Bacteria are important dimethylsulfoniopropionate producers in marine aphotic and high-pressure environments

Abstract

Dimethylsulfoniopropionate (DMSP) is an important marine osmolyte. Aphotic environments are only recently being considered as potential contributors to global DMSP production. Here, our Mariana Trench study reveals a typical seawater DMSP/dimethylsulfide (DMS) profile, with highest concentrations in the euphotic zone and decreased but consistent levels below. The genetic potential for bacterial DMSP synthesis via the dsyB gene and its transcription is greater in the deep ocean, and is highest in the sediment.s DMSP catabolic potential is present throughout the trench waters, but is less prominent below 8000 m, perhaps indicating a preference to store DMSP in the deep for stress protection. Deep ocean bacterial isolates show enhanced DMSP production under increased hydrostatic pressure. Furthermore, bacterial dsyB mutants are less tolerant of deep ocean pressures than wild-type strains. Thus, we propose a physiological function for DMSP in hydrostatic pressure protection, and that bacteria are key DMSP producers in deep seawater and sediment.

Fig. 1. Depth profile of DMSP, DMS, and chlorophyll a in Challenger Deep seawater and sediment samples.

a Sampling sites and depths. b Total DMSP concentrations in seawater and sediment samples. c Total DMS and chlorophyll a in seawater samples. Data in b are presented as means ± SD.

Fig. 2. The importance of DMSP synthesis genes in Challenger Deep samples.

a Percentage of bacteria with DsyB and MmtN (left), and profiles of the bacterial communities harboring them (right) in depth-profiled samples determined by metagenomic analysis. Sample names are defined by size fraction and sampling depth, e.g., FL10500 is the free-living fraction at 10,500 m. FL: free-living; PA: particle-associated. b Absolute abundance of 16S rRNA and dsyB gene copies in the seawater and sediment at various depths, determined by qPCR. c Transcript abundance of dsyB in FL water and sediment samples, and of mmtN in sediment from different depths. d The effects of hydrostatic pressure on DMSP production. Left Y axis indicate strains ZYF240 (Pseudooceanicola nanhaiensis isolated from 8000 m seawater of the Mariana Trench), ZYF612 (Labrenzia aggregata isolated from 9600 m seawater of the Mariana Trench), and Marinibacterium sp. strain La6. Right Y axis indicates Pelagibaca bermudensis strain J526. e The survival of DMSP-producing bacteria J526 and La6 (wild type), dsyB⁻ mutant variants, dsyB⁻ mutants containing cloned dsyB, and dsyB⁻ mutant isolates supplied with DMSP, after incubation at 60 MPa for 10 days. Data in e, f are presented as means ± SD.

Fig. 3. The abundance of DMSP catabolic genes in Challenger Deep water samples.

a The relative abundance of bacterial cells containing the DMSP demethylation gene dmdA at different depths (left), with the top nine affiliated orders containing them shown in the heat map (right). Genera belonging to Gammaproteobacteria are labeled in pink; those in black font are Alphaproteobacteria or Actinobacteria. b Absolute abundance of dmdA in the seawater and sediment at various depths, as determined by qPCR. c The relative abundance of bacterial cells containing DMSP cleavage genes at different depths (left) with the top four affiliated genera of each gene shown in the heat map (right). Genera belonging to Gammaproteobacteria are labeled in pink; those in black font are Alphaproteobacteria. FL: free-living; PA: particle-associated.

Fig. 4. The proposed cycling of DMSP throughout the water column.

Phytoplankton are the major contributors to DMSP production in the photic zone, whereas in aphotic zones, where no sunlight penetrates, heterotrophic bacteria likely contribute significantly to DMSP production. DMSP produced in the surface waters can sink to lower levels. Sedimentary DMSP levels are two to three orders of magnitude higher, per equivalent mass, than the seawater, and are also most likely produced by bacteria. The relative abundance of DMSP catabolic genes was lowest in the deepest water and sediment samples, and DMSP can play a role in protecting bacteria against increased hydrostatic pressure in such deep waters and sediment. DMSP and DMS produced in the surface water is labeled in blue. Deep-ocean DMSP and DMS is in yellow and sedimentary DMSP is labeled in brown. Values in this figure represent DMSP or DMS concentration ranges determined by this study.