Correlation of Key Physiological Properties of Methanosarcina Isolates with Environment of Origin

• Published in: Applied and environmental microbiology Vol. 87; no. 13; p. e0073121
• Main Authors: Zhou, Jinjie, Holmes, Dawn E, Tang, Hai-Yan, Lovley, Derek R
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 11.06.2021
• Subjects: Acetates - metabolism; Acetic acid; Anaerobic digestion; Anaerobiosis; Bioreactors; Carbon; Cycles; Cytochrome; Cytochromes; Digesters; Ecosystem; Electron density; Electron transfer; Electron Transport; Energy conservation; Energy metabolism; Environmental Microbiology; Ethanol - metabolism; Genome, Archaeal; Genomes; Geographical distribution; Greenhouse gases; Hydrogen - metabolism; Hydrogen production; Hydrogenase; Metabolism; Metagenomics; Methane; Methane - metabolism; Methanosarcina; Methanosarcina - genetics; Methanosarcina - isolation & purification; Methanosarcina - metabolism; Organic soils; Organic wastes; Phylogeny; Physiology; Relative abundance; Renewable energy; Sediments; Soils; Species; Substrates; Methanosarcina; extracellular electron transfer; anaerobic respiration; methanogen; c-type cytochrome; Rnf complex; direct interspecies electron transfer (DIET); archaea
• ISSN: 0099-2240; 1098-5336; 1098-5336
• DOI: 10.1128/AEM.00731-21

It is known that the physiology of species can differ significantly, but the ecological impact of these differences is unclear. We recovered two strains of from two different ecosystems with a similar enrichment and isolation method. Both strains had the same ability to metabolize organic substrates and participate in direct interspecies electron transfer but also had major physiological differences. Strain DH-1, which was isolated from an anaerobic digester, used H as an electron donor. Genome analysis indicated that it lacks an Rnf complex and conserves energy from acetate metabolism via intracellular H cycling. In contrast, strain DH-2, a subsurface isolate, lacks hydrogenases required for H uptake and cycling and has an Rnf complex for energy conservation when growing on acetate. Further analysis of the genomes of previously described isolates, as well as phylogenetic and metagenomic data on uncultured in anaerobic digesters and diverse soils and sediments, revealed a physiological dichotomy that corresponded with environment of origin. The physiology of type I revolves around H production and consumption. In contrast, type II species eschew H and have genes for an Rnf complex and the multiheme, membrane-bound -type cytochrome MmcA, shown to be essential for extracellular electron transfer. The distribution of species in diverse environments suggests that the type I H -based physiology is well suited for high-energy environments, like anaerobic digesters, whereas type II Rnf/cytochrome-based physiology is an adaptation to the slower, steady-state carbon and electron fluxes common in organic-poor anaerobic soils and sediments. Biogenic methane is a significant greenhouse gas, and the conversion of organic wastes to methane is an important bioenergy process. species play an important role in methane production in many methanogenic soils and sediments as well as anaerobic waste digesters. The studies reported here emphasize that the genus is composed of two physiologically distinct groups. This is important to recognize when interpreting the role of in methanogenic environments, especially regarding H metabolism. Furthermore, the finding that type I species predominate in environments with high rates of carbon and electron flux and that type II species predominate in lower-energy environments suggests that evaluating the relative abundance of type I and type II may provide further insights into rates of carbon and electron flux in methanogenic environments.