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

Abstract

The energetic situation of terminal fermentations in methanogenesis was analyzed by pool size determinations in sediment cores taken in the oligotrophic Lake Constance, Germany. Distribution profiles of fermentation intermediates and products were measured at three different water depths (2, 10, and 80 m). Methane concentrations were constant below 10 cm of sediment depth. Within the methanogenic zone, concentrations of formate, acetate, propionate, and butyrate varied between 1 and 40 μM, and hydrogen was between 0.5 and 5 Pa. From the distribution profiles of the fermentation intermediates, Gibbs free energy changes for their interconversion were calculated. Pool sizes of formate and hydrogen were energetically nearly equivalent, with -5 ± 5 kJ per mol difference of free energy change (ΔG) for a hypothetical conversion of formate to hydrogen plus CO The ΔG values for conversion of fatty acids to methanogenic substrates and their further conversion to methane and CO were calculated with hydrogen and with formate as intermediates. Syntrophic propionate oxidation reached energetic equilibrium with formate as the sole electron carrier but was sufficiently exergonic if at least some of the electrons were transferred via hydrogen. The energetic consequences of formate versus hydrogen transfer in secondary and methanogenic fermentations indicate that both carrier systems are probably used simultaneously to optimize the energy yields for the partners involved. In the terminal steps of methane formation in freshwater lake sediments, fermenting bacteria cooperate syntrophically with methanogens and homoacetogens at minimum energy increments via interspecies electron transfer. The energy yields of the partner organisms in these cooperations have so far been calculated based mainly on hydrogen partial pressures. In the present study, we also analyzed pools of formate as an alternative electron carrier in sediment cores of an oligotrophic lake. The formate and hydrogen pools appeared to be energetically nearly equivalent and are likely to be used simultaneously for interspecies electron transfer. Calculations of reaction energies of the partners involved suggest that propionate degradation may also proceed through the pathway, which converts propionate via butyrate and acetate to three acetate residues, thus circumventing one energetically difficult fatty acid oxidation step.

Coupled Aerobic Methane Oxidation and Arsenate Reduction Contributes to Soil-Arsenic Mobilization in Agricultural Fields

“…Overall, reaction stoichiometry, metagenomic analyses, and metabolite measurements all support a synergistic nature of methane-dependent arsenate reduction, carried out by the aerobic methanotrophs and members of Burkholderiaceae, with formate as the interspecies electron carrier. Formate is well known to support methanogenesis-based syntrophy − and was demonstrated to mediate the methane-oxidation-based selenate reduction recently . The present study provides another clear example for formate coupling aeMO to the reduction of oxides, highlighting the possibility that similar trophic relationships may link methane metabolism to a range of terminal electron acceptors in (hyp)­oxic environments.…”

Stimulation of Smithella‐dominating propionate oxidation in a sediment enrichment by magnetite and carbon nanotubes

“…) suggests that this pathway was indeed responsible for propionate oxidation in the enrichment cultivation. Smithella have been reported to play an important role in propionate degradation in different environments including paddy field soils (Lueders et al ., ; Gan et al ., ), natural wetlands (Chauhan and Ogram, ), lake sediment (Montag and Schink, ) and anaerobic bioreactors (Zhang et al ., ). These organisms seem also to be adapted to various harsh conditions in bioreactors such as low propionate concentration (Ariesyady et al ., ), limitation of trace elements Mo, W and Se (Worm et al ., ) and high organic loading and toxic accumulation (Ban et al ., ).…”

Isolation and genomic and physiological characterization ofParageobacillussp. G301, the isolate capable of both hydrogenogenic and aerobic carbon monoxide oxidation

“…Thus, G301 would gain energy with CO-mediated respiration in disparate environmental conditions. This metabolic trait may be advantageous in an oxic-anoxic interface because it allows prokaryotes to use CO from the atmosphere or other sources such as hydrothermal vents (72), soil (73), seawater (74) or freshwater environments (75, 76) with fluctuating O 2 levels. Explorations in such changeable environmental conditions would lead to the discovery of novel CO oxidizers with previously unknown combinations of distinct CO metabolisms, providing further insight into the diversity, evolution, and industrial applications of such prokaryotes with intriguing respiration.…”