Candidatus Alkanophaga archaea from heated hydrothermal vent sediment oxidize petroleum alkanes

Abstract

The methyl-coenzyme M reductase (Mcr) enables archaea to produce and oxidize methane, critically impacting the global greenhouse gas budget. Recently cultured archaea activate short- and long-chain n-alkanes with divergent Mcr variants, termed alkyl-coenzyme M reductases (Acrs). Here, we probed the anaerobic oxidation of mid-chain petroleum alkanes at 70°C using oil-rich sediments from the Guaymas Basin. Incubations with alkanes from pentane to tetradecane produced active cultures. In these cultures, archaea of the genus Candidatus Alkanophaga activate the alkanes with Acrs and completely oxidize the alkyl groups to CO2. Ca. Alkanophaga form a deep-branching sister clade to the methanotrophs ANME-1 and are closely related to the short-chain alkane oxidizers Ca. Syntrophoarchaeum. This suggests that multi-carbon alkane metabolism preceded methane metabolism in the class Syntrophoarchaeia. Ca. Alkanophaga shuttle the electrons from alkane oxidation to sulfate-reducing Thermodesulfobacteria. The two partners form consortia that are potential key players in petroleum degradation in heated oil reservoirs.

Discovery of two archaeal GDGT lipid modifying enzymes reveals diverse microbes capable of H-GDGT biosynthesis and modification

“…Of particular interest are two Euryarchaeota MAGs within Alkanophaga and Thermoplasmata. The first MAG belongs to Candidatus Alkanophaga volatiphilum, an “oil eating” (C 5 -C 7 hydrocarbons) microbe identified in an anoxic, thermophilic (70 °C) enrichment culture from Guaymas Basin sediments (52). It is plausible that organisms like Candidatus Alkanophaga volatiphilum would associate closely with oil in these settings and their highly cyclized H-GDGTs would be deposited and diagenetically degraded into ARN acids.…”

Beyond methane, new frontiers in anaerobic microbial hydrocarbon utilizing pathways

“…Ca. Alkanophaga utilizes alkanes containing 5–14 carbon atoms and fully oxidizes the alkyl groups to CO 2 (Zehnle et al., 2023). An additional long‐chain activating ACR was recently discovered in Ca.…”

“…While sulfate‐reducing and denitrifying bacteria were initially recognized as the first microbes known to consume alkanes anaerobically, our understanding of alkane utilization has greatly expanded since these initial findings (Aeckersberg et al., 1991; Ehrenreich et al., 2000). Both archaea and bacteria can anaerobically activate methane and long‐chain hydrocarbons such as hexadecane and tetradecane using sulfate or nitrite as terminal electron acceptors (Borrel, 2022; Ettwig et al., 2010; Zehnle et al., 2023; Zhou et al., 2022). Our understanding of alkane utilization has expanded, now including metals and carbon dioxide as terminal electron acceptors, broadening the range of environments where these anaerobic microbes can survive (Ji et al., 2020; Leu et al., 2020).…”