Ecophysiology of Methanococcus maripaludis and Desulfovibrio vulgaris : the role of structure in relation to function

Abstract

Sulfate-reducing bacteria (SRB) and methanogenic archaea are known to interact in anaerobic environments under a range of conditions, and the nature of the interaction is dependent on the concentration of available carbon and energy sources, electron acceptors and the metabolic potential of the specific genera present. In the absence of sulfate, SRB can participate in a mutualism by product inhibition with hydrogenotrophic methanogens. SRB reduce protons to form hydrogen gas as a methanogenic substrate, and methanogens prevent inhibition of hydrogenase activity in the SRB by consuming the evolved hydrogen, making the interaction beneficial to both parties. This type of interaction can occur in nature when organisms are free-swimming or attached to a surface as biofilm. The impact of structured biofilm on ecosystem function at various scales is becoming increasingly clear, as this growth mode concentrates biomass which can increase the capacity for compound immobilization, affect hydrodynamic flow paths, and leave cells in altered physiological states. In spite of this, few studies have systematically characterized mutualistic interactions within the biofilm state using model organisms. Syntrophic continuous culture of Desulfovibrio vulgaris Hildenborough and Methanococcus maripaludis was monitored from inoculation through steady state for biofilm and planktonic community structure and function in terms of biomass production, lactate oxidation, and methane production. This biofilm was structurally distinct from monoculture biofilms grown under the same conditions and yield of biomass per lactate mass flux or methane produced was much higher when biofilm was present under lactate limitation. The results suggested that biofilm helped optimize carrying capacity of the syntrophic culture. Observations in coculture biofilm of attraction by M. maripaludis to a surface in the presence of a hydrogen-producing biofilm indicated a tactic response in the archaeum. Movement toward favorable conditions, or chemotaxis is a strategy employed across all three domains of life, yet chemotaxis in archaea is still poorly described, and no previous work has demonstrated taxis toward a hydrogen source, like a syntrophic partner, in spite of its role in electron flow in anaerobic communities. Here we present the first direct observation of taxis toward hydrogen, or "hydrogenotaxis" in the archaeum M. maripaludis.