1. ¹Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA
2. ²Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA

Correspondence: EF DeLong, Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 48-427 MIT, 15 Vassar Street, Cambridge, MA, USA. E-mail: delong@mit.edu

³Current address: School of Civil and Environmental Engineering and School of Biology, Georgia Institute of Technology, Atlanta, GA, USA

Received 3 March 2008; Revised 26 May 2008; Accepted 26 May 2008; Published online 26 June 2008.

Abstract

Microorganisms represent the largest reservoir of biodiversity on Earth, both in numbers and total genetic diversity, but it remains unclear whether this biodiversity is organized in discrete units that correspond to ecologically coherent species. To further explore this question, we examined patterns of genomic diversity in sympatric microbial populations. Analyses of a total of 200 Mb of microbial community genomic DNA sequence recovered from 4000 m depth in the Pacific Ocean revealed discrete sequence-defined populations of Bacteria and Archaea, with intrapopulation genomic sequence divergence ranging from 1% to 6%. The populations appeared to be maintained, at least in part, by intrapopulation genetic exchange (homologous recombination), although the frequency of recombination was estimated to be about three times lower than that observed previously in thermoacidophilic archaeal biofilm populations. Furthermore, the genotypes of a given population were clearly distinguishable from their closest co-occurring relatives based on their relative abundance in situ. The genetic distinctiveness and the matching sympatric abundances imply that these genotypes share similar ecophysiological properties, and therefore may represent fundamental units of microbial diversity in the deep sea. Comparisons to surface-dwelling relatives of the Sargasso Sea revealed that distinct sequence-based clusters were not always detectable, presumably due to environmental variations, further underscoring the important relationship between environmental contexts and genetic mechanisms, which together shape and sustain microbial population structure.