Do Atlantic Herring emit sulfur-rich flatulences?

Microbial dimethyl sulfide (DMS) production is very important in the global sulfur cycle, being the major route of sulfur transfer from oceans to atmosphere and then back to the land.

Microbes convert dimethylsulfoniopropionate (DMSP), mainly produced by marine phytoplankton, to DMS by at least three different enzymes that cleave DMSP. One of these, DddL, is a DMSP lyase, whose products are acrylate and DMS, and has thus far only been found in marine α-proteobacteria. Another enzyme, DddP, occurs in α-proteobacteria and in some fungi, but its mechanism of action is unknown. 

The third system involves an acyl CoA transferases encoded by dddD, a gene that occurs in marine γ-proteobacteria and in other bacterial taxa who acquired it by horizontal gene transfer. 

DMSP-catabolizing bacteria have been already isolated from several DMSP-rich environments, including corals, algal blooms, copepods and salt marshes. But this was the first time that such bacteria have been isolated from the gut microflora of a fish, the Atlantic Herring (Clupea harengus) in this case, which feeds on copepods, which in turn consume DMSP-containing phytoplankton.

In this study, after a series of enrichments in DMSP-containing liquid medium, the gut samples were cultured by the authors, on minimal agar plates with DMSP as the sole carbon source. Two different colony types were identified and assayed for DMS production by gas chromatography. The 16S rRNA genes were cloned and then sequenced and the closest (99% identical) relatives were found to be Pseudomonas guineae LMG 24017 and Psychrobacter arenosus R7T. These newly isolated strains were termed J465 and J466, respectively and both produced large amounts of DMS, whose levels were significantly enhanced when cells were pre-grown on 5-mM DMSP. The two strains were also examined for growth on acrylate and 3-hydroxypropionate (one of the earliest catabolites formed after the action of DddD on DMSP), as some other DMSP-catabolizing species can use these compounds. Pseudomonas J465 did not grow on either compound, but Psychrobacter J466 grew on 3-hydroxy-propionate as the sole carbon source. Moreover, acrylate and 3-hydroxy-propionate were found to induce DMS production in Psychrobacter J466, but not in Pseudomonas J465.

To identify the relevant genes in these new isolates, genomic libraries of the two strains were constructed by the authors, mobilizing a wide host-range cosmid into Escherichia coli and screening it for any gene that conferred DMS production to the host. One such cosmid was identified from each library and their inserts were sequenced. Both contained homologues of dddD, which is responsible for the initial step in DMSP catabolism. In addition, several neighboring genes resembled those that occur near dddD in Marinomonas MWYL1, such as dddT (involved in DMSP transport), dddR (DMSP regulation) or dddB and dddC, which are involved in the later stages of DMSP catabolism and which respectively encode polypeptides related to alcohol dehydrogenases and aldehyde dehydrogenases.

In another study on the Atlantic Menhaden (a close relative of the Herring), approximately 65% of the DMSP was shown to be incorporated into the animals’ flesh or excreted unmodified, with very little DMS being actually released when fish were fed DMSP-containing algae. The fate of the remaining 35% of DMSP is unknown, but it can be demethylated, through the action of dmdA (a widespread gene in marine bacteria) in a process that liberates no DMS. Or otherwise the DMS eventually formed by Dddþ bacteria could be catabolized by other DMS-using bacteria.

Dddþ microbes may occur in other marine carnivores such as seabirds, cetaceans, penguins and seals which often use DMS as a chemoattractant to find their prey. So it might even be in the fish’s interest not to emit it, especially since herrings may communicate at night by forming bubbles from their posteriors. 

Further work is thus needed to determine the full range of bacterial types, and the relative contributions of different pathways involved in DMSP catabolism in marine predators and it would be interesting to establish the contributions of such animal's microflora to the global turnover of DMSP.

Reference:

Curson, A.R.J., Sullivan, M.J., Todd, J.D. & Johnston, A.W.B. (2010). Identification of genes for dimethyl sulfide production in bacteria in the gut of Atlantic herring (Clupea harengus). ISME J 4:144–146.