DMS(P): the amazing story of a pervasive indicator molecule in the marine food web

Dimethylsulfide.  Does that word mean anything to you?  “Why yes,” you organic chemistry nerds may say, “It clearly is a molecule of sulfur with two methyl groups attached.”  That’s as far as I could have gotten – until this past week, when I inundated myself with information on dimethylsulfide (DMS) due to a paper published in Science.  Now I’m enlightened – what a wonderful molecule!  Let me spoil it for you: it is simultaneously a defense mechanism, a chemical cue pervasive throughout the marine food web, and an effector on the earth’s climate.  (See illustration at bottom of post for summary.)  That’s right.  Just a sulfur molecule with two methyl groups attached.  Now let’s back up a bit.

DMS is a sulfur compound that accounts for 50-60% of the total natural reduced sulfur flux to the atmosphere (even more than either volcanoes or vegetation).  While sulfur in the atmosphere can cause acid rain, it is also very important, as it helps form clouds.  In order for water to transition from a gas to liquid in the atmosphere, it needs a small particle in the air to adhere onto, known as a cloud condensation nucleus.  Sulfur oxide, which can be derived from DMS, is one of these particles.  Clouds not only carry our precipitation, but help to reflect sunlight (and thus heat) back into space, affecting our planet’s climate.

After the realization of its importance as a cloud condensation nucleus, scientists began to look for DMS’s planetary source and found that 95% of the atmospheric DMS originates in the oceans – but from where?  As illustrated in my figure, it is actually formed in certain species of phytoplankton and released when cells leak, most often due to herbivory by other organisms.  The phytoplankton itself actually makes a molecule called DMSP (dimethylsuphoniopropionate, if you must know).  When its cell wall begins to break down, stores of DMSP (from an unknown location within the cell) and an enzyme, DMSP-lyase, are released into the surrounding water.  This DMSP-lyase removes the P-group, leaving us with our favorite molecule of the day, DMS.

In 1987, the CLAW hypothesis (named for its authors) was put forward by James Lovelock and a handful of his lackeys to support his infamous Gaia hypothesis which suggests that microorganisms regulate the Earth’s climate to maintain conditions suitable for life.  CLAW hypothesized that levels of DMSP and its P-cleaving enzyme in phytoplankton are regulated by light and temperature, with greater amounts of DMSP produced when it gets warm in order to send more DMS into the atmosphere, deflecting sunlight and reducing global temperatures.  However, like most support for the Gaia hypothesis, this idea requires that phytoplankton act altruistically, releasing the DMS for the good of the planet, which does not make much sense in light of natural selection.  (A good review of this and the above sections can be found in this paper by Rafel Simo.)

A 2001 MEPS paper by Kathryn Van Alstyne and others provides evidence that the release of DMSP and DMSP-lyase by phytoplankton is actually a chemical defense mechanism.  After DMSP-lyase activity, the resulting products are DMS and acrylase or acrylic acid.  The authors found that acrylic acid deterred grazing by two species of sea urchins on algae, and they suggest that this is due to an aversion to acidity by the urchin itself or that the acid irritates its gut microbes.  While the evidence is not directly causative, as the authors showed a reaction to acrylic acid and not to DMSP-produced acrylic acid in vivo, it does suggest (with other evidence) that the important part of this reaction to the phytoplankton is not DMS, but rather its byproduct.

Fig. 1 from Van Alstyne et al. (2001), showing the DMSP-lyase reaction

Smaller grazers, such as isopods, had no reaction to the acrylic acid in that paper.  But a paper published in Science this week (July 16 2010) by Justin Seymour, Rafel Simo, and others looks into the effects of DMSP on the smallest grazers: microbes.  Using “microfluid technology” (see details at end of post), the researchers measured the strength of attraction of 4 different types of microbes (7 species) to varying concentrations of DMSP, DMS, DMSO (dimethylsulfoxide, a DMS and DMSP degradation product), GBT (glycine betaine, a molecule analogous to DMSP in structure and function), and artificial seawater (as a control).

1. Each of the 3 species of autotrophic plankton reacted differently to DMSP in the water.  The algae Micromonas pusilla showed strong attraction to DMSP, taking it up presumably as a carbon and sulfur source.  The cyanobacterium Synechococcus sp. showed no reaction.  Most strangely, the algae Dunaliella tertiolecta moved very strongly toward DMSP, but not to assimilate it directly; rather, it cleaved the molecule into DMS extracellularly and potentially assimilated that molecule instead.  The authors do not know why this action occurs.
2. Two species of bacteria, Pseudoalteromonas haloplanktis and Silicibacter sp., each moved toward the DMSP for assimilation as part of their carbon and sulfur requirements.
3. Two consumers, one a herbivore to eat the algae itself (Oxyrrhis marina) and the other a bacteriovore which strove to eat the bacteria consuming the DMSP, each showed positive chemotaxis and moved toward the DMSP source.

This last part is the most interesting: these two microbe species use the DMSP as a chemical signal that there is food around.  Out of all the molecules that could leak from the burst cell and indicate prey, it is this very molecule, DMSP, that does the trick.

But wait: didn’t the 2001 paper I just wrote about suggest that DMSP is a chemical defense of phytoplankton?  What is it doing drawing in its own predators?  The authors suggest that previous studies have flawed experimental design, releasing far too much bulk DMSP into the environment in contrast to their own “microfluid technology.”  Previous studies, such as a 1997 Nature paper by Gordon Wolfe and a 2003 paper by Suzanne Strom, found that O. marina has a higher tolerance to digesting DMSP and is less repelled than other species.  More work should be done in order to get to the root of this contradiction.

Thus far, we have DMSP attracting bacteria to consume the DMSP itself, drawing in an herbivore to consume the DMSP-producer, and a bacteriovore attracted to the DMSP in order to find its own bacterial prey.  This is not the end of the story, as DMSP is a prey indicator at higher trophic levels as well.  A 2008 Science paper out of UC-Davis and UNC found that planktivorous fish use DMSP as a foraging cue, aggregating near DMSP hotspots.  Furthermore, Gabrielle Nevitt reviewed literature in 2008 on seabirds (Order: Procellariiformes) using DMS as an olfactory cue to identify patches of its own prey, fish and squid, feeding on the zooplankton and its phytoplankton prey.  A similar pattern has also been found in seals and whale sharks.

The evolutionary implications of this are astounding.  It seems as though many molecules released from a leaky phytoplankton cell could be used as indicators of these clusters of consumption.  However, DMSP has something special: sulfur.  We all know that smell, and perhaps it is this stinkiness that has allowed it to become such a pervasive indicator throughout the marine food web.  In her review, Nevitt discusses the evolution of DMS-sensitivity in seabirds, and using phylogenetic trees, shows that only the species that are reared in dark burrows, relying on smell alone to identify food, currently have DMS-sensitivity.  How did this apparent convergent evolution occur?  Is it convergent?  (I have no answers to these questions.)

Are there any implications for climate in these findings, as DMSP is indirectly responsible for increased albedo (sunlight reflection) in our atmosphere?  I doubt that there are any direct consequences that we can enumerate.  As all biogeochemists know, the stuff of the air frequently comes from the stuff we live on and in: soil and water.  This is simply another tie to the way microbes and abiotic stuffs relate to climate-regulating molecules.  The authors of this week’s Science paper note that “microbial behaviors, played out over microscale chemical landscapes, shape planktonic food webs while potentially influencing climate at global scales.”  DMS as a prey cue should create a positive feedback loop, drawing more herbivores to open more cells and leak increasing DMSP, which in turn draws more herbivores.  Some studies show varying ties of DMSP production to species, light, temperature and salinity (review by Stefels et al. here), but it seems to me that the DMS-as-prey-cue and DMS-as-climate-regulator processes are unlinked, so would not work together in any predictable way.

If you take nothing away, take this: sometimes the universe is more connected than we can imagine.

(Sidenote: should I give up strict science and become a science illustrator?)

NOTES ON MICROFLUID TECHNOLOGY:
The idea behind this technique is that microbes inhabit a “dynamic and patchy nutrient landscape” in which nutrient levels vary over micrometer scales.  The microfluidic device is a chamber designed with the “objective of creating a diffusing band of chemoattractant, to simulate an ephemeral, microscale nutrient patch.”  There is a chamber in the center into which fluorescence-labeled chemoattractant is added to the desired concentration, and then input is cut off.  Thus the chemical will dissipate slowly through the closed chamber, trying to imitate the open ocean.  The researchers then add their microorganisms, and measure their distribution and the distribution of the fluorescent chemical.  This allows the researchers to track the intensity and location of the chemical, as well as the behavior of single organisms.

This information is from a paper in Limnology and Oceanography: Methods by J.R. Seymour, T. Ahmed, and R. Stocker entitled “A microfluidic chemotaxis assay to study microbial behavior in diffusing nutrient patches” (2008: 6 (477-488)).  A pdf copy of this paper is available on Roman Stocker’s webpage, here (pdf warning!).

Here’s a picture of the device, thanks to Roman Stocker.  The blue tube is the microbe input, the green tube is chemical input, and the red tube is for drawing out waste.  It sits on top of a microscope.

DeBose, J., Lema, S., & Nevitt, G. (2008). Dimethylsulfoniopropionate as a Foraging Cue for Reef Fishes Science, 319 (5868), 1356-1356 DOI: 10.1126/science.1151109

Nevitt, G. (2008). Sensory ecology on the high seas: the odor world of the procellariiform seabirds Journal of Experimental Biology, 211 (11), 1706-1713 DOI: 10.1242/jeb.015412

Seymour, J., Simo, R., Ahmed, T., & Stocker, R. (2010). Chemoattraction to Dimethylsulfoniopropionate Throughout the Marine Microbial Food Web Science, 329 (5989), 342-345 DOI: 10.1126/science.1188418

Simó, R. (2001). Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links Trends in Ecology & Evolution, 16 (6), 287-294 DOI: 10.1016/S0169-5347(01)02152-8

Stefels, J., Steinke, M., Turner, S., Malin, G., & Belviso, S. (2007). Environmental constraints on the production and removal of the climatically active gas dimethylsulphide (DMS) and implications for ecosystem modelling Biogeochemistry, 83 (1-3), 245-275 DOI: 10.1007/s10533-007-9091-5

Van Alstyne, K., Wolfe, G., Freidenburg, T., Neill, A., & Hicken, C. (2001). Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage Marine Ecology Progress Series, 213, 53-65 DOI: 10.3354/meps213053

G. V. Wolfe, M. Steinke, & G. O. Kirst (1997). Grazing-activated chemical defence in a unicellular marine alga Nature, 387, 894-897