ANME-1 archaea drive methane accumulation and removal in estuarine sediments

Abstract

Uncultured members of the Methanomicrobia called ANME-1 perform the anaerobic oxidation of methane (AOM) through a process that uses much of the methanogenic pathway. It is unknown whether ANME-1 obligately perform AOM, or whether some of them can perform methanogenesis when methanogenesis is exergonic. Most marine sediments lack advective transport of methane, so AOM occurs in the sulfate methane transition zone (SMTZ) where sulfate-reducing bacteria consume hydrogen produced by fermenters, making hydrogenotrophic methanogenesis exergonic in the reverse direction. When sulfate is depleted deeper in the sediments, hydrogen accumulates making hydrogenotrophic methanogenesis exergonic, and methane accumulates in the methane zone (MZ). In White Oak River estuarine sediments, we found that ANME-1 comprised 99.5% of 16S rRNA genes from amplicons and 100% of 16S rRNA genes from metagenomes of the Methanomicrobia in the SMTZ and 99.9% and 98.3%, respectively, in the MZ. Each of the 16 ANME-1 OTUs (97% similarity) had peaks in the SMTZ that coincided with peaks of putative sulfate-reducing bacteria Desulfatiglans sp. and SEEP-SRB1. In the MZ, ANME-1, but no putative sulfate-reducing bacteria or cultured methanogens, increased with depth. Using publicly available data, we found that ANME-1 was the only group expressing methanogenic genes during both net AOM and net methanogenesis in an enrichment. The commonly-held belief that ANME-1 perform AOM is based on the fact that they dominate natural settings and enrichments where net AOM is measured. We found that ANME-1 also dominate natural settings and enrichment where net methanogenesis is measured, so we conclude that ANME-1 perform methane production. Alternating between AOM and methanogenesis, either in a single ANME-1 cell or between different subclades with similar 16S rRNA sequences of ANME-1, may confer a competitive advantage, explaining the predominance of low-energy adapted ANME-1 in methanogenic sediments worldwide.Abstract ImportanceLife may operate differently at very low energy levels. Natural populations of microbes that make methane survive on some of the lowest energy yields of all life. From all available data, we infer that these microbes alternate between methane production and oxidation, depending on which process is energy-yielding in the environment. This means that much of the methane produced naturally in marine sediments occurs through an organism that is also capable of destroying it under different circumstances.

Thermogenic hydrocarbon biodegradation by diverse depth-stratified microbial populations at a Scotian Basin cold seep

“…More surprisingly, contrary to the paradigm that gaseous alkane-oxidizing archaea normally occur where alkanes and sulfate coexist, we observed that ANME-1, ethane-oxidizing and butane-oxidizing archaea were also actively present in sulfate-depleted sediments. Based on their occurrence and activity in shallow coastal sediment cores from Aarhus Bay and White Oak River Estuary, ANME-1 has been proposed to be capable of reverse methanogenesis in sulfate-methane transition or sulfate-depleted sediments [55][56][57] . It is also possible that members of ANME-1 are contributing to methane production in the deep sea cold seep sediments investigated here.…”

The Guaymas Basin Subseafloor Sedimentary Archaeome Reflects Complex Environmental Histories

“…This lineage is closely related to ANMEs recovered from cold, anoxic habitats, such as seafloor seep sediments, methane hydrates, and hypersaline anoxic basins, and distinct from previously described ANME-1 phylotypes from Sonora Margin cold seep sediments and potentially thermophilic ANME-1 phylotypes from Guaymas Basin hydrothermal sediments ( Biddle et al., 2012 ; Holler et al., 2011 ). Although ANME-1 archaea were generally assumed to be obligate methanotrophs, this assumption has been challenged and this lineage has been proposed as potentially methanogenic, based on its occurrence and activity in sulfate-depleted sediments ( Lloyd et al., 2011 ; Kevorkian et al., 2020 ); thus, the biogeochemical role of these archaea would be modulated by the presence or absence of sulfate or concomitant changes in electron donors. ANME-2 and cultured methanogenic lineages were observed in low percent abundances in all cores in this study ( Figure S2 ).…”

Assessing the Effect of Humic Substances and Fe(III) as Potential Electron Acceptors for Anaerobic Methane Oxidation in a Marine Anoxic System

“…Recently, Desulfatiglans sp. have been found to cooccur with ANME-1 and SEEP-SRB in estuarine sediments [ 65 ]. It is, however, unknown whether the sulfur compound reduction by Desulfatiglans sp.…”

“…Besides, ANME-1b has been shown to also be capable of methanogenesis, specifically under high H 2 concentrations [ 65 ]. Although the concentration of H 2 in the incubations was not measured, H 2 may have built up as the consumption of H 2 by SRB was likely inhibited by molybdate.…”