Growth Temperature and Genome Size in Bacteria Are Negatively Correlated, Suggesting Genomic Streamlining During Thermal Adaptation

Prokaryotic genomes are small and compact. Either this feature is caused by neutral evolution or by natural selection favoring small genomes—genome streamlining. Three separate prior lines of evidence argue against streamlining for most prokaryotes. We find that the same three lines of evidence argue for streamlining in the genomes of thermophile bacteria. Specifically, with increasing habitat temperature and decreasing genome size, the proportion of genomic DNA in intergenic regions decreases. Furthermore, with increasing habitat temperature, generation time decreases. Genome-wide selective constraints do not decrease as in the reduced genomes of host-associated species. Reduced habitat variability is not a likely explanation for the smaller genomes of thermophiles. Genome size may be an indirect target of selection due to its association with cell volume. We use metabolic modeling to demonstrate that known changes in cell structure and physiology at high temperature can provide a selective advantage to reduce cell volume at high temperatures.

[1]  R. Jaenicke,et al.  Stability and stabilization of globular proteins in solution. , 2000, Journal of biotechnology.

[2]  Frédéric Partensky,et al.  Accelerated evolution associated with genome reduction in a free-living prokaryote , 2005, Genome Biology.

[3]  N. Moran,et al.  Comment on "The Origins of Genome Complexity" , 2004, Science.

[4]  N. Moran,et al.  Lifestyle evolution in symbiotic bacteria: insights from genomics. , 2000, Trends in ecology & evolution.

[5]  E. Koonin,et al.  Potential genomic determinants of hyperthermophily. , 2003, Trends in genetics : TIG.

[6]  R. Nussinov,et al.  How do thermophilic proteins deal with heat? , 2001, Cellular and Molecular Life Sciences CMLS.

[7]  N. Lartillot,et al.  A phylogenetic model for investigating correlated evolution of substitution rates and continuous phenotypic characters. , 2011, Molecular biology and evolution.

[8]  Eduardo P. C. Rocha,et al.  The Systemic Imprint of Growth and Its Uses in Ecological (Meta)Genomics , 2010, PLoS genetics.

[9]  J. Felsenstein Comparative Methods with Sampling Error and Within‐Species Variation: Contrasts Revisited and Revised , 2008, The American Naturalist.

[10]  Igor N. Berezovsky,et al.  Protein and DNA Sequence Determinants of Thermophilic Adaptation , 2006, PLoS Comput. Biol..

[11]  M. Noordewier,et al.  Genome Streamlining in a Cosmopolitan Oceanic Bacterium , 2005, Science.

[12]  M. Lynch Streamlining and simplification of microbial genome architecture. , 2006, Annual review of microbiology.

[13]  N. Goldman,et al.  A codon-based model of nucleotide substitution for protein-coding DNA sequences. , 1994, Molecular biology and evolution.

[14]  Eduardo P C Rocha,et al.  Causes of insertion sequences abundance in prokaryotic genomes. , 2007, Molecular biology and evolution.

[15]  N. Moran,et al.  Estimating Population Size and Transmission Bottlenecks in Maternally Transmitted Endosymbiotic Bacteria , 2002, Microbial Ecology.

[16]  F. Crick,et al.  Selfish DNA: the ultimate parasite , 1980, Nature.

[17]  R. Lenski,et al.  Microbial genetics: Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation , 2003, Nature Reviews Genetics.

[18]  N. Moran,et al.  The Dynamics and Time Scale of Ongoing Genomic Erosion in Symbiotic Bacteria , 2009, Science.

[19]  P. Mitchell Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. 1966. , 2011, Biochimica et biophysica acta.

[20]  Janet M. Thornton,et al.  Microeconomic Principles Explain an Optimal Genome Size in Bacteria , 2004, Spanish Bioinformatics Conference.

[21]  D. Tempest,et al.  Metabolic and energetic aspects of the growth of Bacillus stearothermophilus in glucose-limited and glucose-sufficient chemostat culture , 1988, Archives of Microbiology.

[22]  Sean R. Eddy,et al.  Profile hidden Markov models , 1998, Bioinform..

[23]  J. Lobry,et al.  Relationships Between Genomic G+C Content, RNA Secondary Structures, and Optimal Growth Temperature in Prokaryotes , 1997, Journal of Molecular Evolution.

[24]  L. Holm,et al.  The Pfam protein families database , 2005, Nucleic Acids Res..

[25]  R. D. Crotty,et al.  Seasonal variation in cell volume of epilimnetic bacteria , 1988, Microbial Ecology.

[26]  Andrés Moya,et al.  Toward minimal bacterial cells: evolution vs. design , 2008, FEMS microbiology reviews.

[27]  J. Drake,et al.  Genome-Wide Patterns of Nucleotide Substitution Reveal Stringent Functional Constraints on the Protein Sequences of Thermophiles , 2004, Genetics.

[28]  Bernhard Sonnleitner,et al.  Biotechnology of Thermophilic Bacteria — Growth, Products, and Application , 1983, Microbial Activities.

[29]  N. Moran,et al.  Deletional bias and the evolution of bacterial genomes. , 2001, Trends in genetics : TIG.

[30]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

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

[32]  W. Doolittle,et al.  Selfish genes, the phenotype paradigm and genome evolution , 1980, Nature.

[33]  P. Mitchell CHEMIOSMOTIC COUPLING IN OXIDATIVE AND PHOTOSYNTHETIC PHOSPHORYLATION , 1966, Biological reviews of the Cambridge Philosophical Society.

[34]  Patrick Forterre,et al.  A hot story from comparative genomics: reverse gyrase is the only hyperthermophile-specific protein. , 2002, Trends in genetics : TIG.

[35]  Inna Dubchak,et al.  Trends in Prokaryotic Evolution Revealed by Comparison of Closely Related Bacterial and Archaeal Genomes , 2008, Journal of bacteriology.

[36]  R. Nussinov,et al.  How do thermophilic proteins deal with heat? Cell Mol Life Sci , 2001 .

[37]  Effect of Growth Temperature on Fatty Acid Composition of Ten Thermus Strains , 1992, Applied and environmental microbiology.

[38]  E. Koonin,et al.  Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world , 2008, Nucleic acids research.

[39]  T. Coultate,et al.  Energetics of Bacillus stearothermophilus growth: molar growth yield and temperature effects on growth efficiency , 1975, Journal of bacteriology.

[40]  Shibu Yooseph,et al.  Genomic and functional adaptation in surface ocean planktonic prokaryotes , 2010, Nature.

[41]  J. Drake,et al.  The Rate and Character of Spontaneous Mutation in Thermus thermophilus , 2008, Genetics.

[42]  K. Dill,et al.  Physical limits of cells and proteomes , 2011, Proceedings of the National Academy of Sciences.

[43]  K. Katoh,et al.  MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. , 2002, Nucleic acids research.

[44]  William D. Taylor,et al.  Phenotypic Correlates of Genomic DNA Content in Unicellular Eukaryotes and Other Cells , 1983, The American Naturalist.

[45]  E. Birney,et al.  Pfam: the protein families database , 2013, Nucleic Acids Res..

[46]  U. Alon,et al.  Environmental variability and modularity of bacterial metabolic networks , 2007, BMC Evolutionary Biology.

[47]  D. Hartl,et al.  Principles of population genetics , 1981 .

[48]  Andreas Wagner,et al.  Evolutionary Plasticity and Innovations in Complex Metabolic Reaction Networks , 2009, PLoS Comput. Biol..

[49]  R. Varadarajan,et al.  Elucidation of determinants of protein stability through genome sequence analysis , 2000, FEBS letters.

[50]  John W. Drake,et al.  Avoiding Dangerous Missense: Thermophiles Display Especially Low Mutation Rates , 2009, PLoS genetics.

[51]  D Eisenberg,et al.  Transproteomic evidence of a loop-deletion mechanism for enhancing protein thermostability. , 1999, Journal of molecular biology.

[52]  Andreas Wagner,et al.  Energy constraints on the evolution of gene expression. , 2005, Molecular biology and evolution.

[53]  P. Tompa,et al.  Reduction in Structural Disorder and Functional Complexity in the Thermal Adaptation of Prokaryotes , 2010, PloS one.

[54]  H. Kuhn,et al.  Effects of growth temperature on maximal specific growth rate, yield, maintenance, and death rate in glucose-limited continuous culture of the thermophilic Bacillus caldotenax , 1980, European journal of applied microbiology and biotechnology.

[55]  C. Jones,et al.  Energy conservation in the extreme thermophile Thermus thermophilus HB8 , 1982, Archives of Microbiology.