Project: Unsilent partners: Constraining the contribution of methanogen-protist symbioses to total methane production in anoxic marine habitats

NSF abstract:

Overview: There is a growing appreciation for the ubiquity of microbial symbioses on earth, yet in most habitats we have only a basic understanding of their physiology and ecology. Many eukaryotes have evolved specific associations with prokaryotes that capitalize on the relative diversity of prokaryotic metabolisms. In terms of numbers, symbiont populations often rival or exceed free-living prokaryotes in their environment, therefore, through their metabolism, symbionts may have a significant effect on their biotic and abiotic environment. Despite this, there is limited knowledge of the symbiotic function and metabolic activity of most symbiotic taxa.

Symbioses between anaerobic protists and intracellular, methanogenic archaea have been found in many anoxic habitats, however the contribution of symbiont-produced methane (CH4) to the marine CH4 cycle is yet unconstrained. In non-marine environments, like rice paddies and lakes, they have been found to significantly contribute to the production of CH4, suggesting that these symbioses may be important to the biogeochemical cycling of this climate-active gas. However, though taxa known to host methanogens have been detected in general surveys of protists in oxygen (O2) -poor and anoxic marine water columns, to date, they have never been specifically surveyed, and no studies have quantified their contribution to CH4 production in these habitats. Additionally, outside of their methanogenic function, nothing is known about the physiological capacity of their symbionts.

To develop an understanding of the details of these partnerships and to address the contribution of microbial symbionts to the CH4 cycle, the fellow will examine the ecology and physiology of methanogen-protist symbioses in Saanich Inlet (SI), a seasonally anoxic fjord off the coast of British Columbia, Canada that accumulates CH4 (greater than 1 micrometer) in its deep water from a yet unconstrained source. With sponsor Dr. Virginia Edgcomb at Woods Hole Oceanographic Institution (WHOI), the fellow will combine a) fluorescence-activated cell sorting based surveys of the abundance and diversity of methanogen-hosting protists, with assessment of their metabolism through b) the experimental measurement of CH4 production by natural populations and c) analysis of total symbiont gene content (i.e., genomics). This robust combination of observational and experimental approaches will provide valuable insight into distribution, physiology and activity of these symbioses, allowing the first estimation of the contribution of protist-associated methanogens to CH4 production in an anoxic marine water column.

Intellectual merit: Anoxic and low-O2 marine water columns are thought to contribute 50-60% of the global oceanic emission of CH4, a climate-active gas. It is typically assumed that the CH4 in these habitats originates from the underlying sediment, where methanogenesis is known to occur. Water column production is presumed to be unimportant in these areas, as free-living methanogens cannot compete successfully with sulfate-reducing bacteria for common substrates (e.g, Hydrogen) in sulfate-replete seawater. However, symbiotic methanogens are protected from competition with sulfate-reducing bacteria since substrates are host provided. Consequently, methanogenesis by the symbionts of protists in the water column may account for a significant fraction of the CH4 budget in these areas. Thus, the proposed effort will substantially advance our understanding of the underlying source of CH4 in O2-deficient and anoxic marine habitats. Since rising temperatures are predicted to cause the expansion of oxygen-depleted habitats, better insight into CH4 cycling in these areas will become increasingly important to our understanding and modeling of global oceanic CH4 emissions.

Broader Impacts: The broader impacts of the proposed effort include disseminating the findings to the scientific and wider community through public lectures, and supporting participation of underrepresented groups in ocean sciences research through mentorship of 1-2 undergraduates in the WHOI Summer Student and Minority Fellowship programs. Additionally, funds from the annual fellowship allowance have been budgeted to develop an educational unit about marine symbioses with a local non-profit marine education foundation. This unit will be presented by the fellow to K-12 students from disadvantaged communities from the southern New England area.