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. 2023 May 15;12(5):723.
doi: 10.3390/biology12050723.

Prokaryotic Life Associated with Coal-Fire Gas Vents Revealed by Metagenomics

Vitaly V Kadnikov  1 , Andrey V Mardanov  1 , Alexey V Beletsky  1 , Olga V Karnachuk  2 , Nikolai V Ravin  1
Affiliations

Prokaryotic Life Associated with Coal-Fire Gas Vents Revealed by Metagenomics

Vitaly V Kadnikov et al. Biology (Basel). .

Abstract

The natural combustion of underground coal seams leads to the formation of gas, which contains molecular hydrogen and carbon monoxide. In places where hot coal gases are released to the surface, specific thermal ecosystems are formed. Here, 16S rRNA gene profiling and shotgun metagenome sequencing were employed to characterize the taxonomic diversity and genetic potential of prokaryotic communities of the near-surface ground layer near hot gas vents in an open quarry heated by a subsurface coal fire. The communities were dominated by only a few groups of spore-forming Firmicutes, namely the aerobic heterotroph Candidatus Carbobacillus altaicus, the aerobic chemolitoautotrophs Kyrpidia tusciae and Hydrogenibacillus schlegelii, and the anaerobic chemolithoautotroph Brockia lithotrophica. Genome analysis predicted that these species can obtain energy from the oxidation of hydrogen and/or carbon monoxide in coal gases. We assembled the first complete closed genome of a member of uncultured class-level division DTU015 in the phylum Firmicutes. This bacterium, 'Candidatus Fermentithermobacillus carboniphilus' Bu02, was predicted to be rod-shaped and capable of flagellar motility and sporulation. Genome analysis showed the absence of aerobic and anaerobic respiration and suggested chemoheterotrophic lifestyle with the ability to ferment peptides, amino acids, N-acetylglucosamine, and tricarboxylic acid cycle intermediates. Bu02 bacterium probably plays the role of a scavenger, performing the fermentation of organics formed by autotrophic Firmicutes supported by coal gases. A comparative genome analysis of the DTU015 division revealed that most of its members have a similar lifestyle.

Keywords: DTU015; Firmicutes; carboxydotrophy; coal gases; hydrogenotrophy; metagenome; microbial community; thermophiles.

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Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Figures

Figure 1
Figure 1
General view of the area where coal combustion occurs.
Figure 2
Figure 2
Microbial community composition revealed by 16S rRNA gene profiling.
Figure 3
Figure 3
Phylogenomic placement of the Bu02 genome in the maximum likelihood concatenated protein phylogeny of class DTU015. The level of support for internal branches was assessed using the Bayesian test in PhyML. Taxonomy is shown according to the GTDB release R207 (c, class; o, order; f, family). The genome of Thermaerobacter marianensis representing a sister class Thermaerobacteria of the candidate phylum Firmicutes_E was used to root the tree. Genomes from natural aquatic environments are marked in blue, those from anaerobic digesters and wastewater are marked in yellow, and ones from coal-fire sites are marked in grey.
Figure 4
Figure 4
An overview of metabolic pathways encoded in the Bu02 genome. Abbreviations: EMP, Embden-Meyerhof (EM) pathway; PPP, pentose-phosphate pathway; PYK, pyruvate kinase; PPDK, pyruvate phosphate dikinase; POR, pyruvate ferredoxin oxidoreductase; LDH, lactate dehydrogenase; ACS, acetyl-CoA synthetase (ADP-forming); Mae, malic enzyme; PEPCK, phosphoenolpyruvate carboxykinase; ACLY, citrate lyase; Acn, aconitase; Fum, fumarate hydratase; hyd, hydrogenase; PPase, pyrophosphatase; Fd(ox)/Fd(red), ferredoxin, oxidized and reduced form; N+, NAD(P)+; NH, NAD(P)H; CoA, coenzyme A.
Figure 5
Figure 5
Comparative genome analysis of the members of analysis of the candidate class DTU015 performed using the DRAM tool. CAZY, carbohydrate-active enzymes (the presence of enzymes capable of hydrolyzing the substrates indicated at the bottom); DNRA, cytochrome c nitrite reductase (ammonia-forming).
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