ALBERT

Beschreibung: Methanogenesis and anaerobic methane oxidation through methyl-coenzyme M reductase (MCR) as a key enzyme have been suggested to be basal pathways of archaea1. How widespread MCR-based alkane metabolism is among archaea, where it occurs and how it evolved remain elusive. Here, we performed a global survey of MCR-encoding genomes based on metagenomic data from various environments. Eleven high-quality mcr-containing metagenomic-assembled genomes were obtained belonging to the Archaeoglobi in the Euryarchaeota, Hadesarchaeota and different TACK superphylum archaea, including the Nezhaarchaeota, Korarchaeota and Verstraetearchaeota. Archaeoglobi WYZ-LMO1 and WYZ-LMO3 and Korarchaeota WYZ-LMO9 encode both the (reverse) methanogenesis and the dissimilatory sulfate reduction pathway, suggesting that they have the genomic potential to couple both pathways in individual organisms. The Hadesarchaeota WYZ-LMO4–6 and Archaeoglobi JdFR-42 encode highly divergent MCRs, enzymes that may enable them to thrive on non-methane alkanes. The occurrence of mcr genes in different archaeal phyla indicates that MCR-based alkane metabolism is common in the domain of Archaea.

Beschreibung: Methyl‐coenzyme M reductase (MCR) has been originally identified to catalyse the final step of the methanogenesis pathway. About 20 years ago an aerobic me thane‐oxidizing archaea (ANME) were discovered that use MCR enzymes to activate methane. ANME thrive at the thermodynamic limit of life, are slow‐growing, and in most cases form syntrophic consortia with sulfate‐reducing bacteria. Recently, archaea that have the ability to anaerobically oxidize non‐methane multi‐carbon alkanes such as ethane and n ‐butane were described in both enrichment cultures and environmental samples. These an aerobic multi‐carbon alka ne‐oxidizing archaea (ANKA) use enzymes homologous to MCR named alkyl‐coenzyme M reductase (ACR). Here we review the recent progresses on the diversity, distribution and functioning of both ANME and ANKA by presenting a detailed MCR/ACR‐based phylogeny, compare their metabolic pathways and discuss the gaps in our knowledge of physiology of these organisms. To improve our understanding of alkane oxidation in archaea, we identified three directions for future research: (i) expanding cultivation attempts to validate omics‐based metabolic models of yet‐uncultured organisms, (ii) performing biochemical and structural analyses of key enzymes to understand thermodynamic and steric constraints and (iii) investigating the evolution of anaerobic alkane metabolisms and their impact on biogeochemical cycles.

Beschreibung: Methanogens are considered as one of the earliest life forms on Earth, and together with anaerobic methane-oxidizing archaea, they have crucial effects on climate stability. However, the origin and evolution of anaerobic alkane metabolism in the domain Archaea remain controversial. Here, we present evidence that methylotrophic methanogenesis was the ancestral form of this metabolism. Carbon dioxide–reducing methanogenesis developed later through the evolution of tetrahydromethanopterin S-methyltransferase, which linked methanogenesis to the Wood-Ljungdahl pathway for energy conservation. Anaerobic multicarbon alkane metabolisms in Archaea also originated early, with genes coding for the activation of short-chain or even long-chain alkanes likely evolving from an ethane-metabolizing ancestor. These genes were likely horizontally transferred to multiple archaeal clades including Candidatus (Ca.) Bathyarchaeia, Ca. Lokiarchaeia, Ca. Hadarchaeia, and the methanogenic Ca. Methanoliparia.

Beschreibung: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Hou, J., Sievert, S. M., Wang, Y., Seewald, J. S., Natarajan, V. P., Wang, F., & Xiao, X. Microbial succession during the transition from active to inactive stages of deep-sea hydrothermal vent sulfide chimneys. Microbiome, 8(1), (2020): 102, doi:10.1186/s40168-020-00851-8.

Beschreibung: Background Deep-sea hydrothermal vents are highly productive biodiversity hotspots in the deep ocean supported by chemosynthetic microorganisms. Prominent features of these systems are sulfide chimneys emanating high-temperature hydrothermal fluids. While several studies have investigated the microbial diversity in both active and inactive sulfide chimneys that have been extinct for up to thousands of years, little is known about chimneys that have ceased activity more recently, as well as the microbial succession occurring during the transition from active to inactive chimneys. Results Genome-resolved metagenomics was applied to an active and a recently extinct (~ 7 years) sulfide chimney from the 9–10° N hydrothermal vent field on the East Pacific Rise. Full-length 16S rRNA gene and a total of 173 high-quality metagenome assembled genomes (MAGs) were retrieved for comparative analysis. In the active chimney (L-vent), sulfide- and/or hydrogen-oxidizing Campylobacteria and Aquificae with the potential for denitrification were identified as the dominant community members and primary producers, fixing carbon through the reductive tricarboxylic acid (rTCA) cycle. In contrast, the microbiome of the recently extinct chimney (M-vent) was largely composed of heterotrophs from various bacterial phyla, including Delta-/Beta-/Alphaproteobacteria and Bacteroidetes. Gammaproteobacteria were identified as the main primary producers, using the oxidation of metal sulfides and/or iron oxidation coupled to nitrate reduction to fix carbon through the Calvin-Benson-Bassham (CBB) cycle. Further analysis revealed a phylogenetically distinct Nitrospirae cluster that has the potential to oxidize sulfide minerals coupled to oxygen and/or nitrite reduction, as well as for sulfate reduction, and that might serve as an indicator for the early stages of chimneys after venting has ceased. Conclusions This study sheds light on the composition, metabolic functions, and succession of microbial communities inhabiting deep-sea hydrothermal vent sulfide chimneys. Collectively, microbial succession during the life span of a chimney could be described to proceed from a “fluid-shaped” microbial community in newly formed and actively venting chimneys supported by the oxidation of reductants in the hydrothermal fluid to a “mineral-shaped” community supported by the oxidation of minerals after hydrothermal activity has ceased. Remarkably, the transition appears to occur within the first few years, after which the communities stay stable for thousands of years.

Beschreibung: This work was supported by the China Ocean Mineral Resources R&D Association (grant No. DY135-B2-12), the Natural Science Foundation of China (grant No. 41530967, 41921006, 91751205), the Senior User Project of RV KEXUE (KEXUE2019GZ06), and by the US National Science Foundation grant OCE-1136727 and the WHOI Investment in Science Fund to S.M.S.

Beschreibung: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Vigderovich, H., Liang, L., Herut, B., Wang, F., Wurgaft, E., Rubin-Blum, M., & Sivan, O. Evidence for microbial iron reduction in the methanic sediments of the oligotrophic southeastern Mediterranean continental shelf. Biogeosciences, 16(16), (2019): 3165-3181, doi: 10.5194/bg-16-3165-2019.

Beschreibung: Dissimilatory iron reduction is probably one of the oldest types of metabolisms that still participates in important biogeochemical cycles, such as those of carbon and sulfur. It is one of the more energetically favorable anaerobic microbial respiration processes and is usually coupled to the oxidation of organic matter. Traditionally this process is thought to be limited to the shallow part of the sedimentary column in most aquatic systems. However, iron reduction has also been observed in the methanic zone of many marine and freshwater sediments, well below its expected zone and occasionally accompanied by decreases in methane, suggesting a link between the iron and the methane cycles. Nevertheless, the mechanistic nature of this link (competition, redox or other) has yet to be established and has not been studied in oligotrophic shallow marine sediments. In this study we present combined geochemical and molecular evidences for microbial iron reduction in the methanic zone of the oligotrophic southeastern (SE) Mediterranean continental shelf. Geochemical porewater profiles indicate iron reduction in two zones, the uppermost part of the sediment, and the deeper zone, in the layer of high methane concentration. Results from a slurry incubation experiment indicate that the deep methanic iron reduction is microbially mediated. The sedimentary profiles of microbial abundance and quantitative PCR (qPCR) of the mcrA gene, together with Spearman correlation between the microbial data and Fe(II) concentrations in the porewater, suggest types of potential microorganisms that may be involved in the iron reduction via several potential pathways: H2 or organic matter oxidation, an active sulfur cycle, or iron-driven anaerobic oxidation of methane. We suggest that significant upward migration of methane in the sedimentary column and its oxidation by sulfate may fuel the microbial activity in the sulfate methane transition zone (SMTZ). The biomass created by this microbial activity can be used by the iron reducers below, in the methanic zone of the sediments of the SE Mediterranean.

Beschreibung: This study was supported by the joint grant of Israel Science Foundation and the National Natural Science Foundation of China (ISF-NSFC) (grant numbers 31661143022 (FW) and 2561/16 (OS)). Funding was provided to Hanni Vigderovich by the Mediterranean Sea Research Center of Israel.

Beschreibung: Members of the archaeal phylum Bathyarchaeota are among the most abundant microorganisms on Earth. Although versatile metabolic capabilities such as acetogenesis, methanogenesis, and fermentation have been suggested for bathyarchaeotal members, no direct confirmation of these metabolic functions has been achieved through growth of Bathyarchaeota in the laboratory. Here we demonstrate, on the basis of gene-copy numbers and probing of archaeal lipids, the growth of Bathyarchaeota subgroup Bathy-8 in enrichments of estuarine sediments with the biopolymer lignin. Other organic substrates (casein, oleic acid, cellulose, and phenol) did not significantly stimulate growth of Bathyarchaeota. Meanwhile, putative bathyarchaeotal tetraether lipids incorporated 13C from 13C-bicarbonate only when added in concert with lignin. Our results are consistent with organoautotrophic growth of a bathyarchaeotal group with lignin as an energy source and bicarbonate as a carbon source and shed light into the cycling of one of Earth’s most abundant biopolymers in anoxic marine sediment.