Home LiteratureArticle Details
PMID: 18632554 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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

Dagan T, Artzy-Randrup Y, Martin W

Abstract

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.

MeSH Terms
Archaea/genetics Bacteria/genetics Bacterial Proteins/genetics Biological Evolution Gene Regulatory Networks Gene Transfer, Horizontal Genome, Archaeal Genome, Bacterial Models, Genetic Phylogeny Prokaryotic Cells
Chemicals
Bacterial Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Dagan Tal
Institut für Botanik III, Heinrich-Heine Universität Düsseldorf, Universitätsstrasse 1, 40225 Düsseldorf, Germany. tal.dagan@uni-duesseldorf.de
Artzy-Randrup Yael
Martin William
References (44)
44 references, click to expand
  1. Lateral gene transfer and the origins of prokaryotic groups.
    Annu Rev Genet. 2003;37:283-328 PMID: 14616063
  2. Whole-genome analysis of photosynthetic prokaryotes.
    Science. 2002 Nov 22;298(5598):1616-20 PMID: 12446909
  3. Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12.
    DNA Res. 2001 Feb 28;8(1):11-22 PMID: 11258796
  4. The ring of life provides evidence for a genome fusion origin of eukaryotes.
    Nature. 2004 Sep 9;431(7005):152-5 PMID: 15356622
  5. Lessons from studies of Symbiobacterium thermophilum, a unique syntrophic bacterium.
    Biosci Biotechnol Biochem. 2007 May;71(5):1115-21 PMID: 17485837
  6. Network thinking in ecology and evolution.
    Trends Ecol Evol. 2005 Jun;20(6):345-53 PMID: 16701391
  7. Generating uniformly distributed random networks.
    Phys Rev E Stat Nonlin Soft Matter Phys. 2005 Nov;72(5 Pt 2):056708 PMID: 16383786
  8. Phylogenomics and the reconstruction of the tree of life.
    Nat Rev Genet. 2005 May;6(5):361-75 PMID: 15861208
  9. Importance of widespread gene transfer agent genes in alpha-proteobacteria.
    Trends Microbiol. 2007 Feb;15(2):54-62 PMID: 17184993
  10. Pattern pluralism and the Tree of Life hypothesis.
    Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2043-9 PMID: 17261804
  11. Biased biological functions of horizontally transferred genes in prokaryotic genomes.
    Nat Genet. 2004 Jul;36(7):760-6 PMID: 15208628
  12. The net of life: reconstructing the microbial phylogenetic network.
    Genome Res. 2005 Jul;15(7):954-9 PMID: 15965028
  13. Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids?
    Genome Biol. 2007;8(6):R99 PMID: 17547748
  14. Functional cartography of complex metabolic networks.
    Nature. 2005 Feb 24;433(7028):895-900 PMID: 15729348
  15. Scaling theory of transport in complex biological networks.
    Proc Natl Acad Sci U S A. 2007 May 8;104(19):7746-51 PMID: 17470793
  16. Finding community structure in networks using the eigenvectors of matrices.
    Phys Rev E Stat Nonlin Soft Matter Phys. 2006 Sep;74(3 Pt 2):036104 PMID: 17025705
  17. Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution.
    Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):870-5 PMID: 17213324
  18. Evaluation of clustering algorithms for protein-protein interaction networks.
    BMC Bioinformatics. 2006 Nov 06;7:488 PMID: 17087821
  19. A marine microbial consortium apparently mediating anaerobic oxidation of methane.
    Nature. 2000 Oct 5;407(6804):623-6 PMID: 11034209
  20. Adaptive evolution of bacterial metabolic networks by horizontal gene transfer.
    Nat Genet. 2005 Dec;37(12):1372-5 PMID: 16311593
  21. Orthologs, paralogs, and evolutionary genomics.
    Annu Rev Genet. 2005;39:309-38 PMID: 16285863
  22. Uncovering the overlapping community structure of complex networks in nature and society.
    Nature. 2005 Jun 9;435(7043):814-8 PMID: 15944704
  23. Phylogenetic classification and the universal tree.
    Science. 1999 Jun 25;284(5423):2124-9 PMID: 10381871
  24. Highways of gene sharing in prokaryotes.
    Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14332-7 PMID: 16176988
  25. Network motifs: theory and experimental approaches.
    Nat Rev Genet. 2007 Jun;8(6):450-61 PMID: 17510665
  26. Genome-wide experimental determination of barriers to horizontal gene transfer.
    Science. 2007 Nov 30;318(5855):1449-52 PMID: 17947550
  27. Application of phylogenetic networks in evolutionary studies.
    Mol Biol Evol. 2006 Feb;23(2):254-67 PMID: 16221896
  28. Symbiosis as an adaptive process and source of phenotypic complexity.
    Proc Natl Acad Sci U S A. 2007 May 15;104 Suppl 1:8627-33 PMID: 17494762
  29. Visualizing and assessing phylogenetic congruence of core gene sets: a case study of the gamma-proteobacteria.
    Mol Biol Evol. 2006 May;23(5):1019-30 PMID: 16495350
  30. Phylogenetic reconstruction and lateral gene transfer.
    Trends Microbiol. 2004 Sep;12(9):406-11 PMID: 15337161
  31. The COG database: a tool for genome-scale analysis of protein functions and evolution.
    Nucleic Acids Res. 2000 Jan 1;28(1):33-6 PMID: 10592175
  32. Toward automatic reconstruction of a highly resolved tree of life.
    Science. 2006 Mar 3;311(5765):1283-7 PMID: 16513982
  33. An efficient algorithm for large-scale detection of protein families.
    Nucleic Acids Res. 2002 Apr 1;30(7):1575-84 PMID: 11917018
  34. Lethality and centrality in protein networks.
    Nature. 2001 May 3;411(6833):41-2 PMID: 11333967
  35. Prokaryotic evolution in light of gene transfer.
    Mol Biol Evol. 2002 Dec;19(12):2226-38 PMID: 12446813
  36. The prokaryotic tree of life: past, present... and future?
    Trends Ecol Evol. 2008 May;23(5):276-81 PMID: 18367290
  37. Genome phylogeny based on gene content.
    Nat Genet. 1999 Jan;21(1):108-10 PMID: 9916801
  38. Alternative methods for concatenation of core genes indicate a lack of resolution in deep nodes of the prokaryotic phylogeny.
    Mol Biol Evol. 2008 Jan;25(1):83-91 PMID: 17940208
  39. The evolutionary origin of Xanthomonadales genomes and the nature of the horizontal gene transfer process.
    Mol Biol Evol. 2006 Nov;23(11):2049-57 PMID: 16882701
  40. Mechanisms of, and barriers to, horizontal gene transfer between bacteria.
    Nat Rev Microbiol. 2005 Sep;3(9):711-21 PMID: 16138099
  41. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  42. Non-random coextinctions in phylogenetically structured mutualistic networks.
    Nature. 2007 Aug 23;448(7156):925-8 PMID: 17713534
  43. Lateral gene transfer and the nature of bacterial innovation.
    Nature. 2000 May 18;405(6784):299-304 PMID: 10830951
  44. How big is the iceberg of which organellar genes in nuclear genomes are but the tip?
    Philos Trans R Soc Lond B Biol Sci. 2003 Jan 29;358(1429):39-57; discussion 57-8 PMID: 12594917
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2008-07-22
Epub
2008-00-16
Pages
10039-44
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2474566
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com