Bacterial Dimethylsulfoniopropionate Degradation Genes in the Oligotrophic North Pacific Subtropical Gyre

Abstract

<jats:title>ABSTRACT</jats:title><jats:p>Dimethylsulfoniopropionate (DMSP) is an organic sulfur compound that is rapidly metabolized by marine bacteria either by cleavage to dimethylsulfide (DMS) or demethylation to 3-methiolpropionate. The abundance and diversity of genes encoding bacterial DMS production (<jats:italic>dddP</jats:italic>) and demethylation (<jats:italic>dmdA</jats:italic>) were measured in the North Pacific subtropical gyre (NPSG) between May 2008 and February 2009 at Station ALOHA (22°45′N, 158°00′W) at two depths: 25 m and the deep chlorophyll maximum (DCM; ∼100 m). The highest abundance of<jats:italic>dmdA</jats:italic>genes was in May 2008 at 25 m, with ∼16.5% of cells harboring a gene in one of the eight subclades surveyed, while the highest abundance of<jats:italic>dddP</jats:italic>genes was in July 2008 at 25 m, with ∼2% of cells harboring a gene. The<jats:italic>dmdA</jats:italic>gene pool was consistently dominated by homologs from SAR11 subclades, which was supported by findings in metagenomic data sets derived from Station ALOHA. Expression of the SAR11<jats:italic>dmdA</jats:italic>genes was low, with typical transcript:gene ratios between 1:350 and 1:1,400. The abundance of DMSP genes was statistically different between 25 m and the DCM and correlated with a number of environmental variables, including primary production, photosynthetically active radiation, particulate DMSP, and DMS concentrations. At 25 m,<jats:italic>dddP</jats:italic>abundance was positively correlated with pigments that are diagnostic of diatoms; at the DCM,<jats:italic>dmdA</jats:italic>abundance was positively correlated with temperature. Based on gene abundance, we hypothesize that SAR11 bacterioplankton dominate DMSP cycling in the oligotrophic NPSG, with lesser but consistent involvement of other members of the bacterioplankton community.</jats:p>

Single-taxon field measurements of bacterial gene regulation controlling DMSP fate

“…dmdA transcripts were B14-fold more abundant than dddP transcripts (5.8 Â 10 5 versus 5.1 Â 10 4 l À 1 ; Figure 1), a difference that may indicate higher inventories of DmdA compared with DddP in the protein pool of HTCC2255 cells, or may reflect different half-lives of the transcripts or proteins. In any case, it is consistent with earlier comparisons of DMSP gene transcripts in seawater (Levine et al, 2012;Varaljay et al, 2012). Although different in absolute numbers, transcript abundances (Figure 1b; R ¼ 0.96) and expression ratios (Supplementary Figure S3A) showed similar patterns for the two genes and were significantly correlated at the beginning (September 28-30) and end of the deployment (October 20-27).…”

Abundance and Distribution of Dimethylsulfoniopropionate Degradation Genes and the Corresponding Bacterial Community Structure at Dimethyl Sulfide Hot Spots in the Tropical and Subtropical Pacific Ocean

“…The average relative abundance of dddP genes obtained in this study (10%) was about two times higher than the values in the GOS metagenomic data (8,12) and, also, about three times higher than the values that were shown in the stations ALOHA and BATS (17,18). The relatively high values (ca.…”

“…These studies showed that the temporal variability in the abundance of DMSP degradation genes in the Sargasso Sea (18) and the North Pacific Ocean (17) was strongly influenced by seasonal changes in primary production, UV radiation, and depth-related environmental parameters, such as particulate DMSP (DMSPp) and DMS concentrations (17,18,26). However, their findings were limited to a …”

“…It was reported that approximately 60% of marine bacteria in the open ocean and coastal waters contain this gene (16). dmdA genes, which are found mainly in members of the SAR11, SAR116, Gammaproteobacteria, and Roseobacter clades (16)(17)(18)(19), can be grouped into five clades and 14 subclades based on the genes' nucleotide sequences (16,20).…”

Evolutionary Ecology of the Marine Roseobacter Clade

“…DMSP acts as a specific chemical cue that attracts motile and chemotactic bacteria, including roseobacters (86). The fact that the Roseobacter clade is only one of two marine bacterial lineages harboring both of the known pathways for DMSP degradation (the other being the SAR116 clade) (87) suggests that this compound may be a particularly important currency in Roseobacter-phytoplankton interactions (75). Finally, polyunsaturated aldehydes (PUAs) produced mainly by diatoms may selectively inhibit Roseobacter members, with evidence for poor growth in the presence of PUAs for strains related to Roseobacter litoralis and Phaeobacter gallaeciensis (88).…”