Metagenomes and metatranscriptomes shed new light on the microbial-mediated sulfur cycle in a Siberian soda lake

Abstract

Background The planetary sulfur cycle is a complex web of chemical reactions that can be microbial-mediated or can occur spontaneously in the environment, depending on the temperature and pH. Inorganic sulfur compounds can serve as energy sources for specialized prokaryotes and are important substrates for microbial growth in general. Here, we investigate dissimilatory sulfur cycling in the brine and sediments of a southwestern Siberian soda lake characterized by an extremely high pH and salinity, combining meta-omics analyses of its uniquely adapted highly diverse prokaryote communities with biogeochemical profiling to identify key microbial players and expand our understanding of sulfur cycling under haloalkaline conditions. Results Peak microbial activity was found in the top 4 cm of the sediments, a layer with a steep drop in oxygen concentration and redox potential. The majority of sulfur was present as sulfate or iron sulfide. Thiosulfate was readily oxidized by microbes in the presence of oxygen, but oxidation was partially inhibited by light. We obtained 1032 metagenome-assembled genomes, including novel population genomes of characterized colorless sulfur-oxidizing bacteria (SOB), anoxygenic purple sulfur bacteria, heterotrophic SOB, and highly active lithoautotrophic sulfate reducers. Surprisingly, we discovered the potential for nitrogen fixation in a new genus of colorless SOB, carbon fixation in a new species of phototrophic Gemmatimonadetes , and elemental sulfur/sulfite reduction in the “ Candidatus Woesearchaeota.” Polysulfide/thiosulfate and tetrathionate reductases were actively transcribed by various (facultative) anaerobes. Conclusions The recovery of over 200 genomes that encoded enzymes capable of catalyzing key reactions in the inorganic sulfur cycle indicates complete cycling between sulfate and sulfide at moderately hypersaline and extreme alkaline conditions. Our results suggest that more taxonomic groups are involved in sulfur dissimilation than previously assumed. Electronic supplementary material The online version of this article (10.1186/s12915-019-0688-7) contains supplementary material, which is available to authorized users.

Impacts ofDesulfobacteralesandChromatialeson sulfate reduction in the subtropical mangrove ecosystem as revealed by SMDB analysis

“…2C and 2D). This finding was unexpected because previous analysis of the occurrence of inorganic sulfur cycle genes in sequence genomes found that aprA occurs at higher frequencies than the other gene-encoding proteins required for dissimilatory sulfate-reduction genes (Vavourakis et al, 2019).…”

“…Furthermore, the environmental conditions that select for dissimilatory sulfate-reduction gene families for a more frequent reliance on sulfate reduction remain unclear. In addition, metagenomics and metatranscriptomics, which avoid cultivation bottleneck, can characterize uncultivated microorganisms (Vavourakis et al, 2019;Zhang et al, 2019).…”

Methylotrophy, alkane-degradation, and pigment production as defining features of the globally distributed yet-uncultured phylum Binatota

“…Site-or habitat-speci c studies focus on spatiotemporal sampling of a single site or habitat of interest. The obtained genomes are then analyzed to elucidate how resident taxa mediate substrates turnover and elemental cycling, examine microbial interactions on the metabolic and cellular levels, and document how the community responds to natural and anthropogenic changes 1,2,3,4 . Function-based studies focus on genomes from single or multiple habitats to identify and characterize organisms involved in a speci c process, e.g.…”

Abundant Taxa and Favorable Pathways in the Microbiome of Soda-Saline Lakes in Inner Mongolia

“…Soda lakes are a type of saline lake with extremely high pH and salinity due to high concentrations of carbonate/bicarbonate and many other inorganic salts (1). Under alkaline and saline conditions, microbial activities are rather high, including surprisingly high biodiversity (2)(3)(4)(5), relatively high primary productivity rates (6)(7)(8)(9)(10), vigorous oxidation and reduction reactions of sulfur (11)(12)(13)(14)(15), and elevated biochemical cycling of various compounds and elements (16)(17)(18)(19). High concentrations of inorganic ions such as (bi)carbonate and phosphate provide adequate essential elements, while some saline environments, respectively (26).…”