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Thermophilic Chloroflexi Dominate in the Microbial Community

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Thermophilic Chloroflexi Dominate in the Microbial Community microorganisms Article Thermophilic Chloroflexi Dominate in the Microbial Community Associated with Coal-Fire Gas Vents in the Kuznetsk Coal Basin, Russia Vitaly V. Kadnikov 1, Andrey V. Mardanov 1 , Alexey V. Beletsky 1, Mikhail A. Grigoriev 2, Olga V. Karnachuk 2 and Nikolai V. Ravin 1,* 1 Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, 119071 Moscow, Russia; [email protected] (V.V.K.); [email protected] (A.V.M.); [email protected] (A.V.B.) 2 Laboratory of Biochemistry and Molecular Biology, Tomsk State University, 634050 Tomsk, Russia; [email protected] (M.A.G.); [email protected] (O.V.K.) * Correspondence: [email protected] Abstract: Thermal ecosystems associated with areas of underground burning coal seams are rare and poorly understood in comparison with geothermal objects. We studied the microbial communities as- sociated with gas vents from the coal-fire in the mining wastes in the Kemerovo region of the Russian Federation. The temperature of the ground heated by the hot coal gases and steam coming out to the surface was 58 ◦C. Analysis of the composition of microbial communities revealed the dominance of Ktedonobacteria (the phylum Chloroflexi), known to be capable of oxidizing hydrogen and carbon monoxide. Thermophilic hydrogenotrophic Firmicutes constituted a minor part of the community. Citation: Kadnikov, V.V.; Mardanov, Among the well-known thermophiles, members of the phyla Aquificae, Deinococcus-Thermus and A.V.; Beletsky, A.V.; Grigoriev, M.A.; Karnachuk, O.V.; Ravin, N.V. Bacteroidetes were also found. In the upper ground layer, Acidobacteria, Verrucomicrobia, Acti- Thermophilic Chloroflexi Dominate nobacteria, Planctomycetes, as well as Proteobacteria of the alpha and gamma classes, typical of in the Microbial Community soils, were detected; their relative abundancies decreased with depth. The phylum Verrucomicro- Associated with Coal-Fire Gas Vents bia was dominated by Candidatus Udaeobacter, aerobic heterotrophs capable of generating energy in the Kuznetsk Coal Basin, Russia. through the oxidation of hydrogen present in the atmosphere in trace amounts. Archaea made up a Microorganisms 2021, 9, 948. https:// small part of the communities and were represented by thermophilic ammonium-oxidizers. Overall, doi.org/10.3390/microorganisms the community was dominated by bacteria, whose cultivated relatives are able to obtain energy 9050948 through the oxidation of the main components of coal gases, hydrogen and carbon monoxide, under aerobic conditions. Academic Editor: Nils-Kåre Birkeland Keywords: thermophiles; coal gases; hydrogenotrophs; microbial community; Chloroflexi; Candidatus Received: 16 March 2021 Udaeobacter Accepted: 24 April 2021 Published: 28 April 2021 Publisher’s Note: MDPI stays neutral 1. Introduction with regard to jurisdictional claims in published maps and institutional affil- Studies of thermophilic microorganisms that survive and develop at extreme tempera- iations. tures for ordinary life have expanded our understanding of the diversity of microorganisms, their evolution, and mechanisms of adaptation to extreme environmental conditions [1,2]. Most research on thermophiles has focused on thermal ecosystems associated with volcanic activity, such as hot springs and deep-sea hydrothermal vents, or biotechnologically impor- tant objects, such as high-temperature bioreactors, etc. In addition to volcanic activity, the Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. natural combustion of fossil hydrocarbons and coal can lead to the formation of thermal This article is an open access article ecological niches. The phenomena of underground burning coal seams are quite common distributed under the terms and in nature and are found in Australia, Germany, USA (Pennsylvania), China, Russia, India conditions of the Creative Commons and other countries [3]. Such underground fires can last for centuries, for example, a coal Attribution (CC BY) license (https:// seam in Dudweiler (Saar, Germany) has been burning since 1668. An example of long-term creativecommons.org/licenses/by/ natural underground coal fire is Burning Mountain in Australia [4], the burning time of 4.0/). which is estimated to be approximately 6000 years old. Microorganisms 2021, 9, 948. https://doi.org/10.3390/microorganisms9050948 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, x FOR PEER REVIEW 2 of 11 Microorganisms 2021, 9, 948 burning since 1668. An example of long-term natural underground coal fire is Burning2 of 11 Mountain in Australia [4], the burning time of which is estimated to be approximately 6000 years old. Combustion of coal under low oxygen conditions and the presence of water is ac- companiedCombustion by the of formation coal under of lowcoal oxygengases in conditions the reaction and 3 theC + presenceO2 + H2O of → water H2 + 3 is CO accom- [5]. panied by the formation of coal gases in the reaction 3 C + O + H O ! H + 3 CO [5]. Molecular hydrogen can also be formed in a water gas shift reaction:2 2 CO + H22O → CO2 + Molecular hydrogen can also be formed in a water gas shift reaction: CO + H O ! CO + H2. Underground coal fire is a natural analogue of the synthesis gas production2 process2 duringH2. Underground coal gasification. coal fire Gases is a naturalemanating analogue to the of surface the synthesis can also gas contain production light processhydro- carbons,during coal hydrogen gasification. sulfide, Gases sulfur emanating oxides, and to the other surface toxic can compounds also contain such light as hydrocar-benzene, xylene,bons, hydrogen aliphatic sulfide, and halogenated sulfur oxides, compounds and other [3,6,7]. toxic compounds Sulfur compounds such as benzene, and other xylene, ele- mentsaliphatic found and in halogenated coal seams compounds can be delivered [3,6,7]. to Sulfur the surface compounds by the and gas other stream, elements resulting found in in coal seams can be delivered to the surface by the gas stream, resulting in contamination contamination of the surrounding areas [8]. The temperature of the gas coming out to the of the surrounding areas [8]. The temperature of the gas coming out to the surface depends surface depends on the temperature at which the underground coal fire takes place and on the temperature at which the underground coal fire takes place and on the depth of the on the depth of the fire, and is usually in the range from 50 to 800 °C. fire, and is usually in the range from 50 to 800 ◦C. In areas where hot coal gases come to the surface, local extreme ecosystems charac- In areas where hot coal gases come to the surface, local extreme ecosystems character- terized by high temperatures (>50 °C) and the presence of toxic substances were formed ized by high temperatures (>50 ◦C) and the presence of toxic substances were formed [9]. [9]. Hydrogen and CO contained in coal gases can be used by microorganisms as Hydrogen and CO contained in coal gases can be used by microorganisms as high-energy high-energy substrates, which determines the possibility of the development of specific substrates, which determines the possibility of the development of specific communities of communities of thermophilic microorganisms. However, little is known about the com- thermophilic microorganisms. However, little is known about the composition of microbial position of microbial communities in such ecosystems. communities in such ecosystems. The Kuznetsk coal basin (Kemerovo region, Russia) is one of the largest in the world The Kuznetsk coal basin (Kemerovo region, Russia) is one of the largest in the [10].world Coal [10 ].mining Coal in mining this region in this began region in th begane middle in the of the middle 18th ofcentury. the 18th Initially, century. mining Ini- wastially, carried mining out was by carriedthe mine out method, by the minebut rece method,ntly many but recentlymines have many been mines closed. have At been the moment,closed. At coal the is moment, mined in coal an open is mined way, in us aning open overburden way, using operations. overburden The operations. dumps formed The afterdumps mining formed can after periodically mining canignite periodically when the incoming ignite when oxygen the incoming from the oxygensurface fromand coal the interactsurface and[11]. coal At interactpresent, [ 11in]. the At present,area of the in the city area of ofKiselevsk, the city ofa Kiselevsk,large number a large of numbersponta- neousof spontaneous fire areas firehave areas been have recorded been recordedin coal deposits. in coal deposits. The aim of this study was to uncover thethe compositioncomposition of microbialmicrobial communitiescommunities associated with anan undergroundunderground coal coal fire fire site site near near the the city city of Kiselevsk,of Kiselevsk, Kemerovo Kemerovo Region, Re- gion,Russia, Russia, using using 16S rRNA 16S rRNA gene sequencing.gene sequencing. 2. Materials Materials and and Methods Methods 2.1. Study Study Site, Site, Sampling, Sampling, and Chemical Analyses Samples were were taken at an abandoned open open coal coal pit pit near near the town of Kiselevsk, Ke- Ke- merovo Region (Figure(Figure1 ).1). At At the the moment, moment, within within the the city city limits, limits, 9 open-cut 9 open-cut coal coal mines mines are arein operation, in operation, and and all undergroundall underground mines mines are closed.are closed. At one At ofone the of quarries, the quarries, located located near nearthe Dalnie the Dalnie Gory Gory mine, mine,
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