Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer

Talima R Pearson, Philip Giffard, Stephen M Beckstrom-Sternberg, Raymond Auerbach, Heidie Hornstra, Apichai Tuanyok, Erin P. Price, Mindy B. Glass, Benjamin Leadem, James S. Beckstrom-Sternberg, Gerard J Allan, Jeffrey T Foster, David M Wagner, Richard T. Okinaka, Siew H. Sim, Ofori Pearson, Zaining Wu, Jean Chang, Rajinder Kaul, Alex R. HoffmasterThomas S. Brettin, Richard A. Robison, Mark Mayo, Jay E. Gee, Patrick Tan, Bart J. Currie, Paul S Keim

Research output: Contribution to journalArticle

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Abstract

Background: Phylogeographic reconstruction of some bacterial populations is hindered by low diversity coupled with high levels of lateral gene transfer. A comparison of recombination levels and diversity at seven housekeeping genes for eleven bacterial species, most of which are commonly cited as having high levels of lateral gene transfer shows that the relative contributions of homologous recombination versus mutation for Burkholderia pseudomallei is over two times higher than for Streptococcus pneumoniae and is thus the highest value yet reported in bacteria. Despite the potential for homologous recombination to increase diversity, B. pseudomallei exhibits a relative lack of diversity at these loci. In these situations, whole genome genotyping of orthologous shared single nucleotide polymorphism loci, discovered using next generation sequencing technologies, can provide very large data sets capable of estimating core phylogenetic relationships. We compared and searched 43 whole genome sequences of B. pseudomallei and its closest relatives for single nucleotide polymorphisms in orthologous shared regions to use in phylogenetic reconstruction. Results: Bayesian phylogenetic analyses of >14,000 single nucleotide polymorphisms yielded completely resolved trees for these 43 strains with high levels of statistical support. These results enable a better understanding of a separate analysis of population differentiation among >1,700 B. pseudomallei isolates as defined by sequence data from seven housekeeping genes. We analyzed this larger data set for population structure and allele sharing that can be attributed to lateral gene transfer. Our results suggest that despite an almost panmictic population, we can detect two distinct populations of B. pseudomallei that conform to biogeographic patterns found in many plant and animal species. That is, separation along Wallace's Line, a biogeographic boundary between Southeast Asia and Australia. Conclusion: We describe an Australian origin for B. pseudomallei, characterized by a single introduction event into Southeast Asia during a recent glacial period, and variable levels of lateral gene transfer within populations. These patterns provide insights into mechanisms of genetic diversification in B. pseudomallei and its closest relatives, and provide a framework for integrating the traditionally separate fields of population genetics and phylogenetics for other bacterial species with high levels of lateral gene transfer.

Original languageEnglish (US)
Article number78
JournalBMC Biology
Volume7
DOIs
StatePublished - Nov 18 2009

Fingerprint

Burkholderia pseudomallei
Gene transfer
Horizontal Gene Transfer
gene transfer
Genes
Polymorphism
recombination
phylogenetics
polymorphism
Nucleotides
single nucleotide polymorphism
Population
Single Nucleotide Polymorphism
Southeastern Asia
Homologous Recombination
homologous recombination
Essential Genes
phylogeny
genome
South East Asia

ASJC Scopus subject areas

  • Physiology
  • Biotechnology
  • Structural Biology
  • Developmental Biology
  • Plant Science
  • Ecology, Evolution, Behavior and Systematics
  • Cell Biology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer. / Pearson, Talima R; Giffard, Philip; Beckstrom-Sternberg, Stephen M; Auerbach, Raymond; Hornstra, Heidie; Tuanyok, Apichai; Price, Erin P.; Glass, Mindy B.; Leadem, Benjamin; Beckstrom-Sternberg, James S.; Allan, Gerard J; Foster, Jeffrey T; Wagner, David M; Okinaka, Richard T.; Sim, Siew H.; Pearson, Ofori; Wu, Zaining; Chang, Jean; Kaul, Rajinder; Hoffmaster, Alex R.; Brettin, Thomas S.; Robison, Richard A.; Mayo, Mark; Gee, Jay E.; Tan, Patrick; Currie, Bart J.; Keim, Paul S.

In: BMC Biology, Vol. 7, 78, 18.11.2009.

Research output: Contribution to journalArticle

Pearson, TR, Giffard, P, Beckstrom-Sternberg, SM, Auerbach, R, Hornstra, H, Tuanyok, A, Price, EP, Glass, MB, Leadem, B, Beckstrom-Sternberg, JS, Allan, GJ, Foster, JT, Wagner, DM, Okinaka, RT, Sim, SH, Pearson, O, Wu, Z, Chang, J, Kaul, R, Hoffmaster, AR, Brettin, TS, Robison, RA, Mayo, M, Gee, JE, Tan, P, Currie, BJ & Keim, PS 2009, 'Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer', BMC Biology, vol. 7, 78. https://doi.org/10.1186/1741-7007-7-78
Pearson, Talima R ; Giffard, Philip ; Beckstrom-Sternberg, Stephen M ; Auerbach, Raymond ; Hornstra, Heidie ; Tuanyok, Apichai ; Price, Erin P. ; Glass, Mindy B. ; Leadem, Benjamin ; Beckstrom-Sternberg, James S. ; Allan, Gerard J ; Foster, Jeffrey T ; Wagner, David M ; Okinaka, Richard T. ; Sim, Siew H. ; Pearson, Ofori ; Wu, Zaining ; Chang, Jean ; Kaul, Rajinder ; Hoffmaster, Alex R. ; Brettin, Thomas S. ; Robison, Richard A. ; Mayo, Mark ; Gee, Jay E. ; Tan, Patrick ; Currie, Bart J. ; Keim, Paul S. / Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer. In: BMC Biology. 2009 ; Vol. 7.
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abstract = "Background: Phylogeographic reconstruction of some bacterial populations is hindered by low diversity coupled with high levels of lateral gene transfer. A comparison of recombination levels and diversity at seven housekeeping genes for eleven bacterial species, most of which are commonly cited as having high levels of lateral gene transfer shows that the relative contributions of homologous recombination versus mutation for Burkholderia pseudomallei is over two times higher than for Streptococcus pneumoniae and is thus the highest value yet reported in bacteria. Despite the potential for homologous recombination to increase diversity, B. pseudomallei exhibits a relative lack of diversity at these loci. In these situations, whole genome genotyping of orthologous shared single nucleotide polymorphism loci, discovered using next generation sequencing technologies, can provide very large data sets capable of estimating core phylogenetic relationships. We compared and searched 43 whole genome sequences of B. pseudomallei and its closest relatives for single nucleotide polymorphisms in orthologous shared regions to use in phylogenetic reconstruction. Results: Bayesian phylogenetic analyses of >14,000 single nucleotide polymorphisms yielded completely resolved trees for these 43 strains with high levels of statistical support. These results enable a better understanding of a separate analysis of population differentiation among >1,700 B. pseudomallei isolates as defined by sequence data from seven housekeeping genes. We analyzed this larger data set for population structure and allele sharing that can be attributed to lateral gene transfer. Our results suggest that despite an almost panmictic population, we can detect two distinct populations of B. pseudomallei that conform to biogeographic patterns found in many plant and animal species. That is, separation along Wallace's Line, a biogeographic boundary between Southeast Asia and Australia. Conclusion: We describe an Australian origin for B. pseudomallei, characterized by a single introduction event into Southeast Asia during a recent glacial period, and variable levels of lateral gene transfer within populations. These patterns provide insights into mechanisms of genetic diversification in B. pseudomallei and its closest relatives, and provide a framework for integrating the traditionally separate fields of population genetics and phylogenetics for other bacterial species with high levels of lateral gene transfer.",
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AU - Pearson, Talima R

AU - Giffard, Philip

AU - Beckstrom-Sternberg, Stephen M

AU - Auerbach, Raymond

AU - Hornstra, Heidie

AU - Tuanyok, Apichai

AU - Price, Erin P.

AU - Glass, Mindy B.

AU - Leadem, Benjamin

AU - Beckstrom-Sternberg, James S.

AU - Allan, Gerard J

AU - Foster, Jeffrey T

AU - Wagner, David M

AU - Okinaka, Richard T.

AU - Sim, Siew H.

AU - Pearson, Ofori

AU - Wu, Zaining

AU - Chang, Jean

AU - Kaul, Rajinder

AU - Hoffmaster, Alex R.

AU - Brettin, Thomas S.

AU - Robison, Richard A.

AU - Mayo, Mark

AU - Gee, Jay E.

AU - Tan, Patrick

AU - Currie, Bart J.

AU - Keim, Paul S

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N2 - Background: Phylogeographic reconstruction of some bacterial populations is hindered by low diversity coupled with high levels of lateral gene transfer. A comparison of recombination levels and diversity at seven housekeeping genes for eleven bacterial species, most of which are commonly cited as having high levels of lateral gene transfer shows that the relative contributions of homologous recombination versus mutation for Burkholderia pseudomallei is over two times higher than for Streptococcus pneumoniae and is thus the highest value yet reported in bacteria. Despite the potential for homologous recombination to increase diversity, B. pseudomallei exhibits a relative lack of diversity at these loci. In these situations, whole genome genotyping of orthologous shared single nucleotide polymorphism loci, discovered using next generation sequencing technologies, can provide very large data sets capable of estimating core phylogenetic relationships. We compared and searched 43 whole genome sequences of B. pseudomallei and its closest relatives for single nucleotide polymorphisms in orthologous shared regions to use in phylogenetic reconstruction. Results: Bayesian phylogenetic analyses of >14,000 single nucleotide polymorphisms yielded completely resolved trees for these 43 strains with high levels of statistical support. These results enable a better understanding of a separate analysis of population differentiation among >1,700 B. pseudomallei isolates as defined by sequence data from seven housekeeping genes. We analyzed this larger data set for population structure and allele sharing that can be attributed to lateral gene transfer. Our results suggest that despite an almost panmictic population, we can detect two distinct populations of B. pseudomallei that conform to biogeographic patterns found in many plant and animal species. That is, separation along Wallace's Line, a biogeographic boundary between Southeast Asia and Australia. Conclusion: We describe an Australian origin for B. pseudomallei, characterized by a single introduction event into Southeast Asia during a recent glacial period, and variable levels of lateral gene transfer within populations. These patterns provide insights into mechanisms of genetic diversification in B. pseudomallei and its closest relatives, and provide a framework for integrating the traditionally separate fields of population genetics and phylogenetics for other bacterial species with high levels of lateral gene transfer.

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