Network analyses structure genetic diversity in independent genetic worlds

DNA flows between chromosomes and mobile elements, following rules that are poorly understood. This limited knowledge is partly explained by the limits of current approaches to study the structure and evolution of genetic diversity. Network analyses of 119,381 homologous DNA families, sampled from 111 cellular genomes and from 165,529 phage, plasmid, and environmental virome sequences, offer challenging insights. Our results support a disconnected yet highly structured network of genetic diversity, revealing the existence of multiple “genetic worlds.” These divides define multiple isolated groups of DNA vehicles drawing on distinct gene pools. Mathematical studies of the centralities of these worlds’ subnetworks demonstrate that plasmids, not viruses, were key vectors of genetic exchange between bacterial chromosomes, both recently and in the past. Furthermore, network methodology introduces new ways of quantifying current sampling of genetic diversity.

[1]  W. Whitman The Modern Concept of the Procaryote , 2009, Journal of bacteriology.

[2]  Gary D. Bader,et al.  An automated method for finding molecular complexes in large protein interaction networks , 2003, BMC Bioinformatics.

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

[4]  W. Martin,et al.  Getting a better picture of microbial evolution en route to a network of genomes , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  Tal Dagan,et al.  Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution , 2008, Proceedings of the National Academy of Sciences.

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

[7]  S. Tringe,et al.  Comparative Metagenomics of Microbial Communities , 2004, Science.

[8]  Steven G. Cresawn,et al.  Comparative genomics of the mycobacteriophages: insights into bacteriophage evolution. , 2008, Research in microbiology.

[9]  Andreas Wilke,et al.  phylogenetic and functional analysis of metagenomes , 2022 .

[10]  James O. McInerney,et al.  The network of life: genome beginnings and evolution , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  Naryttza N. Diaz,et al.  The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes , 2005, Nucleic acids research.

[12]  P. Sneath The application of computers to taxonomy. , 1957, Journal of general microbiology.

[13]  Søren J. Sørensen,et al.  Conjugative plasmids: vessels of the communal gene pool , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[14]  Folker Meyer,et al.  37. The Metagenomics RAST Server: A Public Resource for the Automatic Phylogenetic and Functional Analysis of Metagenomes , 2011 .

[15]  A. Pühler,et al.  The 64 508 bp IncP-1beta antibiotic multiresistance plasmid pB10 isolated from a waste-water treatment plant provides evidence for recombination between members of different branches of the IncP-1beta group. , 2003, Microbiology.

[16]  F. Rohwer,et al.  Viruses manipulate the marine environment , 2009, Nature.

[17]  H. Brüssow The not so universal tree of life or the place of viruses in the living world , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[18]  K. Jefferson,et al.  What drives bacteria to produce a biofilm? , 2004, FEMS microbiology letters.

[19]  Gipsi Lima-Mendez,et al.  Reticulate representation of evolutionary and functional relationships between phage genomes. , 2008, Molecular biology and evolution.

[20]  Pietro Liò,et al.  Analysis of plasmid genes by phylogenetic profiling and visualization of homology relationships using Blast2Network , 2008, BMC Bioinformatics.

[21]  P. Mieczkowski,et al.  Mosaic Structure of p1658/97, a 125-Kilobase Plasmid Harboring an Active Amplicon with the Extended-Spectrum β-Lactamase Gene blaSHV-5 , 2007, Antimicrobial Agents and Chemotherapy.

[22]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

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

[24]  M. Newman,et al.  Hierarchical structure and the prediction of missing links in networks , 2008, Nature.

[25]  U. Brandes A faster algorithm for betweenness centrality , 2001 .

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

[27]  J. Ravel,et al.  Insights into the Environmental Resistance Gene Pool from the Genome Sequence of the Multidrug-Resistant Environmental Isolate Escherichia coli SMS-3-5 , 2008, Journal of bacteriology.

[28]  P. Bork,et al.  A Molecular Study of Microbe Transfer between Distant Environments , 2008, PloS one.