Marine Chemosynthetic Symbioses

Bacteria and marine eukaryotes often coexist in symbioses that significantly influence the ecology, physiology and evolution of both partners. De Bary (1879) defined symbiosis as “the living together of differently named organisms,” implying that the term encompasses both positive (e.g., mutualism) and negative (e.g., parasitism) associations. Many researchers now view symbiotic interactions as those that persist over the majority of the lifespan of the organisms involved and that provide benefits to each partner beyond those obtained in the absence of association. This chapter describes such symbioses, specifically those between marine invertebrate and protist hosts and chemosynthetic bacterial symbionts. These bacteria, which cluster primarily within the Gammaproteobacteria (Fig. 1), are chemoautotrophs or methanotrophs. In both chemoautotrophic and methanotrophic symbioses, the hosts, through an astonishing array of physiological and behavioral adaptations, provide the symbiont access to the substrates (i.e., electron donors and acceptors) necessary for the generation of energy and bacterial biomass. In exchange, a portion of the carbon fixed by the symbiont is used, either directly or indirectly, for host energy and biosynthesis. These symbioses thereby increase the metabolic capabilities, and therefore the number of ecological niches, of both the host and the bacterial symbiont. In those symbioses for which the electron donor has been explicitly identified, sulfide and other inorganic reduced sulfur compounds (e.g., thiosulfate) fuel energy generation by the chemoautotrophic symbionts, serving as electron sources for oxidative phosphorylation. In these symbioses, the ATP produced in electron transport fuels autotrophic CO 2 fixation via the Calvin cycle. In contrast, bacteria in marine invertebrate-methanotroph symbioses use methane (CH 4 ) as an energy, electron, and carbon source. Unlike their protist or metazoan hosts, chemoautotrophs and methanotrophs share the ability to use reduced inorganic compounds or methane for energy generation and carbon dioxide or methane for carbon fixation and utilization. On the basis of these unique biosynthetic capacities, notably the ability to synthesize C 3 compounds from C 1 compounds, we refer collectively to these bacterial symbionts as “chemosynthetic.” Given the sulfide-rich habitats in which chemoautotrophic symbioses occur, researchers infer that the bacterial symbionts oxidize reduced inorganic sulfur compounds to obtain energy and reducing power for autotrophic carbon fixation. While some endosymbionts (such as those in the protobranchs Solemya velum and S. reidi ; Cavanaugh, 1983; Anderson et al., 1987) utilize thiosulfate (S 2 O 3 μ ), an intermediate in sulfide oxidation, hydrogen sulfide is inferred to be the preferred energy source in a variety of symbioses (see review in Van Dover, 2000). But for many symbioses the actual energy source has not been identified definitively; rather, only an autotrophic metabolism has been confirmed. Indeed, chemosynthetic bacteria utilizing other energy sources (e.g., hydrogen or ammonia) could also serve similar nutritional roles in symbiotic associations. In this review, bacterial symbionts that have been shown to use reduced sulfur compounds (H 2 S, HS μ , S μ 2 , S 2 O 3 μ , S o ) for energy metabolism are referred to as thioautotrophs, while the more general term “chemoautotroph” is used to describe symbionts for which data supporting autotrophic CO 2 fixation exist but for which the lithotrophic energy source is unknown.