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Heterotrophic growth on formate is dependent on the maintenance of intracellular pH for the thermoacidophilic methanotroph Methylacidiphilum sp RTK17.1.

ABSTRACT: In this work, we investigated intracellular pH homeostasis within the thermoacidophilc methanotroph Methylacidiphilum sp. RTK17.1. Our findings show the proton motive force for this species is primarily generated by a pH gradient across the cellular membrane. In batch experiments, the addition of formate resulted in no observable cell growth and, correspondingly, acidification of the cytosol, decreased formate dehydrogenase activity and (presumably) cell-death. Nevertheless, we were able to demonstrable growth on formate as the sole source of metabolizable energy was possible in steady-state (continuous) cultures following the transition from methanol to formate. Under these conditions, biomass productivity yields on formate were 63% less than for growth on methanol. Transcriptome analysis revealed key genes associated with pH homeostasis, methane, methanol and formate metabolism were significantly regulated in response to growth on formate. Collectively, these results suggest environmental formate represents a utilisable source of energy/carbon to the acidophilic methanotrophs during periods of methane starvations and highlights potential short-comings of traditional batch-culture physiological characterisation studies in acidophilic species.

ORGANISM(S): Candidatus Methylacidiphilum infernorum

PROVIDER: GSE145277 | GEO | 2020/10/31

REPOSITORIES: GEO

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Project description:Metabolic flexibility in aerobic methane oxidising bacteria (methanotrophs) enhances cell growth and survival in instances where resources are variable or limiting. Examples include the production of intracellular compounds (such as glycogen or polyhydroxyalkanoates) in response to unbalanced growth conditions and the use of some energy substrates, besides methane, when available. Indeed, recent studies show that verrucomicrobial methanotrophs can grow mixotrophically through oxidation of hydrogen and methane gases via respiratory membrane-bound group 1d [NiFe] hydrogenases and methane monooxygenases respectively. Hydrogen metabolism is particularly important for adaptation to methane and oxygen limitation, suggesting this metabolic flexibility may confer growth and survival advantages. In this work, we provide evidence that, in adopting a mixotrophic growth strategy, the thermoacidophilic methanotroph, Methylacidiphilum sp. RTK17.1 changes its growth rate, biomass yields and the production of intracellular glycogen reservoirs. Under nitrogen-fixing conditions, removal of hydrogen from the feed-gas resulted in a 14 % reduction in observed growth rates and a 144% increase in cellular glycogen content. Concomitant with increases in glycogen content, the total protein content of biomass decreased following the removal of hydrogen. Transcriptome analysis of Methylacidiphilum sp. RTK17.1 revealed a 3.5-fold upregulation of the Group 1d [NiFe] hydrogenase in response to oxygen limitation and a 4-fold upregulation of nitrogenase encoding genes (nifHDKENX) in response to nitrogen limitation. Genes associated with glycogen synthesis and degradation were expressed constitutively and did not display evidence of transcriptional regulation. Collectively these data further challenge the belief that hydrogen metabolism in methanotrophic bacteria is primarily associated with energy conservation during nitrogen fixation and suggests its utilisation provides a competitive growth advantage within hypoxic habitats.

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Heterotrophic growth on formate is dependent on the maintenance of intracellular pH for the thermoacidophilic methanotroph Methylacidiphilum sp RTK17.1.

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