Association of hydrogen metabolism with unitrophic or mixotrophic growth of Methanosarcina barkeri on carbon monoxide

Abstract

Methanosarcina barkeri was adapted to grow on carbon monoxide by sequential transfer of the culture in medium that contained CO (100% of culture headspace). These experiments document the ability of the organism to grow slowly (65-h doubling time) and to produce methane and CO2 either on CO as the sole carbon and energy source or by the simultaneous consumption of methanol and CO. During growth on CO as carbon and energy source, net hydrogen formation occurred when the CO partial pressure in the culture headspace was greater than 20% CO, but hydrogen was consumed when the CO concentration was below this value.Carbon monoxide is an abundant atmospheric pollutant generated by incomplete conbustion of fossil fuels. Carbon monoxide is also formed as a metabolite of microbial metabolism, especially heme degradation by aerobic microorganisms (5,19). The physiological features of anaerobic bacteria that are able to grow on various one-carbon substrates as the sole carbon and electron source (i.e., unicarbonotrophic growth) and to grow mixotrophically on mixtures of onecarbon substrates, including CO, have been reviewed (20). Several genera of anaerobic bacteria have been shown to grow on CO as the energy source, including: Rhodopseudomonas (18), Methanobacterium (2), Butyribacterium (4), Eubacterium (13), Clostridium (9), and Acetobacterium (8).Kluyver and Schnellen (10) demonstrated that Methanosarcina barkeri produced 1 mol of methane and 3 mol of CO2 from 4 mol of CO when cell suspensions were incubated under 1 atm (ca. 101.29 kPa) (100%) of this gas. Later, Daniels et al.(2) showed that M. barkeri oxidized small amounts of added CO during growth on H2-CO2 and that cell extracts contained a methyl viologen-linked CO dehydrogenase activity. The significance of CO metabolism by some anaerobes like Clostridium pasteurianum is enigmatic because this anaerobe consumes CO via CO dehydrogenase activity, but it is not capable of growth on this substrate (3). However, it was established that acetogenic species, like Clostridium thermoaceticum, made acetate during growth with CO as the carbon and energy source (9). Carbon monoxide dehydrogenase has been proposed to function in carbonylation of a methyl group during acetyl-coenzyme Aacetate synthesis in both acetogenic (6) and methanogenic (7, 17) anaerobes. Krzycki and Zeikus (11) reported that the level of this enzyme increased fivefold when M. barkeri was grown on acetate versus on H2-CO2 or methanol as the sole carbon and energy source. This result suggested that CO dehydrogenase of M. barkeri may also function in acetate dissimilation by a biochemical mechanism that involves the production and consumption of a carbonyl group as an intermediary step in methane and CO2 formation. In the present note, we show that M. barkeri is able to grow either * Corresponding author. unicarbonotrophically with CO as the sole carbon and energy source or mixotrophically with CO and methanol.M. barkeri neotype strain MS was routinely cultivated under strictly anoxic conditions in a phosphat...

Carbon monoxide conversion by anaerobic bioreactor sludges

“…The absence of direct methanogenic CO conversion, as found for Nedalco sludge at 30 ‡C, might be explained by a complete inactivation of methanogens due to the high CO concentration in the gas phase [2]. Only M. barkeri has so far been reported to grow at 100% CO in the gas phase after long-term adaptation to slowly increasing CO concentrations [13]. Disrupting the granular structure of the methane-producing sludges resulted in a strongly increased exposure of the active biomass to CO and led to a strong inhibition of methane formation.…”

“…Methanothermobacter thermoautotrophicus [12], and acetotrophic, e.g. Methanosarcina barkeri [13], methanogenesis.…”

Carbon monoxide consumption and production by wetland peats

“…Methanogenic, acetogenic, and sulfate-reducing bacteria are known to oxidize CO via a carbon monoxide dehydrogenase [6]. Several methanogenic strains consume CO during growth on H P and CO P , but growth on CO is very limited [17,24]. Desulfovibrio vulgaris utilizes CO for energy and sulfate reduction, but concentrations s 4.5% in the headspace are inhibitory [14].…”

Enrichment of syngas‐converting communities from a multi‐orifice baffled bioreactor

“…Vancomycin and erythromycin are bacterial inhibitors and the fact that no CO conversion was observed in their presence indicates that CO was not directly metabolized by carboxydotrophic methanogens. Carbon monoxide is inhibitory for most methanogens, and only a few species can actually grow on this substrate: Methanothermobacter thermoautotrophicus (Daniels et al, 1977), Methanothermobacter marburguensis (Diender et al, 2016), Methanosarcina barkeri (O'Brien et al, 1984;Bott et al, 1986) and Methanosarcina acetivorans (Rother and Metcalf, 2004). Both thermophilic Methanothermobacter species grow significantly slower on CO than on H 2 /CO 2 (Daniels et al, 1977;Diender et al, 2016).…”