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

Vavourakis, Charlotte D.; Mehrshad, Maliheh; Balkema, Cherel; Van Hall, Rutger; Andrei, Adrian Ştefan; Ghai, Rohit; Sorokin, Dimitry Y.; Muyzer, Gerard

doi:10.1186/s12915-019-0688-7

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

Title

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

Author

Vavourakis, Charlotte D. (Universiteit van Amsterdam)
Mehrshad, Maliheh (Czech Academy of Sciences and Arts)
Balkema, Cherel (Universiteit van Amsterdam)
Van Hall, Rutger (Universiteit van Amsterdam)
Andrei, Adrian Ştefan (Czech Academy of Sciences and Arts)
Ghai, Rohit (Czech Academy of Sciences and Arts)
Sorokin, Dimitry Y. (TU Delft BT/Environmental Biotechnology; Russian Academy of Sciences)
Muyzer, Gerard (Universiteit van Amsterdam)

Date

2019

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.

Subject

Gemmatimonadetes
Haloalkaliphiles
Metagenomics
Metatranscriptomics
Nitrogen fixation
Polysulfide
Soda lake
Tetrathionate
Thiosulfate
Woesearchaeota