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

The views expressed are those of the author and are not necessarily those of Scientific American.


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In honor of Chemistry Day here on the Scientific American blog network, I’ve dug out partially rewritten a post on ecological chemistry from the Culturing Science archives. Enjoy!

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 (July 19, 2010), when I inundated myself with information on dimethylsulfide (DMS), inspired by a paper published in Science.  Now I’m enlightened – what a wonderful molecule!  Let me spoil it for you: it is a chemical cue pervasive throughout the marine food web that also affects 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 around 60% of the total natural reduced sulfur flux to the atmosphere (even more than either volcanoes or vegetation). (Data last updated January 2011.) We tend to think of atmospheric sulfur as detrimental because it can cause acid rain. But it is also plays an important role, as it helps form clouds. In order for water to transition from gas to a liquid cloud in the atmosphere, it needs to cling onto another particle: a cloud condensation nucleus. Sulfur oxide, which can be derived from DMS, is one of these particles. Clouds not only carry precipitation, but help to reflect sunlight and heat back into space, cooling our planet.

Illustration by me, under creative commons for use with attribution. (I know, you all want to frame this drawing and get it tattooed onto your calves, I understand. JUST CREDIT ME.)

Once scientists realized its importance as a cloud condensation nucleus, they began to search for DMS’s planetary source. They found that 95% of the atmospheric DMS originates in the oceans – but from where?  As illustrated in my drawing over there on the right, it is formed in certain species of phytoplankton. Phytoplankton convert their cellular stores of sulfur into a molecule called DMSP.  When the cell wall breaks down, often by consumption by herbivores, the phytoplankton releases DMSP and an enzyme, DMSP-lyase, into the surrounding water.  This DMSP-lyase removes the phosphate group, leaving us with our favorite molecule of the day, DMS.

Notorious biochemist James Lovelock and a handful of his lackeys integrated DMS into large-scale atmospheric theory in 1987 in the CLAW hypothesis (named for its authors) to support his Gaia hypothesis. The Gaia hypothesis suggests that microorganisms regulate the Earth’s climate to maintain conditions suitable for life.  CLAW hypothesized that a too-warm climate causes phytoplankton to produce greater amounts of DMSP in order to release DMS into the atmosphere, deflecting sunlight and causing global cooling. However, like most support for the Gaia hypothesis, CLAW requires that phytoplankton act altruistically, upregulating DMS for the good of the planet — a concept that 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.)

Instead of considering why phytoplankton release DMSP, 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.  The researchers used a microfluid device to control the diffusion of DMSP in seawater and tried to imitate its motion in the open ocean to the best of their ability. They measured the strength of attraction of 4 different types of microbes (7 species) to varying concentrations of DMSP.

The tested organisms interacted with the molecule in different ways. One algal species and two bacteria absorbed it, presumably for its carbon and sulfur. One algae did not react, and the other cleaved the DMSP into DMS and assimilated that. The final two plankton species moved towards the DMSP, not because they wanted to consume the molecule, but because they wanted to feed upon those that drew near. One herbivorous plankter Oxyrrhis marina gobbled up the baited algae, and a predatory plankter ate the bacteria consuming the DMSP.

This last part is the most interesting: the DMSP is a chemical signal that drew these last two species to their planktonic food.  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.

The story does not end here, as DMSP works as a prey indicator at higher trophic levels as well.  A 2008 Science paper out of UC-Davis and UNC found that planktivorous fish aggregate near DMSP hotspots. Furthermore, in 2008 Gabrielle Nevitt reviewed the literature on how seabirds (Order: Procellariiformes) track fish and squid by smelling out DMSP — which the prey themselves honed in on to locate their own prey, in turn. A similar pattern has also been observed in seals and whale sharks.

Don't you love my handdrawn illustrations? under creative commons for use with attribution

All of these diverse species evolved the ability to sense DMSP, of all molecules, to draw them towards food.  Why DMSP? It has something special to offer that other molecules don’t: 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. Using evolutionary trees, she points out that only those species which rely on smell alone to identify food in dark burrows have DMS-sensitivity as adults.

It’s tempting to jump even further and consider how these predator-prey relationships affect DMS-influenced climate.  I doubt that we can enumerate any direct consequences. The authors of the Science paper note that “microbial behaviors, played out over microscale chemical landscapes, shape planktonic food webs while potentially influencing climate at global scales.”  DMS could generate a positive feedback loop: its initial release draws herbivores to open more cells and leak increasing DMSP, which in turn draws more herbivores, ad infinitum.

Some studies suggest that climatic variables such as light, temperature, and salinity determine what species thrive and thus how much DMSP is produced (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. 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 example of how microbes and abiotic stuffs tie to climate-regulating molecules.

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

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 modellingBiogeochemistry, 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 algaNature, 387, 894-897

 

Hannah Waters About the Author: Hannah Waters writes about natural history and the way people think about nature. She lives and works in Philadelphia, PA, but really on the internet. Follow on Twitter @hannahjwaters.

The views expressed are those of the author and are not necessarily those of Scientific American.





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  1. 1. dunkleosteus 10:09 am 08/2/2011

    Those diagrams are amazing.

    Link to this
  2. 2. hanjeanwat 1:42 pm 08/2/2011

    Thanks! I need to pick my art supplies back up again and do more illustrations :)

    Link to this

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