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

© A.Deniaud / Tara Expéditions

Tara Oceans

Brandon K. Swan (a), Ben Tupper (a), Alexander Sczyrba (b), Federico M. Lauro (c), Manuel Martinez-Garcia (d), José M. González (e), Haiwei Luo (f), Jody J. Wright (g), Zachary C. Landry (h), Niels W. Hanson (i), Brian P. Thompson (a), Nicole J. Poulton (a), Patrick Schwientek (j), Silvia G. Acinas (k), Stephen J. Giovannoni (h), Mary Ann Moran (f), Steven J. Hallam (g,i), Ricardo Cavicchioli (c), Tanja Woyke (j), and Ramunas Stepanauskas (a,1)

a. Bigelow Laboratory for Ocean Sciences, East Boothbay, ME 04544;
b. Center for Biotechnology, Bielefeld University, 33615 Bielefeld, Germany;
c. School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW 2052, Australia;
d. Department of Physiology, Genetics and Microbiology, University of Alicante, 03080 Alicante, Spain;
e. Department of Microbiology, University of La Laguna, ES-38206 La Laguna, Tenerife, Spain;
f. Department of Marine Sciences, University of Georgia, Athens, GA 30602;
g. Microbiology and Immunology, University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
h. Department of Microbiology, Oregon State University, Corvallis, OR 97331;
i. Graduate Program in Bioinformatics, University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
j. US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
k. Department of Marine Biology and Oceanography, Institute of Marine Science, Consejo Superior de Investigaciones Científicas, ES-08003 Barcelona, Spain

Edited by W. Ford Doolittle, Dalhousie University, Halifax, Canada, and approved May 28, 2013 (received for review March 7, 2013)

Capturedecran 2015-01-13a16.38.18

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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, free-living 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.