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

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.This work was supported by National Science Foundation Grants EF-826924 (to R.S.), OCE-821374 (to R.S.), and OCE-1232982 (to R.S. and B.K.S.); US Department of Energy (DOE) JGI 2011 Microbes Program Grant CSP 387 (to R.S., B.K.S., S.G., M.A.M., F.M.L., R.C. and S.G.A.); the Gordon and Betty Moore Foundation (M.A.M.); Spanish Ministry of Science and Innovation Grant CGL2011-26848/BOS (to S.G.A) and CONSOLIDER-INGENIO2010 Program Grant CSD2008-00077 (to S.G.A. and J.M.G.); the Natural Sciences and Engineering Research Council of Canada (NSERC); the Canada Foundation for Innovation, and the Canadian Institute for Advanced Research (CIFAR; S.J.H.). J.J.W. was supported by NSERC. Research activities of R.C. and F.M.L. are supported by the Australian Research Council, and research activities of R.C. are supported by the Australian Antarctic Science program. Work conducted by the DOE Joint Genome Institute is supported by the DOE’s Office of Science under Contract DE-AC02-05CH11231. This is contribution no. 006 of the Tara Oceans Expedition 2009–2012