An investigation of anaerobic methane oxidation by consortia of methanotrophic archaea and bacterial partners using nanoSIMS and process-based modeling

Yimeng Shi1, Chris Kempes2,3, Grayson Chadwick4, Shawn McGlynn4,5, Xiaojia He1, Victoria J Orphan4 and Christof D Meile6, (1)The University of Georgia, Department of Marine Sciences, Athens, GA, United States, (2)Santa Fe Institute, Santa Fe, CA, United States, (3)California Institute of Technology, Control and Dynamical Systems, Pasadena, CA, United States, (4)California Institute of Technology, Division of Geological and Planetary Sciences, Pasadena, CA, United States, (5)Tokyo Metropolitan University, Department of Biological Sciences, Tokyo, Japan, (6)University of Georgia, Department of Marine Sciences, Athens, GA, United States
Abstract:
The anaerobic oxidation of methane in marine sediments plays an important role in the global methane cycle. Mediated by a microbial consortium consisting of archaea and bacteria, it is estimated that almost 80% of all the methane that arises from marine sediments is oxidized anaerobically by this process (Reeburgh 2007, Chemical Reviews 107, 486–513).

We used reactive transport modeling to compare and contrast potential mechanisms of methane oxidation. This included acetate, hydrogen, formate, and disulfide acting as intermediates that are exchanged between archaea and bacteria. Moreover, we investigated electron transport through nanowires, facilitating the electron exchange between the microbial partners. It was shown that reaction kinetics, transport intensities, and energetic considerations all could decisively impact the overall rate of methane consumption.

Informed by observed microbial cell distribution, we applied the model to a range of spatial distribution patterns of archaea and bacteria. We found that a consortium with evenly distributed archaeal and bacterial cells has the potential to more efficiently oxidize methane, because the vicinity of bacteria and archaea counteracts the build up of products and therefore prevents the thermodynamic shutdown of microbial metabolism.

Single cell stable isotope enrichment in archaeal-bacterial consortia observed by nanoSIMS revealed rather uniform levels of anabolic activity within consortia with different spatial distribution patterns. Comparison to model simulation illustrates that efficient exchange is necessary to reproduce such observations and prevent conditions that are energetically unfavorable for methane oxidation to take place. Model simulations indicate that a recently described mechanism of direct interspecies electron transport between the methanotrophic archaea and its bacterial partner through a conductive matrix (McGlynn et al. 2015, Nature, 10.1038/nature15512) is consistent with observations.

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