An interesting paper was recently published by Durham et al. in PNAS: Cryptic carbon and sulfur cycling between surface ocean plankton. The all-star author list includes members of the Armbrust Lab at the University of Washington, the Moran Lab at the University of Georgia, Athens, and the Van Mooy Lab at WHOI.
For a long time a compound known as dimethylsulfoniopropionate (DMSP) has been recognized as a major component of both the reduced sulfur and dissolved organic carbon (DOC) pools in the ocean. As described here, DMSP is produced by phytoplankton in response to various environmental stresses, and is readily consumed by many marine bacteria (some bacteria produce DMS, a climatically active volatile, as a byproduct of this consumption). In this way it is an excellent example of the microbial loop; dissolved DMSP cannot be directly consumed by zooplankton, but it can be consumed by higher trophic levels after repackaging in microbial biomass. Presumably, however, DMSP is only one of many important components of the DOC pool. Determining the other major components turns out to be a rather difficult task. There are two ways a researcher might go about this.
Figure from Durham et al., 2014 and shows the pathway for the intracellular catabolism of DHPS by R. pomeroyi, ending with the excretion of bisulfite.
First, a chemist might try and analyze the different compounds in seawater and determine, structurally, which are likely to be consumed by marine bacteria. The second bit is relatively easy, but isolating any compound from the salty, organically complex milieu that is seawater is not. Only through the application of expensive and time consuming methods can a targeted compound by isolated, and it is necessary to know in advance what the target compound is.
Second, a biologist might try to analyze the genetic composition or gene expression pattern of marine bacteria to determine what enzymes the bacteria are using, or have the capacity to use. An abundance of transporters specific to a certain compound, or class of compounds, for example, suggests that this compound is, for that bacteria, an important substrate. Unfortunately determining which enzymes are specific to what compounds is almost as difficult as the bulk analysis of carbon compounds in seawater. Most of what we know about microbial enzyme specificity comes from studies using E. coli, which may or may not have much to do with what bacteria are doing in the marine environment. To be absolutely certain about the role of any enzyme it is necessary to perform costly and tedious experiments with a laboratory isolate, a requirement that eliminates the vast, unculturable majority of marine bacteria from any potential analysis.
Durham et al. waded into this particular quagmire with both approaches. Working with a model system composed of one diatom, Thalassiosira pseudonana, and one bacterium, Roseobacter pomeroyi, they compared the gene expression profiles of bacteria grown in the presence of the diatom with profiles from pure cultures. Surprisingly, genes strongly upregulated in the presence of the diatom included transporters for the reduced organo-sulfur compound C3-sulfonate 2,3-dihyhdroxypropane-1-sulfonate (DHPS), and genes coding for hydrogenase enzymes involved in DHPS catabolism, including the gene hpsN. Taking this hint the researchers were able to grow R. pomeroyi on DHPS as the sole carbon source, observing gene expression profile similar to when R. pomeroyi was grown in the presence of the diatom. Because DHPS was not a component of the media used in the initial experiment it must have been produced by the diatom, and clearly it is an acceptable growth substrate for R. pomeroyi. But how important is it in the natural environment?
With a target compound and a target gene in hand, Durham et al. were able to quantify DHPS in seawater during a cruise in the North Pacific, while simultaneously collecting metatranscriptomes and metagenomes. They observed an abundance of hpsN transcripts coincident with diatom cell counts and high DHPS concentrations. At coastal stations the concentration of DHPS actually exceeded that of DMSP. This is a great paper, but is just a first look at a story that is sure to have geographic and taxonomic complexity. I’m sure we’ll be hearing a lot more about DHPS (and other, yet to be revealed components of the DOC pool) in the coming years.
