Metabolic Basis for the Microbial Oxidation of Atmospheric Methane

Abstract

Abstract Atmospheric methane oxidizing bacteria (atmMOB) constitute the sole biological sink for atmospheric methane and have been discovered worldwide over the past decades. Still, insufficient knowledge about the metabolic basis of atmMOB, caused by the lack of pure cultures, limits our ability to manage, study, and exploit the atmospheric methane sink and thus to fight the 21st century methane surge. Here we combine filter cultivation, trace gas oxidation, 15N2-incorporation experiments, and comparative proteomics, to assess the potential of seven methanotrophic species to grow on atmospheric methane. Four species, three of which are outside the canonical atmMOB group USCα, enduringly oxidized atmospheric methane, hydrogen, and carbon monoxide with distinct substrate preferences over a 12-month growth period "on air". Despite this mixotrophy and high specific affinities for methane, the estimated energy yields of the atmMOB were substantially lower than previously assumed necessary for cellular maintenance, contradicting the basic energy premise for atmMOB. Comparative proteomics indicate major physiological adjustments to grow “on air” as the atmMOB allocated their proteomes to decrease energy intensive processes, including biosynthesis, and increase investments into trace gases oxidation. Our work outlines the metabolic basis of atmMOB, microorganisms that exploit the atmosphere as energy and carbon source while mitigating the potent greenhouse gas methane.