Team Play: Determining Syntrophic Interactions in Hydrocarbon Biodegradation Processes

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Microorganisms in the natural world exist as mixed communities whose collective metabolism substantially contributes to biogeochemical and/or nutrient cycling phenomena that can have profound impacts on global health including our climate, water, and land resources. In anoxic environments, mixed microbial communities comprised of Bacteria and Archaea are able to biotransform organic matter to methane through a metabolic process known as syntrophy. Syntrophy is defined as a thermodynamically interdependent (mutualistic) metabolism wherein different species within mixed anaerobic communities must cooperate to carry out a given metabolic reaction that cannot be catabolized by each organism alone. Such team play' metabolism operates near the thermodynamic equilibrium, yet contributes substantially to the natural cycling of organic matter to CH4 and CO2 in anoxic ecosystems such as wetlands, animal guts, landfills, rice paddies, and wastewater treatment systems, and is a prevalent process in anoxic hydrocarbon-associated ecosystems such as natural oil and gas seeps, deep subsurface energy reservoirs, and shallow hydrocarbon-contaminated groundwater systems. However, the ecological principles underlying the syntrophic metabolism of most organic compounds, including hydrocarbons, remain to be fully explored. The over-arching, long-term objective of my research program is to determine the interactions that govern syntrophic communities associated with methanogenic hydrocarbon biodegradation processes. The two major short-term objectives for the proposed work that will address gaps in knowledge in this field of study are to (1) identify the interactions and potential roles of poorly understood syntrophic members in mixed consortia, including those of uncultivated taxa (such as Atribacteria') and other community members that have been identified in our hydrocarbon-metabolizing methanogenic cultures and in other environments, and (2) to experimentally assess mechanisms used by methanogenic hydrocarbon-degrading community members (such as via indirect or direct interspecies electron transfer, mediators, or nutrient interdependencies) to form mutually beneficial partnerships with each other. The proposed research program will offer insights into how microbial community members collectively interact to biotransform organic matter thus contributing to a broader understanding of biogeochemical cycling. The focus on hydrocarbon-degrading systems undergoing such team play' will help to improve our understanding of how best to apply biological solutions to remediate hydrocarbon-contaminated environments in Canada and elsewhere.