Elemental sulfur and acetate can support life of a novel strictly anaerobic haloarchaeon

Abstract

Archaea domain is comprised of many versatile taxa that often colonize extreme habitats. Here, we report the discovery of strictly anaerobic extremely halophilic euryarchaeon, capable of obtaining energy by dissimilatory reduction of elemental sulfur using acetate as the only electron donor and forming sulfide and CO 2 as the only products. This type of respiration has never been observed in hypersaline anoxic habitats and is the first example of such metabolic capability in the entire Archaea domain. We isolated and cultivated these unusual organisms, selecting one representative strain, HSR2, for detailed characterization. Our studies including physiological tests, genome sequencing, gene expression, metabolomics and [ 14 C]-bicarbonate assimilation assays revealed that HSR2 oxidized acetate completely via the tricarboxylic acid cycle. Anabolic assimilation of acetate occurred via activated glyoxylate bypass and anaplerotic carboxylation. HSR2 possessed sulfurtransferase and an array of membrane-bound polysulfide reductase genes, all of which were expressed during the growth. Our findings suggest the biogeochemical contribution of haloarchaea in hypersaline anoxic environments must be reconsidered.

Sugar metabolism of the first thermophilic planctomycete Thermogutta terrifontis: comparative genomic and transcriptomic approaches

“…Phylogenetic analyses were performed according to Sorokin et al, 2016 using the maximum likelihood method in MEGA6 (Tamura et al, 2013). Initial multiple amino acid sequence alignments were done in Mafft 7 (Katoh et al, 2013).…”

Discrimination of haloarchaeal genera using Raman spectroscopy and robust methods for multivariate data analysis

“…Archaea belonging to Halobacteria Class (also called haloarchaea) are obligate halophilic chemo‐organotrophs abundantly present in salt lakes and other hypersaline environments (with salt concentration up to saturation limit) . In saline habitats, the haloarchaeal communities play significant roles in the biogeochemical cycling of carbon, nitrogen and, possibly sulfur . Some strains possess the unique ability of biosynthesizing silver (Ag) nanoparticles with spherical morphology .…”

Halanaeroarchaeum sulfurireducens gen. nov., sp. nov., the first obligately anaerobic sulfur-respiring haloarchaeon, isolated from a hypersaline lake

“…Our recent study on the microbiology of reductive sulfur cycling in hypersaline habitats resulted in the discovery of a novel functional group of haloarchaea in anaerobic sediments of hypersaline lakes growing exclusively by dissimilatory elemental sulfur respiration (Sorokin et al, 2016). This metabolic type was previously unknown among the haloarchaea, but even more surprising anaerobic acetate oxidation with a low-potential electron acceptor such as elemental sulfur has not yet been demonstrated in the whole archaeal kingdom.…”

“…Next, their metabolism was extremely narrow, limited to acetate and pyruvate as electron donors/carbon source, and elemental sulfur as electron acceptor. The details of anaerobic growth kinetics have been described previously (Sorokin et al, 2016). In general, the cultures growing with acetate produced more sulfide (up to 9 mM in one month) and less biomass than the cultures grown on pyruvate.…”

“…The enrichment and isolation procedures, the medium composition and cultivation conditions have been described previously (Sorokin et al, 2016). Overall, anaerobic enrichments using acetate as electron donor/carbon source and elemental sulfur as electron acceptor at 4 M NaCl, pH 7 and 37 C resulted in isolation of four strains of haloarchaea designated HSR2 T , HSR3, HSR4 and HSR5.…”