

[68]  Jinling Huang,et al.  Horizontal gene transfer: building the web of life , 2015, Nature Reviews Genetics.

[69]  M. Coetzee,et al.  Prokaryotic species are sui generis evolutionary units. , 2019, Systematic and applied microbiology.

[70]  Otto X. Cordero,et al.  Explaining microbial genomic diversity in light of evolutionary ecology , 2014, Nature Reviews Microbiology.

[71]  Otto X. Cordero,et al.  Competition–dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations , 2014, Proceedings of the National Academy of Sciences.

[72]  Chih-Wen Che,et al.  CELLO2GO: A Web Server for Protein subCELlular LOcalization Prediction with Functional Gene Ontology Annotation , 2014 .

[73]  Pekka Marttinen,et al.  Speciation trajectories in recombining bacterial species , 2016, bioRxiv.

[74]  Florent Lassalle,et al.  Ecological speciation in bacteria: reverse ecology approaches reveal the adaptive part of bacterial cladogenesis. , 2015, Research in microbiology.

[75]  F. Taddei,et al.  Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[76]  Kathryn M. Kauffman,et al.  A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria , 2018, Nature.

[77]  N. W. Davis,et al.  Genome sequence of enterohaemorrhagic Escherichia coli O157:H7 , 2001, Nature.

[78]  Miriam L. Land,et al.  Trace: Tennessee Research and Creative Exchange Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification Recommended Citation Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification , 2022 .

[79]  B. Shapiro,et al.  Ordering microbial diversity into ecologically and genetically cohesive units. , 2014, Trends in microbiology.