Genomic and Metabolic Insights into Two Novel Thiothrix Species from Enhanced Biological Phosphorus Removal Systems

Nikolai V. Ravin,Dmitry D. Smolyakov,Eugeny V. Gruzdev,Tatyana S. Rudenko,Andrey V. Mardanov,Alexey V. Beletsky,Nikolai V. Pimenov,Yulia Yu. Berestovskaya,Margarita Yu. Grabovich,Maria V. Gureeva,Nikita D. Markov

doi:10.3390/microorganisms8122030

Nikolai V. Ravin, Dmitry D. Smolyakov + Show 9 more

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https://doi.org/10.3390/microorganisms8122030

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Abstract

Two metagenome-assembled genomes (MAGs), obtained from laboratory-scale enhanced biological phosphorus removal bioreactors, were analyzed. The values of 16S rRNA gene sequence identity, average nucleotide identity, and average amino acid identity indicated that these genomes, designated as RT and SSD2, represented two novel species within the genus Thiothrix, ‘Candidatus Thiothrix moscowensis’ and ‘Candidatus Thiothrix singaporensis’. A complete set of genes for the tricarboxylic acid cycle and electron transport chain indicates a respiratory type of metabolism. A notable feature of RT and SSD2, as well as other Thiothrix species, is the presence of a flavin adenine dinucleotide (FAD)-dependent malate:quinone oxidoreductase instead of nicotinamide adenine dinucleotide (NAD)-dependent malate dehydrogenase. Both MAGs contained genes for CO2 assimilation through the Calvin–Benson–Bassam cycle; sulfide oxidation (sqr, fccAB), sulfur oxidation (rDsr complex), direct (soeABC) and indirect (aprBA, sat) sulfite oxidation, and the branched Sox pathway (SoxAXBYZ) of thiosulfate oxidation to sulfur and sulfate. All these features indicate a chemoorganoheterotrophic, chemolithoautotrophic, and chemolithoheterotrophic lifestyle. Both MAGs comprise genes for nitrate reductase and NO-reductase, while SSD2 also contains genes for nitrite reductase. The presence of polyphosphate kinase and exopolyphosphatase suggests that RT and SSD2 could accumulate and degrade polyhosphates during the oxic-anoxic growth cycle in the bioreactors, such as typical phosphate-accumulating microorganisms.

Highlights

Filamentous colorless sulfur bacteria (FCSB) have been a classic object of microbiology since the time of S.N
25 metagenome-assembled genomes (MAGs) obtained from metagenomes of natural hydrogen sulfide biotopes are currently available. Two of these genomes were attributed to certain species, T. nivea DOLJORAL78_51_81 [5,6] and T. lacustris A8 [7], and 23 others were designated as Thiothrix sp. or uncultured Thiothrix sp. [8,9,10]
To obtain MAGs of microbial community members, we sequenced the metagenome of activated sludge from of the polyphosphate accumulating organisms (PAOs) bioreactor operated at Research Center of Biotechnology (Moscow, Russia) using Illumina technique

Summary

Introduction

Filamentous colorless sulfur bacteria (FCSB) have been a classic object of microbiology since the time of S.N. The bacteria retained in the genus after the last taxonomic revision [4] include five species: T. nivea, T. fructosivorans, T. unzii, T. caldifontis and T. lacustris. Despite the fact that the genomes of T. lacustris (GCF_000621325.1), T. caldifontis (GCF_900107695.1), and T. nivea (GCF_000260135.1) are available from databases, comprehensive analysis of the main metabolic pathways of sulfur, carbon, and nitrogen has not been reported. 25 metagenome-assembled genomes (MAGs) obtained from metagenomes of natural hydrogen sulfide biotopes are currently available. Two of these genomes were attributed to certain species, T. nivea DOLJORAL78_51_81 [5,6] and T. lacustris A8 [7], and 23 others were designated as Thiothrix sp. Two of these genomes were attributed to certain species, T. nivea DOLJORAL78_51_81 [5,6] and T. lacustris A8 [7], and 23 others were designated as Thiothrix sp. or uncultured Thiothrix sp. [8,9,10]

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