A quantitative account of genomic island acquisitions in prokaryotes

BackgroundMicrobial genomes do not merely evolve through the slow accumulation of mutations, but also, and often more dramatically, by taking up new DNA in a process called horizontal gene transfer. These innovation leaps in the acquisition of new traits can take place via the introgression of single genes, but also through the acquisition of large gene clusters, which are termed Genomic Islands. Since only a small proportion of all the DNA diversity has been sequenced, it can be hard to find the appropriate donors for acquired genes via sequence alignments from databases. In contrast, relative oligonucleotide frequencies represent a remarkably stable genomic signature in prokaryotes, which facilitates compositional comparisons as an alignment-free alternative for phylogenetic relatedness.In this project, we test whether Genomic Islands identified in individual bacterial genomes have a similar genomic signature, in terms of relative dinucleotide frequencies, and can therefore be expected to originate from a common donor species.ResultsWhen multiple Genomic Islands are present within a single genome, we find that up to 28% of these are compositionally very similar to each other, indicative of frequent recurring acquisitions from the same donor to the same acceptor.ConclusionsThis represents the first quantitative assessment of common directional transfer events in prokaryotic evolutionary history. We suggest that many of the resident Genomic Islands per prokaryotic genome originated from the same source, which may have implications with respect to their regulatory interactions, and for the elucidation of the common origins of these acquired gene clusters.

[1]  H. Ochman,et al.  Evolutionary dynamics of full genome content in Escherichia coli , 2000, The EMBO journal.

[2]  Ulrich Dobrindt,et al.  Genomic islands in pathogenic and environmental microorganisms , 2004, Nature Reviews Microbiology.

[3]  Fiona S. L. Brinkman,et al.  The Association of Virulence Factors with Genomic Islands , 2009, PloS one.

[4]  A van der Ende,et al.  An acquisition account of genomic islands based on genome signature comparisons , 2005, BMC Genomics.

[5]  Korine S. E. Ung,et al.  Evidence of a Large Novel Gene Pool Associated with Prokaryotic Genomic Islands , 2005, PLoS genetics.

[6]  Matthew K. Waldor,et al.  Lysogenic Conversion by a Filamentous Phage Encoding Cholera Toxin , 1996, Science.

[7]  Maureen L. Coleman,et al.  Genomic Islands and the Ecology and Evolution of Prochlorococcus , 2006, Science.

[8]  Angela C. M. Luyf,et al.  Compositional discordance between prokaryotic plasmids and host chromosomes , 2006, BMC Genomics.

[9]  Mark J. Pallen,et al.  Bacterial pathogenomics , 2007, Nature.

[10]  K. Jolley,et al.  A chromosomally integrated bacteriophage in invasive meningococci , 2005, The Journal of experimental medicine.

[11]  Rickard Sandberg,et al.  Quantifying the species-specificity in genomic signatures, synonymous codon choice, amino acid usage and G+C content. , 2003, Gene.

[12]  W. W. Lathem,et al.  A Plasminogen-Activating Protease Specifically Controls the Development of Primary Pneumonic Plague , 2007, Science.

[13]  S Karlin,et al.  Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes. , 2001, Trends in microbiology.

[14]  J. Hacker,et al.  Pathogenicity islands and the evolution of microbes. , 2000, Annual review of microbiology.

[15]  G. B. Golding,et al.  Gene amelioration demonstrated: the journey of nascent genes in bacteria. , 2008, Genome.

[16]  P. Forterre,et al.  A hidden reservoir of integrative elements is the major source of recently acquired foreign genes and ORFans in archaeal and bacterial genomes , 2009, Genome Biology.

[17]  Fiona S. L. Brinkman,et al.  Evaluation of genomic island predictors using a comparative genomics approach , 2008, BMC Bioinformatics.

[18]  Angela C. M. Luyf,et al.  The reach of the genome signature in prokaryotes , 2006, BMC Evolutionary Biology.

[19]  Fiona S. L. Brinkman,et al.  Detecting genomic islands using bioinformatics approaches , 2010, Nature Reviews Microbiology.

[20]  S. Karlin,et al.  Dinucleotide relative abundance extremes: a genomic signature. , 1995, Trends in genetics : TIG.

[21]  R. Waaijer,et al.  An in vitro strategy for the selective isolation of anomalous DNA from prokaryotic genomes. , 2004, Nucleic acids research.

[22]  Carsten Damm,et al.  Score-based prediction of genomic islands in prokaryotic genomes using hidden Markov models , 2006, BMC Bioinformatics.

[23]  Fiona S. L. Brinkman,et al.  IslandViewer: an integrated interface for computational identification and visualization of genomic islands , 2009, Bioinform..

[24]  Antoine H. C. van Kampen,et al.  delta rho-Web, an online tool to assess composition similarity of individual nucleic acid sequences , 2005, Bioinform..

[25]  Kelly P. Williams,et al.  Islander: a database of integrative islands in prokaryotic genomes, the associated integrases and their DNA site specificities , 2004, Nucleic Acids Res..

[26]  Steven J. M. Jones,et al.  IslandPath: aiding detection of genomic islands in prokaryotes , 2003, Bioinform..

[27]  Frank Oliver Glöckner,et al.  TETRA: a web-service and a stand-alone program for the analysis and comparison of tetranucleotide usage patterns in DNA sequences , 2004, BMC Bioinformatics.

[28]  P. Deschavanne,et al.  Genomic signature: characterization and classification of species assessed by chaos game representation of sequences. , 1999, Molecular biology and evolution.

[29]  Howard Ochman,et al.  The Emergence and Fate of Horizontally Acquired Genes in Escherichia coli , 2008, PLoS Comput. Biol..

[30]  Rainer Merkl,et al.  SIGI: score-based identification of genomic islands , 2004, BMC Bioinformatics.

[31]  Rainer Merkl,et al.  The genome sequence of Clostridium tetani, the causative agent of tetanus disease , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R. Sandberg,et al.  Capturing whole-genome characteristics in short sequences using a naïve Bayesian classifier. , 2001, Genome research.

[33]  E. Skjerve,et al.  Examination of Genome Homogeneity in Prokaryotes Using Genomic Signatures , 2009, PloS one.

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

[35]  R. Amann,et al.  Application of tetranucleotide frequencies for the assignment of genomic fragments. , 2004, Environmental microbiology.

[36]  J Hacker,et al.  Pathogenicity islands: the tip of the iceberg. , 2001, Microbes and infection.

[37]  H. Ochman,et al.  Amelioration of Bacterial Genomes: Rates of Change and Exchange , 1997, Journal of Molecular Evolution.

[38]  Hanah Margalit,et al.  Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence , 2008, Nucleic acids research.

[39]  Ren Zhang,et al.  A systematic method to identify genomic islands and its applications in analyzing the genomes of Corynebacterium glutamicum and Vibrio vulnificus CMCP6 chromosome I , 2004, Bioinform..