Genomic Reconstruction of an Uncultured Hydrothermal Vent Gammaproteobacterial Methanotroph (Family Methylothermaceae) Indicates Multiple Adaptations to Oxygen Limitation

Abstract

Hydrothermal vents are an important contributor to marine biogeochemistry, producing large volumes of reduced fluids, gasses, and metals and housing unique, productive microbial and animal communities fueled by chemosynthesis. Methane is a common constituent of hydrothermal vent fluid and is frequently consumed at vent sites by methanotrophic bacteria that serve to control escape of this greenhouse gas into the atmosphere. Despite their ecological and geochemical importance, little is known about the ecophysiology of uncultured hydrothermal vent-associated methanotrophic bacteria. Using metagenomic binning techniques, we recovered and analyzed a near-complete genome from a novel gammaproteobacterial methanotroph (B42) associated with a white smoker chimney in the Southern Lau basin. B42 was the dominant methanotroph in the community, at ∼80x coverage, with only four others detected in the metagenome, all on low coverage contigs (7x–12x). Phylogenetic placement of B42 showed it is a member of the Methylothermaceae, a family currently represented by only one sequenced genome. Metabolic inferences based on the presence of known pathways in the genome showed that B42 possesses a branched respiratory chain with A- and B-family heme copper oxidases, cytochrome bd oxidase and a partial denitrification pathway. These genes could allow B42 to respire over a wide range of oxygen concentrations within the highly dynamic vent environment. Phylogenies of the denitrification genes revealed they are the result of separate horizontal gene transfer from other Proteobacteria and suggest that denitrification is a selective advantage in conditions where extremely low oxygen concentrations require all oxygen to be used for methane activation.

Patiriisocius marinistellae gen. nov., sp. nov., isolated from the starfish Patiria pectinifera, and reclassification of Ulvibacter marinus as a member of the genus Patiriisocius comb. nov.

“…Although U. marinus IMCC12008 T made a robust cluster with strain KK4 T in the phylogenetic trees based on 16S rRNA genes, UBGCs and DarAB (Figs 1 and 2, S2), the AAI value between them was 72.5 % (), which was around the genus boundary provided by previous studies [28–31] and this study; type strains in the UMA cluster shared >73 % AAI values in each genus (73.7 % in Ulvibater ; 75.0–84.5 % in Aequorivita (Table S7). Similarity in 16S rRNA gene between strain KK4 T and U.…”

“…Moreover, AAI between strain KK4 T / U. marinus IMCC12008 T and other related strains were 61.9–68.2% and 61.5–67.4 % (), which are lower than the genus delineation threshold (70–76 %) recommended in previous studies [28–31]. These results indicated the novel genus status of strain KK4 T as well as U.…”

Phototrophic Methane Oxidation in a Member of the Chloroflexi Phylum

“…In nonphototrophic aerobic methanotrophs, electrons from methane are run through electron transport chains and ultimately donated to O 2 (or, rarely, oxidized nitrogen species, e.g. Skennerton et al 2015) at complex IV; this respiration of methane-derived electrons results in a small, finite number of protons pumped across the membrane per methane molecule oxidized, in contrast to phototrophs which can conserve energy from light via cyclic electron transfer without net consumption of electrons. As a result, the energetic yield per methane molecule of photomethanotrophy could be much higher than purely respiratory methanotrophy.…”

“…C. photoalkanotrophicum was recovered (Ward et al 2017a), but this organism also encodes genes for cytochrome c552 nitrite reductase which is capable of reducing hydroxylamine to ammonia (Einsle et al 1999); genes for this enzyme appear to have been acquired via HGT, and may be an adaptation to avoid hydroxylamine toxicity due to incidental ammonia oxidation-a strategy observed in some denitrifying methanotrophs (e.g. Skennerton et al 2015). However, this incidental ammonia cycling would neither yield a net flux of oxidized nitrogen species nor provide electrons for the phototrophic electron transport chain in Ca.…”

Follow the Oxygen: Comparative Histories of Planetary Oxygenation and Opportunities for Aerobic Life

“…This metabolism requires O 2 for the activation of methane and typically couples this process to aerobic respiration (Hanson and Hanson, 1996). Recently, however, it has been discovered that the terminal electron accepting process for this metabolism is more versatile than previously realized, with the potential in some bacteria to couple aerobic methanotrophy to nitrate reduction when O 2 concentrations are low (e.g., Kits et al, 2015;Skennerton et al, 2015). The recent discovery of nitrate in martian sediment (Stern et al, 2015) therefore additionally supports the potential viability of this metabolism in some martian environments.…”