Genomic Evidence for Phototrophic Oxidation of Small Alkanes in a Member of the Chloroflexi Phylum

Biological methane cycling plays an important role in Earths climate and the global carbon cycle, with biological methane oxidation (methanotrophy) modulating methane release from numerous environments including soils, sediments, and water columns. Methanotrophy is typically coupled to aerobic respiration or anaerobically via the reduction of sulfate, nitrate, or metal oxides, and while the possibility of coupling methane oxidation to phototrophy (photomethanotrophy) has been proposed, no organism has ever been described that is capable of this metabolism. Here we described a new bacterial genome from a member of the Chloroflexi phylum--termed here Candidatus Chlorolinea photomethanotrophicum--with cooccurring methanotrophy and phototrophy pathways, suggesting a novel link between these two metabolisms. Recovered as a metagenome-assembled genome from microbial mats in an iron-rich hot spring in Japan, Ca. C. photomethanotrophicum forms a new lineage within the Chloroflexi phylum and expands the known metabolic diversity of this already diverse clade. Ca. C. photomethanotrophicum appears to be metabolically versatile, capable of phototrophy (via a Type 2 reaction center), aerobic respiration, nitrite reduction, oxidation of methane and carbon monoxide, and potentially carbon fixation via a novel pathway composed of hybridized components of the serine cycle and the 3-hydroxypropionate bicycle. The biochemical network of this organism is constructed from components from multiple organisms and pathways, further demonstrating the modular nature of metabolic machinery and the ecological and evolutionary importance of horizontal gene transfer in the establishment of novel pathways. SignificanceMethane is a major greenhouse gas, and the production and consumption of methane is largely driven by the metabolism of microorganisms. Although it has been hypothesized for decades that some bacteria may be capable of growth by eating methane and conserving energy from sunlight (photomethanotrophy), this metabolism has never been discovered in nature. Here, we describe the first genetic evidence for a bacterium capable of photomethanotrophy, adding a new pathway to the known diversity of how microbes can make a living. This discovery also adds a new link to the global carbon cycle, and may provide new opportunities for designing biotechnological tools for processing methane.