Characterization of exocellular DNA in the oligotrophic ocean

Abstract

Approximately half of the DNA in the open ocean is present outside of living cells. Together, this exocellular DNA (or dissolved DNA; D-DNA) is comprised of truly dissolved “free” DNA (F-DNA), virion encapsidated DNA, and DNA inside of membrane vesicles. It is ubiquitous in nature yet its sources, sinks, and ecological characteristics are largely unknown. One reason for the uncertainty is the methodological limitation that precludes a distinction among the three pools that comprise D-DNA. Using a novel method that provides complete separation of vesicles, viruses, and F-DNA, the first fully sequenced open ocean water-column profile of exocellular DNA was obtained. Euphotic zone F-DNA (75-125 m) contained mostly bacterial and viral sequences, with bacteria dominating in the mesopelagic zone (500-1000 m). A high proportion of mesopelagic zone (500 and 1000 m) F-DNA sequences appeared to originate from surface waters, including a large amount of DNA contributed by high-light Prochlorococcus ecotypes. These results indicate the composition of F-DNA in different regions of the water-column (euphotic and mesopelagic) and suggest potential mechanisms for dissolved organic matter cycling and export. Experiments designed to examine the dynamics of F-DNA suggest that it is produced by viral lysis of microbial cells, and may be consumed by heterotrophic bacteria and protists. Collectively, this research provides novel insights into the microbial origins and dynamics of F-DNA in the open ocean.