The Timetree of Prokaryotes: New Insights into Their Evolution and Speciation.

The increasing size of timetrees in recent years has led to a focus on diversification analyses to better understand patterns of macroevolution. Thus far, nearly all studies have been conducted with eukaryotes primarily because phylogenies have been more difficult to reconstruct and calibrate to geologic time in prokaryotes. Here, we have estimated a timetree of 11,784 'species' of prokaryotes and explored their pattern of diversification. We used data from the small subunit ribosomal RNA along with an evolutionary framework from previous multi-gene studies to produce three alternative timetrees. For each timetree we surprisingly found a constant net diversification rate derived from an exponential increase of lineages and showing no evidence of saturation (rate decline), the same pattern found previously in eukaryotes. The implication is that prokaryote diversification as a whole is the result of the random splitting of lineages and is neither limited by existing diversity (filled niches) nor responsive in any major way to environmental changes.

[1]  Luke J. Harmon,et al.  GEIGER: investigating evolutionary radiations , 2008, Bioinform..

[2]  Koichiro Tamura,et al.  Estimating divergence times in large molecular phylogenies , 2012, Proceedings of the National Academy of Sciences.

[3]  Yan Boucher,et al.  Higher-level classification of the Archaea: evolution of methanogenesis and methanogens. , 2005, Archaea.

[4]  Daniel L. Rabosky LASER: A Maximum Likelihood Toolkit for Detecting Temporal Shifts in Diversification Rates from Molecular Phylogenies , 2006 .

[5]  James R. Cole,et al.  Ribosomal Database Project: data and tools for high throughput rRNA analysis , 2013, Nucleic Acids Res..

[6]  Koichiro Tamura,et al.  Evolutionary Genetics Analysis Version 6 . 0 , 2013 .

[7]  F. Cohan Bacterial species and speciation. , 2001, Systematic biology.

[8]  D. Rabosky Diversity-Dependence, Ecological Speciation, and the Role of Competition in Macroevolution , 2013 .

[9]  H. Cornell Is regional species diversity bounded or unbounded? , 2013, Biological reviews of the Cambridge Philosophical Society.

[10]  A. Knoll,et al.  Biomarker evidence for green and purple sulphur bacteria in a stratified Palaeoproterozoic sea , 2005, Nature.

[11]  J. Plotkin,et al.  Inferring the Dynamics of Diversification: A Coalescent Approach , 2010, PLoS biology.

[12]  Harold J. Morowitz,et al.  Annihilation of ecosystems by large asteroid impacts on the early Earth , 1989, Nature.

[13]  Raul Munoz,et al.  Release LTPs104 of the All-Species Living Tree. , 2011, Systematic and applied microbiology.

[14]  K. Chater,et al.  Genetics of bacterial diversity , 1989 .

[15]  W. Glassley,et al.  The rise of continents¿An essay on the geologic consequences of photosynthesis , 2006 .

[16]  Oliver G. Pybus,et al.  Testing macro–evolutionary models using incomplete molecular phylogenies , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[17]  Mike A. Steel,et al.  The expected length of pendant and interior edges of a Yule tree , 2009, Appl. Math. Lett..

[18]  Klaus Peter Schliep,et al.  phangorn: phylogenetic analysis in R , 2010, Bioinform..

[19]  Sudhir Kumar,et al.  Discovering the Timetree of Life , 2009 .

[20]  Sudhir Kumar,et al.  Tree of Life Reveals Clock-Like Speciation and Diversification , 2014, Molecular biology and evolution.

[21]  Keita Yamada,et al.  Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era , 2006, Nature.

[22]  Tanja Stadler,et al.  Mammalian phylogeny reveals recent diversification rate shifts , 2011, Proceedings of the National Academy of Sciences.

[23]  J. Plotkin,et al.  EXPLOSIVE RADIATION OF A BACTERIAL SPECIES GROUP , 2012, Evolution; international journal of organic evolution.

[24]  J. T. Staley Transitioning Toward a Universal Species Concept for the Classification of all Organisms , 2013 .

[25]  F. M. Stewart,et al.  The population genetics of antibiotic resistance. II: Analytic theory for sustained populations of bacteria in a community of hosts. , 1998, Theoretical population biology.

[26]  J. Kristjánsson,et al.  Genetic diversity analysis of Rhodothermus reflects geographical origin of the isolates , 2000, Extremophiles.

[27]  Natalia N. Ivanova,et al.  Insights into the phylogeny and coding potential of microbial dark matter , 2013, Nature.

[28]  Jonathan A. Eisen,et al.  Phylogeny of Bacterial and Archaeal Genomes Using Conserved Genes: Supertrees and Supermatrices , 2013, PloS one.

[29]  J. Sepkoski,et al.  A compendium of fossil marine animal genera , 2002 .

[30]  M. Pagel,et al.  Phylogenies reveal new interpretation of speciation and the Red Queen , 2010, Nature.

[31]  A. Mchardy,et al.  Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota , 2015, Proceedings of the National Academy of Sciences.

[32]  F. Cohan,et al.  Bacterial Speciation: Genetic Sweeps in Bacterial Species , 2019 .

[33]  H. Ochman,et al.  Lateral gene transfer and the nature of bacterial innovation , 2000, Nature.

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

[35]  W. Doolittle,et al.  Lateral gene transfer , 2011, Current Biology.

[36]  Daniel L. Rabosky,et al.  Clade Age and Species Richness Are Decoupled Across the Eukaryotic Tree of Life , 2012, PLoS biology.

[37]  Reconciling Diversification: Random Pulse Models of Speciation and Extinction , 2014, The American Naturalist.

[38]  D. M. Ward,et al.  Geographical isolation in hot spring cyanobacteria. , 2003, Environmental microbiology.

[39]  D. Dykhuizen Santa Rosalia revisited: Why are there so many species of bacteria? , 2004, Antonie van Leeuwenhoek.

[40]  W. Jetz,et al.  The global diversity of birds in space and time , 2012, Nature.

[41]  S. Hedges,et al.  A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land , 2004, BMC Evolutionary Biology.

[42]  Andrew P. Martin,et al.  THE RATE AND PATTERN OF CLADOGENESIS IN MICROBES , 2004, Evolution; international journal of organic evolution.

[43]  P. Yarza,et al.  The All-Species Living Tree Project , 2014 .

[44]  Daniel L Rabosky,et al.  LASER: A Maximum Likelihood Toolkit for Detecting Temporal Shifts in Diversification Rates From Molecular Phylogenies , 2006, Evolutionary bioinformatics online.

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

[46]  Nick Goldman,et al.  PhyloSim - Monte Carlo simulation of sequence evolution in the R statistical computing environment , 2011, BMC Bioinformatics.

[47]  林继红,et al.  古细菌(Archaebacteria)表面糖蛋白 , 1990 .

[48]  A. Oren Naming Cyanophyta/Cyanobacteria - a bacteriologist's view. , 2011 .

[49]  Sudhir Kumar,et al.  The timetree of life , 2009 .

[50]  R. MacLean,et al.  Adaptive radiation in microbial microcosms. , 2005, Journal of evolutionary biology.

[51]  Se-Ran Jun,et al.  Whole-proteome phylogeny of prokaryotes by feature frequency profiles: An alignment-free method with optimal feature resolution , 2009, Proceedings of the National Academy of Sciences.

[52]  R. Kassen Toward a General Theory of Adaptive Radiation , 2009, Annals of the New York Academy of Sciences.

[53]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[54]  K. Schleifer,et al.  The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. , 2008, Systematic and applied microbiology.

[55]  Katherine H. Freeman,et al.  Estimated Minimal Divergence Times of the Major Bacterial and Archaeal Phyla , 2003 .

[56]  John Maynard Smith,et al.  The population genetics of bacteria , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[57]  M. Liles,et al.  Molecular Phylogenetics and Temporal Diversification in the Genus Aeromonas Based on the Sequences of Five Housekeeping Genes , 2014, PloS one.

[58]  Kenneth H. Williams,et al.  Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling , 2015, Current Biology.

[59]  S. Hedges,et al.  A major clade of prokaryotes with ancient adaptations to life on land. , 2009, Molecular biology and evolution.

[60]  E. Rocha,et al.  Horizontal Transfer, Not Duplication, Drives the Expansion of Protein Families in Prokaryotes , 2011, PLoS genetics.

[61]  Daniel L. Rabosky,et al.  BAMMtools: an R package for the analysis of evolutionary dynamics on phylogenetic trees , 2014 .

[62]  T. Hauer,et al.  CyanoDB. cz-On-line database of cyanobacterial genera. Univ. of South Bohemia & Inst. of Botany AS CR , 2013 .