Genetics, diversity, and distribution of the dimethylsulfoniopropionate (DMSO) demethylase in marine bacterioplankton

Abstract

The flux of dimethylsulfide (DMS) from ocean surface waters is the foremost natural source of sulfur to the atmosphere and influences climate via aerosol formation. Marine bacterioplankton can regulate sulfur flux by converting the precursor dimethylsulfoniopropionate (DMSP) either to DMS via a cleavage pathway or to sulfur compounds that are not climatically active via a demethylation pathway. The gene responsible for demethylating DMSP and diverting the sulfur to the climatically inactive form is identified here, and given the gene designation dmdA. The gene was present in cultured representatives of the Roseobacter and SAR11 taxa, suggesting these may be primary mediators of DMSP demethylation in the ocean. It was also found in the less abundant marine Rhodospiralles and in the OM60 clade of the gammaproteobacteria. Using metagenomic data from the 2007 Global Ocean Sampling (GOS) expedition, it was determined that 58% (±9%) of prokaryotic cells in marine surface waters contain a dmdA homolog, giving them the genetic capability to demethylate DMSP. This metagenomic data also revealed five DmdA protein clades, designated A-E. All clades except Clade B harbor a dmdA from a cultured marine taxon (A, Roseobacter and Rhodospiralles; C and D, SAR11; E, gammaproteobacteria OM60). However, G+C content analysis indicates that most clades are taxonomically heterogeneous. An analysis of dmdA sequences over the course of an induced phytoplankton bloom in Gulf of Mexico surface waters revealed that dmdA diversity is high. Saturation for gene clusters at the 90% similarity level was not reached in a rarefaction analysis of ~90,000 sequences. The representation of the five recognized clades of dmdA did not shift substantially over the course of the phytoplankton bloom compared to non-bloom controls, and there was no evidence for “bloom” and “non-bloom” clades. These results may not be surprising in light of recent data showing similarity in the kinetic parameters of purified proteins from representatives of two different DmdA clades. The pool of dmdA genes was predictable based on the taxonomic composition of the bacterioplankton but not from environmental variables, including DMSP supply and concentration. Together these studies indicate that a large and diverse fraction of marine surface water bacterioplankton are capable of participating in DMSP demethylation, a critical step in the marine sulfur cycle.