Microbial co-habitation and lateral gene transfer: what transposases can tell us

BackgroundDetermining the habitat range for various microbes is not a simple, straightforward matter, as habitats interlace, microbes move between habitats, and microbial communities change over time. In this study, we explore an approach using the history of lateral gene transfer recorded in microbial genomes to begin to answer two key questions: where have you been and who have you been with?ResultsAll currently sequenced microbial genomes were surveyed to identify pairs of taxa that share a transposase that is likely to have been acquired through lateral gene transfer. A microbial interaction network including almost 800 organisms was then derived from these connections. Although the majority of the connections are between closely related organisms with the same or overlapping habitat assignments, numerous examples were found of cross-habitat and cross-phylum connections.ConclusionsWe present a large-scale study of the distributions of transposases across phylogeny and habitat, and find a significant correlation between habitat and transposase connections. We observed cases where phylogenetic boundaries are traversed, especially when organisms share habitats; this suggests that the potential exists for genetic material to move laterally between diverse groups via bridging connections. The results presented here also suggest that the complex dynamics of microbial ecology may be traceable in the microbial genomes.

[1]  G. Schoolnik,et al.  Genomic and Phenotypic Diversity of Coastal Vibrio cholerae Strains Is Linked to Environmental Factors , 2007, Applied and Environmental Microbiology.

[2]  I-Min A. Chen,et al.  The Genomes On Line Database (GOLD) in 2007: status of genomic and metagenomic projects and their associated metadata , 2007, Nucleic Acids Res..

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

[4]  Eugene W. Myers,et al.  Basic local alignment search tool. Journal of Molecular Biology , 1990 .

[5]  Patricia Siguier,et al.  ISfinder: the reference centre for bacterial insertion sequences , 2005, Nucleic Acids Res..

[6]  S. Ishii,et al.  Cladophora (Chlorophyta) spp. Harbor Human Bacterial Pathogens in Nearshore Water of Lake Michigan , 2006, Applied and Environmental Microbiology.

[7]  Konstantinos T. Konstantinidis,et al.  Towards a Genome-Based Taxonomy for Prokaryotes , 2005, Journal of bacteriology.

[8]  David DeShazer,et al.  Genomic patterns of pathogen evolution revealed by comparison of Burkholderia pseudomallei, the causative agent of melioidosis, to avirulent Burkholderia thailandensis , 2006, BMC Microbiology.

[9]  P. Tchounwou,et al.  The Seasonality of Fecal Coliform Bacteria Pollution and its Influence on Closures of Shellfish Harvesting Areas in Mississippi Sound , 2005, International journal of environmental research and public health.

[10]  M. Eriksson,et al.  Degradation of Polycyclic Aromatic Hydrocarbons at Low Temperature under Aerobic and Nitrate-Reducing Conditions in Enrichment Cultures from Northern Soils , 2003, Applied and Environmental Microbiology.

[11]  Jason A. Papin,et al.  * Corresponding authors , 2006 .

[12]  J. Banfield,et al.  Community structure and metabolism through reconstruction of microbial genomes from the environment , 2004, Nature.

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

[14]  C. Meisner,et al.  Virulence of Burkholderia cepacia complex strains in gp91phox−/− mice , 2007, Cellular microbiology.

[15]  K. Klose,et al.  Vibrio cholerae and cholera: out of the water and into the host. , 2002, FEMS microbiology reviews.

[16]  Natalia N. Ivanova,et al.  Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite , 2007, Nature.

[17]  H. Heuer,et al.  Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids. , 2008, FEMS microbiology ecology.

[18]  Rudolf Amann,et al.  Bacterial Community Dynamics during Start-Up of a Trickle-Bed Bioreactor Degrading Aromatic Compounds , 1998, Applied and Environmental Microbiology.

[19]  D. Griffin,et al.  Atmospheric transport of mold spores in clouds of desert dust. , 2003, Archives of environmental health.

[20]  Norma P. Tavakoli,et al.  Transposition is modulated by a diverse set of host factors in Escherichia coli and is stimulated by nutritional stress , 2005, Molecular microbiology.

[21]  W. Ludwig,et al.  SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB , 2007, Nucleic acids research.

[22]  H. Ochman,et al.  The ancestry of insertion sequences common to Escherichia coli and Salmonella typhimurium , 1993, Journal of bacteriology.

[23]  P. Watnick,et al.  Vibrio cholerae Infection of Drosophila melanogaster Mimics the Human Disease Cholera , 2005, PLoS pathogens.

[24]  Andreas Wagner,et al.  Periodic extinctions of transposable elements in bacterial lineages: evidence from intragenomic variation in multiple genomes. , 2006, Molecular biology and evolution.

[25]  Nikos Kyrpides,et al.  The Genomes On Line Database (GOLD) in 2007: status of genomic and metagenomic projects and their associated metadata , 2007, Nucleic Acids Res..

[26]  C. Panis,et al.  Characterization of a mosaic ISS1 element and evidence for the recent horizontal transfer of two different types of ISS1 between Streptococcus thermophilus and Lactococcus lactis. , 1996, Gene.

[27]  I-Min A. Chen,et al.  The integrated microbial genomes (IMG) system in 2007: data content and analysis tool extensions , 2007, Nucleic Acids Res..

[28]  Andrés Moya,et al.  Estimating the extent of horizontal gene transfer in metagenomic sequences , 2008, BMC Genomics.

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

[30]  J. Roth,et al.  Ohno's dilemma: Evolution of new genes under continuous selection , 2007, Proceedings of the National Academy of Sciences.

[31]  T. Whittam,et al.  Genetic diversity and population structure of Escherichia coli isolated from freshwater beaches. , 2007, Environmental microbiology.

[32]  Darren A. Natale,et al.  The COG database: an updated version includes eukaryotes , 2003, BMC Bioinformatics.

[33]  N. White,et al.  Quantitative recovery of Burkholderia pseudomallei from soil in Thailand. , 1995, Transactions of the Royal Society of Tropical Medicine and Hygiene.

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

[35]  Inna Dubchak,et al.  The integrated microbial genomes (IMG) system , 2005, Nucleic Acids Res..

[36]  T. Yomo,et al.  Insertion sequence IS6100 on plasmid pOAD2, which degrades nylon oligomers , 1994, Journal of bacteriology.

[37]  M. Pérez‐Losada,et al.  Population genetics of microbial pathogens estimated from multilocus sequence typing (MLST) data. , 2006, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[38]  Peer Bork,et al.  Medusa: a simple tool for interaction graph analysis , 2005, Bioinform..

[39]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[40]  B. Raymond,et al.  Ecological consequences of ingestion of Bacillus cereus on Bacillus thuringiensis infections and on the gut flora of a lepidopteran host. , 2008, Journal of invertebrate pathology.