Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution

Lateral gene transfer is an important mechanism of natural variation among prokaryotes, but the significance of its quantitative contribution to genome evolution is debated. Here, we report networks that capture both vertical and lateral components of evolutionary history among 539,723 genes distributed across 181 sequenced prokaryotic genomes. Partitioning of these networks by an eigenspectrum analysis identifies community structure in prokaryotic gene-sharing networks, the modules of which do not correspond to a strictly hierarchical prokaryotic classification. Our results indicate that, on average, at least 81 ± 15% of the genes in each genome studied were involved in lateral gene transfer at some point in their history, even though they can be vertically inherited after acquisition, uncovering a substantial cumulative effect of lateral gene transfer on longer evolutionary time scales.

[1]  Christopher M Thomas,et al.  Mechanisms of, and Barriers to, Horizontal Gene Transfer between Bacteria , 2005, Nature Reviews Microbiology.

[2]  Peer Bork,et al.  Genome-Wide Experimental Determination of Barriers to Horizontal Gene Transfer , 2007, Science.

[3]  L. Stone,et al.  Generating uniformly distributed random networks. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[4]  E. Koonin.  Orthologs, Paralogs, and Evolutionary Genomics 1 , 2005 .

[5]  M. Newman,et al.  Finding community structure in networks using the eigenvectors of matrices. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[6]  W. Doolittle,et al.  Lateral gene transfer and the origins of prokaryotic groups. , 2003, Annual review of genetics.

[7]  Olaf Pfannkuche,et al.  A marine microbial consortium apparently mediating anaerobic oxidation of methane , 2000, Nature.

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

[9]  Andrew S Lang,et al.  Importance of widespread gene transfer agent genes in alpha-proteobacteria. , 2007, Trends in microbiology.

[10]  T. Beppu,et al.  Lessons from Studies of Symbiobacterium thermophilum, a Unique Syntrophic Bacterium , 2007, Bioscience, biotechnology, and biochemistry.

[11]  H. Matsuda,et al.  Biased biological functions of horizontally transferred genes in prokaryotic genomes , 2004, Nature Genetics.

[12]  E. Koonin.  Orthologs, paralogs, and evolutionary genomics. , 2005, Annual review of genetics.

[13]  R. Burt.  Models of Network Structure , 1980 .

[14]  T. Vicsek,et al.  Uncovering the overlapping community structure of complex networks in nature and society , 2005, Nature.

[15]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[16]  R. Guimerà,et al.  Functional cartography of complex metabolic networks , 2005, Nature.

[17]  Leon Goldovsky,et al.  The net of life: reconstructing the microbial phylogenetic network. , 2005, Genome research.

[18]  Michael Y. Galperin,et al.  The COG database: a tool for genome-scale analysis of protein functions and evolution , 2000, Nucleic Acids Res..

[19]  J. Lake,et al.  The ring of life provides evidence for a genome fusion origin of eukaryotes , 2004, Nature.

[20]  N. Moran,et al.  Symbiosis as an adaptive process and source of phenotypic complexity , 2007, Proceedings of the National Academy of Sciences.

[21]  W. Martin,et al.  Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution , 2007, Proceedings of the National Academy of Sciences.

[22]  S. Havlin,et al.  Scaling theory of transport in complex biological networks , 2007, Proceedings of the National Academy of Sciences.

[23]  R. Carter.  11 – IT and society , 1991 .

[24]  W. Doolittle,et al.  Prokaryotic evolution in light of gene transfer. , 2002, Molecular biology and evolution.

[25]  Patrick C Phillips,et al.  Network thinking in ecology and evolution. , 2005, Trends in ecology & evolution.

[26]  J. McInerney,et al.  The prokaryotic tree of life: past, present... and future? , 2008, Trends in ecology & evolution.

[27]  W. Doolittle,et al.  Alternative methods for concatenation of core genes indicate a lack of resolution in deep nodes of the prokaryotic phylogeny. , 2007, Molecular biology and evolution.

[28]  M. P. Cummings.  PHYLIP (Phylogeny Inference Package) , 2004 .

[29]  U. Alon.  Network motifs: theory and experimental approaches , 2007, Nature Reviews Genetics.

[30]  M. Hattori,et al.  Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. , 2001, DNA research : an international journal for rapid publication of reports on genes and genomes.

[31]  Mark E. J. Newman,et al.  The Structure and Function of Complex Networks , 2003, SIAM Rev..

[32]  W. Doolittle,et al.  Visualizing and assessing phylogenetic congruence of core gene sets: a case study of the gamma-proteobacteria. , 2006, Molecular biology and evolution.

[33]  J. Beatty,et al.  Importance of widespread gene transfer agent genes in α-proteobacteria , 2007 .

[34]  Eric Bapteste,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:Pattern pluralism and the Tree of Life hypothesis , 2007 .

[35]  Mark E. J. Newman,et al.  Power-Law Distributions in Empirical Data , 2007, SIAM Rev..

[36]  Jacques van Helden,et al.  Evaluation of clustering algorithms for protein-protein interaction networks , 2006, BMC Bioinformatics.

[37]  B. Snel,et al.  Genome phylogeny based on gene content , 1999, Nature Genetics.

[38]  B. Snel,et al.  Toward Automatic Reconstruction of a Highly Resolved Tree of Life , 2006, Science.

[39]  J. Peter Gogarten,et al.  Whole-Genome Analysis of Photosynthetic Prokaryotes , 2002, Science.

[40]  F. Delsuc,et al.  Phylogenomics and the reconstruction of the tree of life , 2005, Nature Reviews Genetics.

[41]  Yan Boucher,et al.  Phylogenetic reconstruction and lateral gene transfer. , 2004, Trends in microbiology.

[42]  Anton J. Enright,et al.  An efficient algorithm for large-scale detection of protein families. , 2002, Nucleic acids research.

[43]  Jordi Bascompte,et al.  Non-random coextinctions in phylogenetically structured mutualistic networks , 2007, Nature.

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

[45]  Albert-László Barabási,et al.  Internet: Diameter of the World-Wide Web , 1999, Nature.

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

[47]  L. Orgel,et al.  Phylogenetic Classification and the Universal Tree , 1999 .

[48]  Jinling Huang,et al.  Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? , 2007, Genome Biology.

[49]  D. Huson,et al.  Application of phylogenetic networks in evolutionary studies. , 2006, Molecular biology and evolution.

[50]  Timothy J. Harlow,et al.  Highways of gene sharing in prokaryotes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[51]  W. Doolittle,et al.  How big is the iceberg of which organellar genes in nuclear genomes are but the tip? , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[52]  A. Barabasi,et al.  Lethality and centrality in protein networks , 2001, Nature.

[53]  A. Moya,et al.  The evolutionary origin of Xanthomonadales genomes and the nature of the horizontal gene transfer process. , 2006, Molecular biology and evolution.