Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean

Brandon K. Swan, Ben Tupper, Alexander Sczyrba, Federico M. Lauro, Manuel Martinez-Garcia, José M. Gonźalez, Haiwei Luo, Jody J. Wright, Zachary C. Landry, Niels W. Hanson, Brian P. Thompson, Nicole J. Poulton, Patrick Schwientek, Silvia G. Acinas, Stephen J. Giovannoni, Mary Ann Moran, Steven J. Hallam, Ricardo Cavicchioli, Tanja Woyke, Ramunas Stepanauskas*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

207 Citations (Scopus)

Abstract

Planktonic bacteria dominate surface ocean biomass and influence global biogeochemical processes, but remain poorly characterized owing to difficulties in cultivation. Using large-scale single cell genomics, we obtained insight into the genome content and biogeography of many bacterial lineages inhabiting the surface ocean. We found that, compared with existing cultures, natural bacterioplankton have smaller genomes, fewer gene duplications, and are depleted in guanine and cytosine, noncoding nucleotides, and genes encoding transcription, signal transduction, and noncytoplasmic proteins. These findings provide strong evidence that genome streamlining and oligotrophy are prevalent features among diverse, freeliving bacterioplankton, whereas existing laboratory cultures consist primarily of copiotrophs. The apparent ubiquity of metabolic specialization and mixotrophy, as predicted from single cell genomes, also may contribute to the difficulty in bacterioplankton cultivation. Using metagenome fragment recruitment against single cell genomes, we show that the global distribution of surface ocean bacterioplankton correlates with temperature and latitude and is not limited by dispersal at the time scales required for nucleotide substitution to exceed the current operational definition of bacterial species. Single cell genomes with highly similar small subunit rRNA gene sequences exhibited significant genomic and biogeographic variability, highlighting challenges in the interpretation of individual gene surveys and metagenome assemblies in environmental microbiology. Our study demonstrates the utility of single cell genomics for gaining an improved understanding of the composition and dynamics of natural microbial assemblages.

Original languageEnglish
Pages (from-to)11463-11468
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume110
Issue number28
DOIs
Publication statusPublished - 9 Jul 2013
Externally publishedYes

Keywords

  • Comparative genomics
  • Marine microbiology
  • Microbial ecology
  • Microbial microevolution
  • Operational taxonomic unit

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