Hydrogen or formate: Alternative key players in methanogenic degradation

Abstract

Hydrogen and formate are important electron carriers in methanogenic degradation in anoxic environments such as sediments, sewage sludge digestors and biogas reactors. Especially in the terminal steps of methanogenesis, they determine the energy budgets of secondary (syntrophically) fermenting bacteria and their methanogenic partners. The literature provides considerable data on hydrogen pool sizes in such habitats, but little data exist for formate concentrations due to technical difficulties in formate determination at low concentration. Recent evidence from biochemical and molecular biological studies indicates that several secondary fermenters can use both hydrogen and formate for electron release, and may do so even simultaneously. Numerous strictly anaerobic bacteria contain enzymes which equilibrate hydrogen and formate pools to energetically equal values, and recent measurements in sewage digestors and biogas reactors indicate that - beyond occasional fluctuations - the pool sizes of hydrogen and formate are indeed energetically nearly equivalent. Nonetheless, a thermophilic archaeon from a submarine hydrothermal vent, Thermococcus onnurineus, can obtain ATP from the conversion of formate to hydrogen plus bicarbonate at 80°C, indicating that at least in this extreme environment the pools of formate and hydrogen are likely to be sufficiently different to support such an unusual type of energy conservation.

Formate and Hydrogen as Electron Shuttles in Terminal Fermentations in an Oligotrophic Freshwater Lake Sediment

“…In secondary fermentations, fatty acids and alcohols that are released as products of primary fermentations are converted to compounds that can be used by methanogens, i.e., C 1 compounds, hydrogen, and acetate. The electrons released in these fermentations are transferred to methanogenic partners either as hydrogen gas or as formate at low concentrations to render these fermentations energetically feasible (2,4,(10)(11)(12)(13). For many years, hydrogen was considered the more important electron carrier, mostly because hydrogen partial pressures could easily be measured in the headspace of culture bottles or digesters.…”

“…For many years, hydrogen was considered the more important electron carrier, mostly because hydrogen partial pressures could easily be measured in the headspace of culture bottles or digesters. Nonetheless, formate was already discussed as an alternative electron shuttle with the descriptions of the very first defined syntrophic cocultures (4,10,(12)(13)(14). Later work has shown that several secondary ("syntrophically") fermenting bacteria may release formate rather than hydrogen as an electron sink (15)(16)(17)(18)(19)(20)(21)(22), and most hydrogen-oxidizing methanogenic partners can use both hydrogen and formate as an electron source.…”

“…Perhaps especially in propionate oxidation, both electron transfer channels are used simultaneously; i.e., some of the electrons are released via hydrogen and others via formate, and both balance out to a situation that attributes just sufficient energy to the propionate oxidizer. The choice of electron carrier might as well depend on the availability of suitable partner methanogens available in the immediate surroundings (13). Although earlier radiolabeling experiments have shown that the majority of methanogenic propionate degradation in lake sediments proceeds through syntrophic oxidation via succinate (58), one may consider also the alternative fermentation path via transformation of two propionates to three acetates that Smithella propionica catalyzes (36,59,60).…”

Energy conservation mechanisms and electron transfer in syntrophic propionate-oxidizing microbial consortia

“…However, the interspecies exchange of hydrogen and formate has been the most widely studied. Hydrogen and formate are formed by secondary fermenting bacteria to release the excess of electrons during the oxidative degradation of organic acids (Schink, 1997;McInerney et al, 2009;Stams and Plugge, 2009;Schink et al, 2017).…”

“…Since Bryant and co-workers discovered that their cultures of Methanobacillus omelianskii did not contain one species but a syntrophic coculture of two types of microorganisms, hydrogen and formate were recognized from the very beginning as key metabolites in the electron transfer processes between the ethanol oxidizing bacterium and the methanogenic partner (Bryant et al, 1967). Since then, many syntrophic associations have been described and the debate over which compound is the main interspecies electron carrier between the diverse syntrophic associations continues (McInerney et al, 2009;Sieber et al, 2012;Morris et al, 2013;Schink et al, 2017).…”