Vasily Vavilin, Lyudmila Lokshina, Sergey Rytov; Using kinetic isotope effect to evaluate the significance of the sequential and parallel steps: formation of microbial consortium during reversible anaerobic methane oxidation coupled with sulfate reduction. Water Sci Technol 1 June 2019; 79 (11): 2056–2067. doi: https://doi.org/10.2166/wst.2019.201
Methane is considered as an important greenhouse gas and its emission from marine sediments is controlled by anaerobic methane oxidation (AOM) coupled with sulphate reduction (SR). During AOM, methane is oxidized with sulfate as the terminal electron acceptor. This process is mediated by a syntrophic consortium of anaerobic archaea (ANME) and Desulfosarcina-like bacteria (DSS), which often form small aggregates or voluminous mats. Isotope signatures of sulfur compounds are important tools for studying sulfur cycling in the environment. So, it is necessary to interpret the isotope effects of the processes involved. Holler and coauthors noticed that so far there was no satisfying explanation for the variation of the isotopic fractionation factors between the cultures of different origin. By studying sulfur isotope effects caused by AOM-SR under continuous incubation at various methane influent concentrations, Deusner and coauthors showed that the smallest sulfur and oxygen isotope fractionation was observed for the highest influent methane concentration with the highest AOM-SR rate. This phenomenon apparently contradicts the general conclusion that the rates of concentration changes of heavier substrates, products and biomasses usually are proportional to the rates of concentration changes of the total (light + heavier) substrates, products and biomasses, respectively.
In the presented paper an attempt was made to resolve these problems by the using of mathematical modeling, the powerful research instrument. The dynamics of anaerobic oxidation of methane coupled with sulfate reduction was described. It turned out that formation of consortia of anaerobic archaea and Desulfosarcina-like bacteria may have a significant effect on sulfur isotope fractionation. A good fit of the dynamic model to experimental data was obtained only when assuming active biomass accumulation. It was shown that during anaerobic oxidation the fractionation of sulfur isotopes is universally proportional to the rate of formation of microbial consortia which coincides with an increase of the total reaction rate. The presented model explains the lower sulfur isotope fractionation factors at a higher rate of anaerobic oxidation of methane by the shorter average distance between microbial consortia and the respective sulfur substrates. Despite the offered dynamic model being rather complex, it substantially reduces the overall complexity of reactions involved in AOM and SR, highlighting the most critical steps. Introducing of isotope’s concentrations enables evaluating microorganisms’ activity. It is very useful instrument allowing adding new knowledge to experimental methods which determine the presence of the microorganisms in the environment but not their activity. This method has already been applied successfully for clarifying microorganisms’ activity in various environments such as marches, lakes and anaerobic digesters.
The authors hope that this article will help to understand the processes of anaerobic methane oxidation coupled with sulfate reduction in marine sediments more deeply and demonstrate the power of modeling in understanding of incomprehensible processes.
Further reading
Deusner C., Holler T., Arnold G.L., Bernasconi S.M., Formolo M.J. & Brunner B., 2014. Sulfur and oxygen isotope fractionation during sulfate reduction coupled to anaerobic oxidation of methane is dependent on methane concentration. Earth Planet. Sci. Letter 399, 61-73.
Holler T., Wegener G., Knittel K., BoetiusA., Brunner B., Kuypers M.M.M. & WiddelF. 2009. Substantial and fractionation during anaerobic oxidation of methane by marine consortia enriched in vitro. Env. Microbiol. Reports, 1(5), 370-376.
Milucka J., Ferdelman T.G., Polerecky L., Franzke D., Wegener G., Schmid M., Lieberwirth I., Wagner M., Widdel F. & Kuypers M.M.M. 2012. Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature, 491, 541-546.
Vavilin V.A. 2013. Estimating changes of isotopic fractionation based on chemical reactions and microbial dynamics during anaerobic methane oxidation: apparent zero- and first-order kinetics at high and low initial methane concentrations. Ant. Leeuwenhoek, 103, 375-383.
Vavilin V.A., Rytov S.V. & Conrad, R. 2017. Modelling methane formation in sediments of tropical lakes focusing on syntrophic acetate oxidation: Dynamic and static carbon isotope equations. Ecol. Modell., 363,:81–95.
Vavilin V.A., Rytov S.V. & Lokshina L.Y. 2018a. Modelling the specific pathway of CH4 and CO2 formation using carbon isotope fractionation: an example for a boreal mesotrophic fen. Isot. Environ. Health S., 54, 475-493.
Vavilin V.A., Rytov S.V. & Lokshina L.Y. 2018b. Dynamic isotope equations for 13CH4 and 13CO2 describing methane formation with a focus on the effect of anaerobic respiration in sediments of some tropical lakes. Ecol. Modell., 386, 59-70.