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Evolutionary and Genomic Microbiology

Microdiversification of a Pelagic Polynucleobacter Species Is Mainly Driven by Acquisition of Genomic Islands from a Partially Interspecific Gene Pool

Matthias Hoetzinger, Johanna Schmidt, Jitka Jezberová, Ulrike Koll, Martin W. Hahn
Haruyuki Atomi, Editor
Matthias Hoetzinger
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Johanna Schmidt
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Jitka Jezberová
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Ulrike Koll
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Martin W. Hahn
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Haruyuki Atomi
Kyoto University
Roles: Editor
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DOI: 10.1128/AEM.02266-16
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ABSTRACT

Microdiversification of a planktonic freshwater bacterium was studied by comparing 37 Polynucleobacter asymbioticus strains obtained from three geographically separated sites in the Austrian Alps. Genome comparison of nine strains revealed a core genome of 1.8 Mb, representing 81% of the average genome size. Seventy-five percent of the remaining flexible genome is clustered in genomic islands (GIs). Twenty-four genomic positions could be identified where GIs are potentially located. These positions are occupied strain specifically from a set of 28 GI variants, classified according to similarities in their gene content. One variant, present in 62% of the isolates, encodes a pathway for the degradation of aromatic compounds, and another, found in 78% of the strains, contains an operon for nitrate assimilation. Both variants were shown in ecophysiological tests to be functional, thus providing the potential for microniche partitioning. In addition, detected interspecific horizontal exchange of GIs indicates a large gene pool accessible to Polynucleobacter species. In contrast to core genes, GIs are spread more successfully across spatially separated freshwater habitats. The mobility and functional diversity of GIs allow for rapid evolution, which may be a key aspect for the ubiquitous occurrence of Polynucleobacter bacteria.

IMPORTANCE Assessing the ecological relevance of bacterial diversity is a key challenge for current microbial ecology. The polyphasic approach which was applied in this study, including targeted isolation of strains, genome analysis, and ecophysiological tests, is crucial for the linkage of genetic and ecological knowledge. Particularly great importance is attached to the high number of closely related strains which were investigated, represented by genome-wide average nucleotide identities (ANI) larger than 97%. The extent of functional diversification found on this narrow phylogenetic scale is compelling. Moreover, the transfer of metabolically relevant genomic islands between more distant members of the Polynucleobacter community provides important insights toward a better understanding of the evolution of these globally abundant freshwater bacteria.

FOOTNOTES

    • Received 29 August 2016.
    • Accepted 7 November 2016.
    • Accepted manuscript posted online 11 November 2016.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.02266-16 .

  • Copyright © 2017 American Society for Microbiology.

All Rights Reserved .

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Microdiversification of a Pelagic Polynucleobacter Species Is Mainly Driven by Acquisition of Genomic Islands from a Partially Interspecific Gene Pool
Matthias Hoetzinger, Johanna Schmidt, Jitka Jezberová, Ulrike Koll, Martin W. Hahn
Applied and Environmental Microbiology Jan 2017, 83 (3) e02266-16; DOI: 10.1128/AEM.02266-16

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Microdiversification of a Pelagic Polynucleobacter Species Is Mainly Driven by Acquisition of Genomic Islands from a Partially Interspecific Gene Pool
Matthias Hoetzinger, Johanna Schmidt, Jitka Jezberová, Ulrike Koll, Martin W. Hahn
Applied and Environmental Microbiology Jan 2017, 83 (3) e02266-16; DOI: 10.1128/AEM.02266-16
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KEYWORDS

Burkholderiaceae
Genetic Variation
Genome, Bacterial
Genomic Islands
Ponds
Polynucleobacter
ecophysiology
environmental genomics
functional diversity

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