Formate as an Energy Source for Microbial Metabolism in Chemosynthetic Zones of Hydrothermal Ecosystems

Abstract

Formate, a simple organic acid known to support chemotrophic hyperthermophiles, is found in hot springs of varying temperature and pH. However, it is not yet known how metabolic strategies that use formate could contribute to primary productivity in hydrothermal ecosystems. In an effort to provide a quantitative framework for assessing the role of formate metabolism, concentration data for dissolved formate and many other solutes in samples from Yellowstone hot springs were used, together with data for coexisting gas compositions, to evaluate the overall Gibbs energy for many reactions involving formate oxidation or reduction. The result is the first rigorous thermodynamic assessment of reactions involving formate oxidation to bicarbonate and reduction to methane coupled with various forms of iron, nitrogen, sulfur, hydrogen, and oxygen for hydrothermal ecosystems. We conclude that there are a limited number of reactions that can yield energy through formate reduction, in contrast to numerous formate oxidation reactions that can yield abundant energy for chemosynthetic microorganisms. Because the energy yields are so high, these results challenge the notion that hydrogen is the primary energy source of chemosynthetic microbes in hydrothermal ecosystems.

Organic, Gas, and Element Geochemistry of Hydrothermal Fluids of the Newly Discovered Extensive Hydrothermal Area in the Wallis and Futuna Region (SW Pacific)

“…It is well established that VFAs constitute a significant food source for some microorganisms and thus help sustaining hydrothermal ecosystems [97][98][99][100]. Besides, some bacteria have proven to be capable of using naphthalene [101] and tubeworms, hydrocarbons [102].…”

Carbon Source Preference in Chemosynthetic Hot Spring Communities

“…The low concentrations of 14 C-labeled formate and acetate radiotracers used in our microcosm assays were chosen to closely match previously reported concentrations of formate (acetate concentrations have yet to be reported) in YNP hot springs (Ͻ10 M) (18) and thus minimize the rate of induction of microbial processes above their basal or in situ rate. Moreover, formate occurs increasingly in the protonated form as pH decreases (it has a pK a of 3.75 at 80°C, meaning that half of all formate is protonated at pH 3.75).…”

“…The presence of organic acids at concentrations capable of supporting the growth of organisms has been reported in many marine and continental hydrothermal environments (e.g., see references 16 and 17), including those in Yellowstone National Park (YNP), Wyoming, where formate was measured at concentrations of up to 10 M in 56 hot springs (18). The low concentrations of formate in some YNP hot springs (18) may reflect the preferential utilization of this substrate by endogenous populations or a low rate of influx of this substrate into the system.…”

“…The low concentrations of formate in some YNP hot springs (18) may reflect the preferential utilization of this substrate by endogenous populations or a low rate of influx of this substrate into the system. In support of the former possibility, numerous thermophilic organisms capable of growth on formate have been isolated from hot springs (e.g., see references 14 and 19).…”

“…The energy yield associated with aerobic organic acid oxidation, in particular, formate oxidation, is predicted to be equal to or greater than that derived from the aerobic oxidation of other available reductants (e.g., H 2 , H 2 S, Fe 2ϩ , S 8 ) under the geochemical conditions that prevail in most hydrothermal systems (18). This indicates that formate may be preferentially metabolized by facultatively autotrophic populations, such as Thermocrinis or Hydrogenobacter spp., when it is available.…”