title: Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions.
abstract: The utilization of methane, a potent greenhouse gas, is an important component of local and global carbon cycles that is characterized by tight linkages between methane-utilizing (methanotrophic) and nonmethanotrophic bacteria. It has been suggested that the methanotroph sustains these nonmethanotrophs by cross-feeding, because subsequent products of the methane oxidation pathway, such as methanol, represent alternative carbon sources. We established cocultures in a microcosm model system to determine the mechanism and substrate that underlay the observed cross-feeding in the environment. Lanthanum, a rare earth element, was applied because of its increasing importance in methylotrophy. We used co-occurring strains isolated from Lake Washington sediment that are involved in methane utilization: a methanotroph and two nonmethanotrophic methylotrophs. Gene-expression profiles and mutant analyses suggest that methanol is the dominant carbon and energy source the methanotroph provides to support growth of the nonmethanotrophs. However, in the presence of the nonmethanotroph, gene expression of the dominant methanol dehydrogenase (MDH) shifts from the lanthanide-dependent MDH (XoxF)-type, to the calcium-dependent MDH (MxaF)-type. Correspondingly, methanol is released into the medium only when the methanotroph expresses the MxaF-type MDH. These results suggest a cross-feeding mechanism in which the nonmethanotrophic partner induces a change in expression of methanotroph MDHs, resulting in release of methanol for its growth. This partner-induced change in gene expression that benefits the partner is a paradigm for microbial interactions that cannot be observed in studies of pure cultures, underscoring the importance of synthetic microbial community approaches to understand environmental microbiomes.
authors.affiliation: Department of Chemical Engineering, University of Washington, Seattle, WA 98195.|Department of Microbiology, University of Washington, WA 98195.
authors.forename: Sascha M B
authors.initials: SM
authors.lastname: Krause
authors.affiliation: Department of Microbiology, University of Washington, WA 98195.
authors.forename: Timothy
authors.initials: T
authors.lastname: Johnson
authors.affiliation: Department of Microbiology, University of Washington, WA 98195.
authors.forename: Yasodara
authors.initials: Y
authors.lastname: Samadhi Karunaratne
authors.affiliation: Department of Chemical Engineering, University of Washington, Seattle, WA 98195.
authors.forename: Yanfen
authors.initials: Y
authors.lastname: Fu
authors.affiliation: Department of Chemical Engineering, University of Washington, Seattle, WA 98195.|eScience Institute, University of Washington, WA 98195.
authors.forename: David A C
authors.initials: DA
authors.lastname: Beck
authors.affiliation: Department of Chemical Engineering, University of Washington, Seattle, WA 98195.
authors.forename: Ludmila
authors.initials: L
authors.lastname: Chistoserdova
authors.affiliation: Department of Chemical Engineering, University of Washington, Seattle, WA 98195; lidstrom@uw.edu.|Department of Microbiology, University of Washington, WA 98195.
authors.forename: Mary E
authors.identifier: 0000-0002-1949-2792
authors.initials: ME
authors.lastname: Lidstrom
mesh_terms: D000429:Alcohol Oxidoreductases / Q000378:metabolism; D001419:Bacteria / Q000187:drug effects / Q000378:metabolism*; D001426:Bacterial Proteins / Q000378:metabolism; D002244:Carbon / Q000378:metabolism*; D015964:Gene Expression Regulation, Bacterial / Q000187:drug effects; D028581:Lanthanoid Series Elements / Q000494:pharmacology*; D008697:Methane / Q000378:metabolism*; D000432:Methanol / Q000378:metabolism; D056265:Microbial Interactions / Q000187:drug effects*; D010084:Oxidation-Reduction / Q000187:drug effects; D014861:Washington
chemical_list: D001426:Bacterial Proteins; D028581:Lanthanoid Series Elements; D002244:Carbon; D000429:Alcohol Oxidoreductases; C019641:alcohol dehydrogenase (acceptor); D008697:Methane; D000432:Methanol
keywords: Methylobacter; eco-physiology; flow cytometry; metabolic transformation; synthetic ecology