Comparative Genome Analysis of the Genus Thiothrix Involving Three Novel Species, Thiothrix subterranea sp. nov. Ku-5, Thiothrix litoralis sp. nov. AS and "Candidatus Thiothrix anitrata" sp. nov. A52, Revealed the Conservation of the Pathways of Dissimilatory Sulfur Metabolism and Variations in the Genetic Inventory for Nitrogen Metabolism and Autotrophic Carbon Fixation.

Nikolai V Ravin,Margarita Y Grabovich,Olga V Karnachuk,Richard J Roberts,Alexey V Beletsky,Andrey A Novikov,Tatyana S Rudenko,Alexey Fomenkov,Andrey L Rakitin,Luo Sun,Nikita D Markov,Dmitry D Smolyakov

doi:10.3389/fmicb.2021.760289

Abstract

Two strains of filamentous, colorless sulfur bacteria were isolated from bacterial fouling in the outflow of hydrogen sulfide-containing waters from a coal mine (Thiothrix sp. Ku-5) and on the seashore of the White Sea (Thiothrix sp. AS). Metagenome-assembled genome (MAG) A52 was obtained from a sulfidic spring in the Volgograd region, Russia. Phylogenetic analysis based on the 16S rRNA gene sequences showed that all genomes represented the genus Thiothrix. Based on their average nucleotide identity and digital DNA-DNA hybridization data these new isolates and the MAG represent three species within the genus Thiothrix with the proposed names Thiothrix subterranea sp. nov. Ku-5T, Thiothrix litoralis sp. nov. AST, and “Candidatus Thiothrix anitrata” sp. nov. A52. The complete genome sequences of Thiothrix fructosivorans QT and Thiothrix unzii A1T were determined. Complete genomes of seven Thiothrix isolates, as well as two MAGs, were used for pangenome analysis. The Thiothrix core genome consisted of 1,355 genes, including ones for the glycolysis, the tricarboxylic acid cycle, the aerobic respiratory chain, and the Calvin cycle of carbon fixation. Genes for dissimilatory oxidation of reduced sulfur compounds, namely the branched SOX system (SoxAXBYZ), direct (soeABC) and indirect (aprAB, sat) pathways of sulfite oxidation, sulfur oxidation complex Dsr (dsrABEFHCEMKLJONR), sulfide oxidation systems SQR (sqrA, sqrF), and FCSD (fccAB) were found in the core genome. Genomes differ in the set of genes for dissimilatory reduction of nitrogen compounds, nitrogen fixation, and the presence of various types of RuBisCO.

Highlights

At the end of the 19th century, Sergei Winogradsky described filamentous, colorless sulfur bacteria, often present as foulings in running waters rich in hydrogen sulfide, and gave this group of microorganisms the generic name Thiothrix
In this work we describe three new species of the genus Thiothrix, Thiothrix subterranea sp. nov
The samples for metagenomic analysis, as well as for the isolation of new Thiothrix isolates were taken from microbial fouling in the place of the outflow of sulfidic water from a drained well from the closed and flooded coal mine “Severnaya” in Kemerovo region of Russia (55◦19.59 N, 84◦4.59 E), a sulfidic spring in the Volgograd region of Russia (49◦8.921 N, 44◦6.236 E) and on the shore of the White Sea, Russia at the border of the freshwater stream flowing into the sea (66◦33.17 N, 33◦5.58 E) (Figures 1A,C,D)

Summary

Introduction

At the end of the 19th century, Sergei Winogradsky described filamentous, colorless sulfur bacteria, often present as foulings in running waters rich in hydrogen sulfide, and gave this group of microorganisms the generic name Thiothrix. They can accumulate elemental sulfur in the form of intracellular inclusion bodies and are characterized by the ability to form rosettes and the presence of a pronounced mucous sheath in the filaments. Due to the flexible sulfur, nitrogen and carbon metabolism and the ability for aerobic and anaerobic growth, these bacteria can occupy various ecological niches As a rule, they dominate microbial populations in sulfide-rich waters, forming powerful bacterial fouling (Larkin and Shinabarger, 1983; Chernousova et al, 2010; Rossmassler et al, 2016)

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Conclusion