Microbiologists and geochemists have shown that marine methane oxidation coupled to sulfate respiration can be performed by a single microorganism, a member of the ancient kingdom of the Archaea, and doesn't need to be carried out in collaboration with a bacterium, as previously thought.

Vast amounts of methane are stored under the ocean floor. Anaerobic oxidation of methane coupled to sulfate respiration (AOM) prevents the release of this potent greenhouse gas into the atmosphere. Although the process was discovered 35 years ago it has remained a mystery how microorganisms perform this reaction. A decade ago, it was discovered that two different microorganisms are often associated with AOM. It was proposed that these two microorganisms perform different parts of the AOM reaction. One, an archaeon, was supposed to oxidize methane and the other, a bacterium, was supposed to respire sulfate. This implied the existence of an intermediate compound to be shuttled from the methane oxidizer to the sulfate respirer.

Now, a team has shown that the archaeon not only oxidizes methane but can also respire sulfate and does not necessarily need the bacterial partner. It appears that the archaeon does not employ the common enzyme toolbox that other known sulfate-respiring microorganisms use, but relies on a different, unknown pathway.



In this model, methane oxidation and sulfate respiration to elemental sulfur (or all the way to sulfide) is performed by the methanotrophic archaea (ANME). The associated bacteria (DSS) are disproportionators (sulfur fermentors), which take up produced elemental sulfur in the form of disulfide and turn it into sulfate and sulfide. Dark circles represent iron- and phosphorus-rich precipitates found in the bacteria. Credit: Jana Milucka, MPI f. Marine Microbiology

The basis for this shift in thinking is the observation that elemental sulfur is formed and accumulates in the methane-oxidizing archaeon. “Using chromatographic and state-of-the-art spectroscopic techniques we found surprisingly high concentrations of elemental sulfur in our cultures,” says Professor Marcel Kuypers from  the Max Planck Institute for Marine Microbiolog, “The single-cell techniques showed that the sulfur content in the methane-degrading archaeon was much higher than in the bacterium. Our experiments show that this sulfur is formed during sulfate respiration.”

What does the bacterium do if the archaeon does both sulfate respiration and methane oxidation? “The bacteria actually make a living off of the elemental sulfur produced by the archaea,” explains Jana Milucka, first author of the study. “The bacteria grow by splitting the elemental sulfur into sulfate and hydrogen sulfide. This is a form of fermentation, like the process that produces alcohol.”


The enrichment of the microorganisms responsible for marine AOM, archaea in red and bacteria in green from the Isis Mud Volcano in the Mediterranean Sea has taken 8 years of continuous incubation. Without these cultures it would not have been possible to trace down the complex sulfur cycling involved in AOM. Credit: Jana Milucka, MPI for Marine Microbiology

“Until now we have always had trouble explaining the occurrence of elemental sulfur in oxygen-free sediments,”, notes co-author Tim Ferdelman, scientist at the MPI Bremen. ”Our discoveries not only provide a mechanism for marine methane oxidation but also cast a new light on the carbon and sulfur cycling in marine, methane-rich sediments.”

Citation: Jana Milucka, Timothy G. Ferdelman, Lubos Polerecky, Daniela Franzke, Gunter Wegener, Markus Schmid, Ingo Lieberwirth, Michael Wagner, Friedrich Widdel, Marcel M. M. Kuypers, 'Zerovalent sulfur is a key intermediate in marine methane oxidation', Nature, 2012. 8 November, 2012. Doi: 10.1038/nature11656