Horizontal gene transfer and the evolution of bacterial and archaeal population structure.

Many bacterial and archaeal lineages have a history of extensive and ongoing horizontal gene transfer and loss, as evidenced by the large differences in genome content even among otherwise closely related isolates. How ecologically cohesive populations might evolve and be maintained under such conditions of rapid gene turnover has remained controversial. Here we synthesize recent literature demonstrating the importance of habitat and niche in structuring horizontal gene transfer. This leads to a model of ecological speciation via gradual genetic isolation triggered by differential habitat-association of nascent populations. Further, we hypothesize that subpopulations can evolve through local gene-exchange networks by tapping into a gene pool that is adaptive towards local, continuously changing organismic interactions and is, to a large degree, responsible for the observed rapid gene turnover. Overall, these insights help to explain how bacteria and archaea form populations that display both ecological cohesion and high genomic diversity.

[1]  H. Stanley,et al.  On the Size Distribution of Business Firms , 2008 .

[2]  Marina Halac Relational Contracts and the Value of Relationships , 2011 .

[3]  W. Martin,et al.  Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes. , 2011, Genome research.

[4]  Ali Hortaçsu,et al.  Cementing Relationships: Vertical Integration, Foreclosure, Productivity, and Prices , 2007, Journal of Political Economy.

[5]  J. Lawrence,et al.  Protozoan predation, diversifying selection, and the evolution of antigenic diversity in Salmonella. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[6]  W. Doolittle,et al.  On the origin of prokaryotic species. , 2009, Genome research.

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

[8]  D. Grogan,et al.  Recombination of synthetic oligonucleotides with prokaryotic chromosomes: substrate requirements of the Escherichia coli/λRed and Sulfolobus acidocaldarius recombination systems , 2008, Molecular microbiology.

[9]  H. J. Beaumont,et al.  Experimental evolution of bet hedging , 2009, Nature.

[10]  Wayne M. Getz,et al.  Genetic Exchange Across a Species Boundary in the Archaeal Genus Ferroplasma , 2007, Genetics.

[11]  D. Simester,et al.  Direct and Indirect Bargaining Costs and the Scope of the Firm , 2000 .

[12]  W. Doolittle,et al.  Searching for species in haloarchaea , 2007, Proceedings of the National Academy of Sciences.

[13]  Rachel J. Whitaker Allopatric origins of microbial species , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[14]  Julian Parkhill,et al.  Evolution of MRSA During Hospital Transmission and Intercontinental Spread , 2010, Science.

[15]  O. Hart,et al.  CONTRACTS, REFERENCE POINTS, AND COMPETITION—BEHAVIORAL EFFECTS OF THE FUNDAMENTAL TRANSFORMATION , 2009 .

[16]  J. Crémer,et al.  Auctions with costly information acquisition , 2007 .

[17]  O. Williamson,et al.  Markets and Hierarchies: Analysis and Antitrust Implications. , 1977 .

[18]  Vincent J. Denef,et al.  AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature , 2010, The ISME Journal.

[19]  Chad Syverson,et al.  Vertical Integration and Input Flows , 2014 .

[20]  S. Preheim,et al.  O-antigen diversity and lateral transfer of the wbe region among Vibrio splendidus isolates. , 2010, Environmental microbiology.

[21]  James M. Malcomson,et al.  Reputation and Hierarchy in Dynamic Models of Employment , 1988, Journal of Political Economy.

[22]  F. Cohan What are bacterial species? , 2002, Annual review of microbiology.

[23]  Jaideep P. Sundaram,et al.  Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[24]  M. Jackson,et al.  Overcoming Incentive Constraints by Linking Decisions , 2007 .

[25]  Roy Kishony,et al.  Structure and Evolution of Streptomyces Interaction Networks in Soil and In Silico , 2011, PLoS biology.

[26]  D. Dykhuizen,et al.  Detecting selective sweeps in naturally occurring Escherichia coli. , 1994, Genetics.

[27]  G. Ehrlich,et al.  Construction and characterization of a highly redundant Pseudomonas aeruginosa genomic library prepared from 12 clinical isolates: application to studies of gene distribution among populations. , 2006, International journal of pediatric otorhinolaryngology.

[28]  F. Rodríguez-Valera,et al.  The bacterial pan-genome:a new paradigm in microbiology. , 2010, International microbiology : the official journal of the Spanish Society for Microbiology.

[29]  O. Hart,et al.  Property Rights and the Nature of the Firm , 1988, Journal of Political Economy.

[30]  C. Hart,et al.  Use of a Variable Amplicon Typing Scheme Reveals Considerable Variation in the Accessory Genomes of Isolates of Burkholderia pseudomallei , 2006, Journal of Clinical Microbiology.

[31]  Pascal Lapierre,et al.  Low Species Barriers in Halophilic Archaea and the Formation of Recombinant Hybrids , 2012, Current Biology.

[32]  K. Konstantinidis,et al.  Bacterial species may exist, metagenomics reveal. , 2012, Environmental microbiology.

[33]  K. Chaudhuri,et al.  Lipopolysaccharides of Vibrio cholerae II. Genetics of biosynthesis. , 2004, Biochimica et biophysica acta.

[34]  R. Lenski,et al.  Mutation, recombination, and incipient speciation of bacteria in the laboratory. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[35]  A. Danchin,et al.  Organised Genome Dynamics in the Escherichia coli Species Results in Highly Diverse Adaptive Paths , 2009, PLoS genetics.

[36]  Maureen L. Coleman,et al.  Ecosystem-specific selection pressures revealed through comparative population genomics , 2010, Proceedings of the National Academy of Sciences.

[37]  E. Helpman,et al.  Export Versus FDI with Heterogeneous Firms , 2004 .

[38]  J. Burton,et al.  Rapid Pneumococcal Evolution in Response to Clinical Interventions , 2011, Science.

[39]  Giacomo Calzolari,et al.  Relational Contracts and Competitive Screening , 2009 .

[40]  Kevin J. Murphy,et al.  Relational Contracts and the Theory of the Firm , 1997 .

[41]  Ene,et al.  INTEGRATION VERSUS OUTSOURCING IN INDUSTRY EQUILIBRIUM , 2004 .

[42]  David R. Riley,et al.  Comparative genomics: the bacterial pan-genome. , 2008, Current opinion in microbiology.

[43]  P. Reeves,et al.  Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. , 2003, Carbohydrate research.

[44]  Vincent J. Denef,et al.  Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities , 2010, Proceedings of the National Academy of Sciences.

[45]  W. Doolittle,et al.  Genomics and the bacterial species problem , 2006, Genome Biology.

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

[47]  Simon Board Relational Contracts and the Value of Loyalty , 2011 .

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

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

[50]  Steven Tadelis,et al.  Incentives Versus Transaction Costs: A Theory of Procurement Contracts , 2001 .

[51]  F. Blattner,et al.  Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[52]  P. Reeves,et al.  Gene transfer is a major factor in bacterial evolution. , 1996, Molecular biology and evolution.

[53]  B. Wernerfelt,et al.  Costs of Implementation: Bargaining Costs versus Allocative Efficiency , 2008 .

[54]  R. Amann,et al.  The species concept for prokaryotes. , 2013, FEMS microbiology reviews.

[55]  Sarah P Preheim,et al.  Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[56]  Florian Zettelmeyer,et al.  $1,000 Cash Back: The Pass-Through of Auto Manufacturer Promotions , 2006 .

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

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

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

[60]  Otto X. Cordero,et al.  Ecological Populations of Bacteria Act as Socially Cohesive Units of Antibiotic Production and Resistance , 2012, Science.

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

[62]  Elhanan Helpman,et al.  Global Sourcing , 2003, Journal of Political Economy.

[63]  R. Gibbons,et al.  Organization and Information: Firms’ Governance Choices in Rational-Expectations Equilibrium* , 2012 .

[64]  Sherwin Rosen,et al.  Specialization and Human Capital , 1983, Journal of Labor Economics.

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

[66]  J. Hacker,et al.  Ecological fitness, genomic islands and bacterial pathogenicity , 2001, EMBO reports.

[67]  Eric Maskin,et al.  Unforeseen Contingencies and Incomplete Contracts , 1999 .

[68]  C. Fraser,et al.  Sequences, sequence clusters and bacterial species , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

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

[71]  Niko Matouschek Ex Post Inefficiencies in a Property Rights Theory of the Firm , 2004 .

[72]  M. Satterthwaite,et al.  Efficient Mechanisms for Bilateral Trading , 1983 .

[73]  F. Rohwer,et al.  Explaining microbial population genomics through phage predation , 2009, Nature Reviews Microbiology.

[74]  E. Brynjolfsson,et al.  Beyond Computation: Information Technology, Organizational Transformation and Business Performance , 2000 .

[75]  Y. Barzel,et al.  Measurement Cost and the Organization of Markets , 1982, The Journal of Law and Economics.

[76]  F. Cohan The Effects of Rare but Promiscuous Genetic Exchange on Evolutionary Divergence in Prokaryotes , 1994, The American Naturalist.