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Acidobacteria in Fens: Phylogenetic Diversity and Genome Analysis of the Key Representatives

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Abstract—

Acidobacteriota are one of the major prokaryotic groups in soils and peatlands. They are especially abundant in acidic peat bogs, where representatives of the well-characterized class Acidobacteriia predominate. The diversity and metabolic potential of Acidobacteriota inhabiting fens with neutral pH have been studied less thoroughly. We analyzed the composition of acidobacterial communities in four peat bogs and six fens of the Vologda region. The Acidobacteriota-affiliated 16S rRNA gene sequences comprised 30–42 and 7–22% of all reads retrieved from the peat bogs and fens, respectively. The acidobacteria of peat bogs were represented by the orders Acidobacteriales and Bryobacterales of the class Acidobacteriia, while the classes Vicinamibacteria and Blastocat•ellia predominated in fens. Genomes of four uncultured bacteria of Blastocatellia (family Pyrinomonadaceae, two genomes), Vicinamibacteria (family UBA2999), and Thermoanaerobaculia (order UBA5066) were assembled from the metagenomes of peat fens. Genome analysis revealed key pathways of aerobic heterotrophic metabolism in all four microorganisms, including the Embden–Meyerhof pathway, gluconeogenesis, the non-oxidative stage of the pentose phosphate pathway, the tricarboxylic acid cycle, and the electron transport chain of aerobic respiration, including terminal cytochrome c oxidases. All genomes encoded molybdopterin oxidoreductases of the CISM family and multiheme cytochromes c, indicating the possibility of dissimilatory reduction of sulfur compounds and Fe(III) under anaerobic conditions. Probable growth substrates may be amino acids, peptides, and fatty acids. Members of the Pyrinomonadaceae can also use various carbohydrates, including polysaccharides, and are likely involved in the degradation of various biopolymers in peat bogs. Members of Thermoanaerobaculia and Vicinamibacteria lacked the genes for secreted glycosyl hydrolases and probably could only use a limited range of simple sugars. The genome of a bacterium of the class Vicinamibacteria contained a set of genes encoding bacterial microcompartments (metabolosomes) that have not previously been described in acidobacteria and are probably involved in the metabolism of L-rhamnose.

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Funding

The study was supported by the Russian Foundation for Basic Research (grant no. 19-29-05059) and by the Ministry of Science and Higher Education of the Russian Federation (agreement 075-15-2022-318 from April 20, 2022 for the support of a world-class scientific center “Agrotechnologies for the Future” and research topic 122041100029-2).

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Authors and Affiliations

  1. Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, 119071, Moscow, Russia

    S. N. Dedysh & A. A. Ivanova

  2. Skryabin Institute of Bioengineering, Research Center of Biotechnology, Russian Academy of Sciences, 119071, Moscow, Russia

    Sh. A. Begmatov, A. V. Beletsky, A. L. Rakitin, A. V. Mardanov & N. V. Ravin

  3. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, 152742, Borok, Russia

    D. A. Philippov

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  1. S. N. Dedysh
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  2. A. A. Ivanova
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  3. Sh. A. Begmatov
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  4. A. V. Beletsky
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  5. A. L. Rakitin
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  6. A. V. Mardanov
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  7. D. A. Philippov
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  8. N. V. Ravin
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Contributions

The idea of the study was proposed by S.N. Dedysh. Peat sampling and sample description were made by D.A. Philippov. The molecular profiling of prokaryotic communities in peat samples was performed by A.L. Rakitin and A.V. Mardanov. The diversity of acidobacteria was analyzed by A.A. Ivanova. The assembly and analysis of metagenomes were performed by Sh.A. Begmatov, A.V. Beletsky, and N.V. Ravin. The text of the article was written by S.N. Dedysh and N.V. Ravin. All authors took part in discussion of the results.

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Correspondence to N. V. Ravin.

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Dedysh, S.N., Ivanova, A.A., Begmatov, S.A. et al. Acidobacteria in Fens: Phylogenetic Diversity and Genome Analysis of the Key Representatives. Microbiology 91, 662–670 (2022). https://doi.org/10.1134/S0026261722601440

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