Extremophiles Metabolism Laboratory

Evgeny N. Frolov
Ph.D. (Biology)
Head of Laboratory
INMI, room 106
Телефон +7 (499) 135-12-29 ext. 732
E-Mail
evgenii_frolov_89@mail.ru

General information

Laboratory`s main areas of expertise are diversity, physiology and evolution of extremophilic microorganisms i.e. optimally growing at high temperatures (thermophiles), low pH (acidophiles) or salinity (halophiles), including polyextremophiles, capable of growing at more than one extreme parameter. In our work we use various approaches from classical microbiology, molecular biology and biochemistry to various omics. All these allow us to study extremophiles from environmental samples to isolation and characterization of their hyperstable enzymes using both cultivation-based and cultivation-free strategies. Our main research areas are:

  1. Isolation and characterization of novel taxa of extremophilc microorganisms.
  2. Microbial ecology of extremal environments (terrestrial, shallow water and deep sea hot vents, deep subsurface biosphere, hypersaline lakes etc.).
  3. Study of uncultivated microorganisms, the so-called “microbial dark matter”, using cultivation-independent approaches (meta-omics) including “omics”-controlled cultivation.
  4. Novel metabolic pathways: novel electron acceptors, donors and donor/acceptor pairs, including insoluble compounds, novel pathways of autotrophic carbon assimilation.
  5. Energy conservation mechanisms in prokaryotes living in conditions close to the thermodynamic limits of life.
  6. Extremophilic microorganisms, capable of hydrolyzing biopolimers: insoluble proteins, insoluble and/or complex polysaccharides, lipids.
  7. Extremophilic microorganisms capable of carbon monoxide oxidation.
  8. Ectremophilic microorganisms, producing biogas and biofuels (eg. H2, ethanol, methane).
  9. Extremozymes – enzymes from extremophiles belonging to novel families, involved in novel pathways, being promising for biotechnology.

 

Publications

Selected publications:

2023

  • Frolov EN, Elcheninov AG, Gololobova AV, Toshchakov SV, Novikov AA, Lebedinsky AV, Kublanov IV. Obligate autotrophy at the thermodynamic limit of life in a new acetogenic bacterium. Front Microbiol. 2023 May 12;14:1185739. doi: 10.3389/fmicb.2023.1185739.
  • Elcheninov AG, Ugolkov YA, Elizarov IM, Klyukina AA, Kublanov IV, Sorokin DY. Cellulose metabolism in halo(natrono)archaea: a comparative genomics study. Front Microbiol. 2023 Jun 1;14:1112247. doi: 10.3389/fmicb.2023.1112247.
  • Zavarzina DG, Merkel AY, Klyukina AA, Elizarov IM, Pikhtereva VA, Rusakov VS, Chistyakova NI, Ziganshin RH, Maslov AA, Gavrilov SN. Iron or sulfur respiration-an adaptive choice determining the fitness of a natronophilic bacterium Dethiobacter alkaliphilus in geochemically contrasting environments. Front Microbiol. 2023 Jul 14;14:1108245. doi: 10.3389/fmicb.2023.1108245.
  • Frolov EN, Lebedinsky AV, Elcheninov AG, Kublanov IV. Taxonomic proposal for a deep branching bacterial phylogenetic lineage: transfer of the family Thermodesulfobiaceae to Thermodesulfobiales ord. nov., Thermodesulfobiia classis nov. and Thermodesulfobiota phyl. nov. Syst Appl Microbiol. 2023 Jan;46(1):126388. doi: 10.1016/j.syapm.2022.126388.
  • Podosokorskaya OA, Elcheninov AG, Novikov AA, Merkel AY, Kublanov IV. Fontisphaera persica gen. nov., sp. nov., a thermophilic hydrolytic bacterium from a hot spring of Baikal lake region, and proposal of Fontisphaeraceae fam. nov., and Limisphaeraceae fam. nov. within the Limisphaerales ord. nov. (Verrucomicrobiota). Syst Appl Microbiol. 2023 Jul;46(4):126438. doi: 10.1016/j.syapm.2023.126438.
  • Podosokorskaya OA, Elcheninov AG, Gavrilov SN, Petrova NF, Klyukina AA, Zavarzina DG, Merkel AY. New Representatives of the Class Ignavibacteria Inhabiting Subsurface Aquifers of Yessentuki Mineral Water Deposit. Water. 2023; 15(19):3451. https://doi.org/10.3390/w15193451.
  • Maltseva AI, Klyukina AA, Elcheninov AG, Pimenov NV, Rusanov II, Kublanov IV, Kochetkova TV, Frolov EN. Water and Sediments of an Acidic Hot Spring—Distinct Differentiation with Regard to the Microbial Community Composition and Functions. Water. 2023; 15(19):3415. https://doi.org/10.3390/w15193415.
  • Kochetkova TV, Grabarnik IP, Klyukina AA, Zayulina KS, Gavirova LA, Shcherbakova PA, Kachmazov GS, Shestakov AI, Kublanov IV, Elcheninov AG. The Bacterial Microbiota of Artisanal Cheeses from the Northern Caucasus. Fermentation. 2023; 9(8):719. https://doi.org/10.3390/fermentation9080719.
  • Elcheninov AG, Zayulina KS, Klyukina AA, Kremneva MK, Kublanov IV, Kochetkova TV. Metagenomic Insights into the Taxonomic and Functional Features of Traditional Fermented Milk Products from Russia. Microorganisms. 2024; 12(1):16. https://doi.org/10.3390/microorganisms12010016.

 

2022

  • Podosokorskaya OA, Elcheninov AG, Novikov AA, Kublanov IV. Fontivita pretiosa gen. nov., sp. nov., a thermophilic planctomycete of the order Tepidisphaerales from a hot spring of Baikal lake region. Syst Appl Microbiol. 2022 Nov;45(6):126375. doi: 10.1016/j.syapm.2022.126375.
  • Khomyakova MA, Zavarzina DG, Merkel AY, Klyukina AA, Pikhtereva VA, Gavrilov SN, Slobodkin AI. The first cultivated representatives of the actinobacterial lineage OPB41 isolated from subsurface environments constitute a novel order Anaerosomatales. Front Microbiol. 2022 Nov 10;13:1047580. doi: 10.3389/fmicb.2022.1047580.
  • Shulga N, Abramov S, Klyukina A, Ryazantsev K, Gavrilov S. Fast-growing Arctic Fe-Mn deposits from the Kara Sea as the refuges for cosmopolitan marine microorganisms. Sci Rep. 2022 Dec 20;12(1):21967. doi: 10.1038/s41598-022-23449-6.
  • Kochetkova, T.V., Podosokorskaya, O.A., Elcheninov, A.G. et al. Diversity of Thermophilic Prokaryotes Inhabiting Russian Natural Hot Springs. Microbiology. 2022 91:1–27. doi: 10.1134/S0026261722010064.
  • Gavrilov, S.N., Potapov, E.G., Prokof’eva, M.I. et al. Diversity of Novel Uncultured Prokaryotes in Microbial Communities of the Yessentukskoye Underground Mineral Water Deposit. Microbiology. 2022 91:28–44. doi: 10.1134/S0026261722010039.
  • Kochetkova TV, Grabarnik IP, Klyukina AA, Zayulina KS, Elizarov IM, Shestakova OO, Gavirova LA, Malysheva AD, Shcherbakova PA, Barkhutova DD, Karnachuk OV, Shestakov AI, Elcheninov AG, Kublanov IV. Microbial Communities of Artisanal Fermented Milk Products from Russia. Microorganisms. 2022 Oct 29;10(11):2140. doi: 10.3390/microorganisms10112140.

2021

  • Gavrilov S.N., Zavarzina D.G., Elizarov I.M., Tikhonova T.V., Dergousova N.I., Popov V.O., Lloyd J.R., Knight D., El-Naggar M.Y., Pirbadian S., Leung K.M., Robb F.T., Zakhartsev M.V., Bretschger O., Bonch-Osmolovskaya E.A. Novel Extracellular Electron Transfer Channels in a Gram-Positive Thermophilic Bacterium. Front Microbiol. 2021 11:597818. doi: 10.3389/fmicb.2020.597818.
  • Elcheninov AG, Podosokorskaya OA, Kovaleva OL, Novikov AA, Toshchakov SV, Bonch-Osmolovskaya EA, Kublanov IV. Thermogemmata fonticola gen. nov., sp. nov., the first thermophilic planctomycete of the order Gemmatales from a Kamchatka hot spring. Syst Appl Microbiol. 2021 Jan;44(1):126157. doi: 10.1016/j.syapm.2020.126157.
  • Zayulina, Kseniya S; Elcheninov, Alexander G; Toshchakov, Stepan V; Kochetkova, Tatiana V; Novikov, Andrei A; Blamey, Jenny M; Kublanov, Ilya V; Novel hyperthermophilic crenarchaeon Infirmifilum lucidum gen. nov. sp. nov., reclassification of Thermofilum uzonense as Infirmifilum uzonense comb. nov. and assignment of the family Thermofilaceae to the order Thermofilales ord. nov. Systematic and applied microbiology, 2021, 44, 4, 126230.
  • Frolov EN, Gololobova AV, Klyukina AA, Bonch-Osmolovskaya EA, Pimenov NV, Chernyh NA, Merkel AY. Diversity and Activity of Sulfate-Reducing Prokaryotes in Kamchatka Hot Springs. Microorganisms. 2021 Oct 1;9(10):2072. doi: 10.3390/microorganisms9102072.
  • Karaseva, A.I., Elcheninov, A.G., Perevalova, A.A. et al. Fervidicoccus fontis Strain 3639Fd, the First Crenarchaeon Capable of Growth on Lipids. Microbiology 2021 90:435–442. doi: 10.1134/S002626172104007X

 

2020 and earlier:

  • Zavarzina DG, Gavrilov SN, Chistyakova NI, Antonova AV, Gracheva MA, Merkel AY, Perevalova AA, Chernov MS, Zhilina TN, Bychkov AY, Bonch-Osmolovskaya EA. Syntrophic growth of alkaliphilic anaerobes controlled by ferric and ferrous minerals transformation coupled to acetogenesis. ISME J. 2020 Feb;14(2):425-436. doi: 10.1038/s41396-019-0527-4.
  • Chernyh NA, Neukirchen S, Frolov EN, Sousa FL, Miroshnichenko ML, Merkel AY, Pimenov NV, Sorokin DY, Ciordia S, Mena MC, Ferrer M, Golyshin PN, Lebedinsky AV, Cardoso Pereira IA, Bonch-Osmolovskaya EA. Dissimilatory sulfate reduction in the archaeon ‘Candidatus Vulcanisaeta moutnovskia’ sheds light on the evolution of sulfur metabolism. Nat Microbiol. 2020 Nov;5(11):1428-1438. doi: 10.1038/s41564-020-0776-z.
  • Kochetkova TV, Mardanov AV, Sokolova TG, Bonch-Osmolovskaya EA, Kublanov IV, Kevbrin VV, Beletsky AV, Ravin NV, Lebedinsky AV. The first crenarchaeon capable of growth by anaerobic carbon monoxide oxidation coupled with H2 production. Syst Appl Microbiol. 2020 Mar;43(2):126064. doi: 10.1016/j.syapm.2020.126064.
  • Podosokorskaya OA, Kochetkova TV, Novikov AA, Toshchakov SV, Elcheninov AG, Kublanov IV. Tenuifilum thalassicum gen. nov., sp. nov., a novel moderate thermophilic anaerobic bacterium from a Kunashir Island shallow hot spring representing a new family Tenuifilaceae fam. nov. in the class Bacteroidia. Syst Appl Microbiol. 2020 Sep;43(5):126126. doi: 10.1016/j.syapm.2020.126126.
  • Kochetkova TV, Zayulina KS, Zhigarkov VS, Minaev NV, Chichkov BN, Novikov AA, Toshchakov SV, Elcheninov AG, Kublanov IV. Tepidiforma bonchosmolovskayae gen. nov., sp. nov., a moderately thermophilic Chloroflexi bacterium from a Chukotka hot spring (Arctic, Russia), representing a novel class, Tepidiformia, which includes the previously uncultivated lineage OLB14. Int J Syst Evol Microbiol. 2020 Feb;70(2):1192-1202. doi: 10.1099/ijsem.0.003902.
  • Zayulina KS, Kochetkova TV, Piunova UE, Ziganshin RH, Podosokorskaya OA., Kublanov IV. Novel Hyperthermophilic Crenarchaeon Thermofilum adornatum sp. nov. Uses GH1, GH3, and Two Novel Glycosidases for Cellulose Hydrolysis. Front. microbiol. 2020. 10, 2972.
  • Kochetkova, T.V.; Toshchakov, S.V.; Zayulina, K.S.; Elcheninov, A.G.; Zavarzina, D.G.; Lavrushin, V.Y.; Bonch-Osmolovskaya, E.A.; Kublanov, I.V. Hot in Cold: Microbial Life in the Hottest Springs in Permafrost. Microorganisms 2020, 8, 1308.
  • Zavarzina D.G., Kochetkova T.V., Chistyakova N.I., Gracheva M.A., Antonova A.V., Merkel A.Y., Perevalova A.A., Chernov M.S., Koksharov Y.A., Bonch-Osmolovskaya E.A., Gavrilov S.N., Bychkov A.Y. Siderite-based anaerobic iron cycle driven by autotrophic thermophilic microbial consortium. Sci Rep. 2020 10(1):21661. doi: 10.1038/s41598-020-78605-7.
  • Frolov EN, Kublanov IV, Toshchakov SV, Lunev EA, Pimenov NV, Bonch-Osmolovskaya EA, Lebedinsky AV, Chernyh NA. Form III RubisCO-mediated transaldolase variant of the Calvin cycle in a chemolithoautotrophic bacterium. Proc Natl Acad Sci U S A. 2019 Sep 10;116(37):18638-18646. doi: 10.1073/pnas.1904225116.
  • Gavrilov SN, Korzhenkov AA, Kublanov IV, Bargiela R, Zamana LV, Popova AA, Toshchakov SV, Golyshin PN, Golyshina OV. Microbial Communities of Polymetallic Deposits’ Acidic Ecosystems of Continental Climatic Zone With High Temperature Contrasts. Front Microbiol. 2019 Jul 17;10:1573. doi: 10.3389/fmicb.2019.01573.
  • Toshchakov SV, Lebedinsky AV, Sokolova TG, Zavarzina DG, Korzhenkov AA, Teplyuk AV, Chistyakova NI, Rusakov VS, Bonch-Osmolovskaya EA, Kublanov IV, Gavrilov SN. Genomic Insights Into Energy Metabolism of Carboxydocella thermautotrophicaCoupling Hydrogenogenic CO Oxidation With the Reduction of Fe(III) Minerals. Front Microbiol. 2018 Aug 3;9:1759. doi: 10.3389/fmicb.2018.01759.
  • Frolov EN, Zayulina KS, Kopitsyn DS, Kublanov IV, Bonch-Osmolovskaya EA, Chernyh NA. Desulfothermobacter acidiphilus gen. nov., sp. nov., a thermoacidophilic sulfate-reducing bacterium isolated from a terrestrial hot spring. Int J Syst Evol Microbiol. 2018 Mar;68(3):871-875. doi: 10.1099/ijsem.0.002599.
  • Kublanov IV, Sigalova OM, Gavrilov SN, Lebedinsky AV, Rinke C, Kovaleva O, Chernyh NA, Ivanova N, Daum C, Reddy TB, Klenk HP, Spring S, Göker M, Reva ON, Miroshnichenko ML, Kyrpides NC, Woyke T, Gelfand MS, Bonch-Osmolovskaya EA. Genomic Analysis of Caldithrix abyssi, the Thermophilic Anaerobic Bacterium of the Novel Bacterial Phylum Calditrichaeota. Front Microbiol. 2017 Feb 20;8:195. doi: 10.3389/fmicb.2017.00195.
  • Kompantseva EI, Kublanov IV, Perevalova AA, Chernyh NA, Toshchakov SV, Litti YV, Antipov AN, Bonch-Osmolovskaya EA, Miroshnichenko ML. Calorithrix insularis gen. nov., sp. nov., a novel representative of the phylum Calditrichaeota. Int J Syst Evol Microbiol. 2017 May;67(5):1486-1490. doi: 10.1099/ijsem.0.001744.
  • Frolov EN, Kublanov IV, Toshchakov SV, Samarov NI, Novikov AA, Lebedinsky AV, Bonch-Osmolovskaya EA, Chernyh NA. Thermodesulfobium acidiphilum sp. nov., a thermoacidophilic, sulfate-reducing, chemoautotrophic bacterium from a thermal site. Int J Syst Evol Microbiol. 2017 May;67(5):1482-1485. doi: 10.1099/ijsem.0.001745.
  • Gavrilov S, Podosokorskaya O, Alexeev D, Merkel A, Khomyakova M, Muntyan M, Altukhov I, Butenko I, Bonch-Osmolovskaya E, Govorun V, Kublanov I. Respiratory Pathways Reconstructed by Multi-Omics Analysis in Melioribacter roseus, Residing in a Deep Thermal Aquifer of the West-Siberian Megabasin. Front Microbiol. 2017 Jun 30;8:1228. doi: 10.3389/fmicb.2017.01228.
  • Elcheninov AG, Menzel P, Gudbergsdottir SR, Slesarev AI, Kadnikov VV, Krogh A, Bonch-Osmolovskaya EA, Peng X, Kublanov IV. Sugar Metabolism of the First Thermophilic Planctomycete Thermogutta terrifontis: Comparative Genomic and Transcriptomic Approaches. Front Microbiol. 2017 Nov 2;8:2140. doi: 10.3389/fmicb.2017.02140.
  • Gavrilov SN, Stracke C, Jensen K, Menzel P, Kallnik V, Slesarev A, Sokolova T, Zayulina K, Bräsen C, Bonch-Osmolovskaya EA, Peng X, Kublanov IV, Siebers B. Isolation and Characterization of the First Xylanolytic Hyperthermophilic Euryarchaeon Thermococcus sp. Strain 2319×1 and Its Unusual Multidomain Glycosidase. Front Microbiol. 2016 May 3;7:552. doi: 10.3389/fmicb.2016.00552
  • Zavarzina D.G., Chistyakova N.I., Shapkin A.V., Savenko A.V., Zhilina T.N., Kevbrin V.V., Alekseeva T.V., Mardanov A.V., Gavrilov S.N., Bychkov A.Yu. 2016. Oxidative biotransformation of biotite and glauconite by alkaliphilic anaerobes: The effect of Fe oxidation on the weathering of phyllosilicates. Chem. Geol. 439:98-109.
  • Frank YA, Kadnikov VV, Gavrilov SN, Banks D, Gerasimchuk AL, Podosokorskaya OA, Merkel AY, Chernyh NA, Mardanov AV, Ravin NV, Karnachuk OV, Bonch-Osmolovskaya EA. Stable and Variable Parts of Microbial Community in Siberian Deep Subsurface Thermal Aquifer System Revealed in a Long-Term Monitoring Study. Front Microbiol. 2016 Dec 27;7:2101. doi: 10.3389/fmicb.2016.02101.
  • Sorokin DY, Toshchakov SV, Kolganova TV, Kublanov IV. Halo(natrono)archaea isolated from hypersaline lakes utilize cellulose and chitin as growth substrates. Front Microbiol. 2015 Sep 15;6:942. doi: 10.3389/fmicb.2015.00942.
  • Podosokorskaya OA, Bonch-Osmolovskaya EA, Beskorovaynyy AV, Toshchakov SV, Kolganova TV, Kublanov IV. Mobilitalea sibirica gen. nov., sp. nov., a halotolerant polysaccharide-degrading bacterium. Int J Syst Evol Microbiol. 2014 Aug;64(Pt 8):2657-2661. doi: 10.1099/ijs.0.057109-0.
  • Podosokorskaya OA, Kadnikov VV, Gavrilov SN, Mardanov AV, Merkel AY, Karnachuk OV, Ravin NV, Bonch-Osmolovskaya EA, Kublanov IV. Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae. Environ Microbiol. 2013 Jun;15(6):1759-71. doi: 10.1111/1462-2920.12067.
  • Lebedinsky AV, Mardanov AV, Kublanov IV, Gumerov VM, Beletsky AV, Perevalova AA, Bidzhieva SKh, Bonch-Osmolovskaya EA, Skryabin KG, Ravin NV. Analysis of the complete genome of Fervidococcus fontis confirms the distinct phylogenetic position of the order Fervidicoccales and suggests its environmental function. Extremophiles. 2014 Mar;18(2):295-309. doi: 10.1007/s00792-013-0616-7.
  • Podosokorskaya OA, Bonch-Osmolovskaya EA, Novikov AA, Kolganova TV, Kublanov IV. Ornatilinea apprima gen. nov., sp. nov., a cellulolytic representative of the class Anaerolineae. Int J Syst Evol Microbiol. 2013 Jan;63(Pt 1):86-92. doi: 10.1099/ijs.0.041012-0.
  • Kim YJ, Lee HS, Kim ES, Bae SS, Lim JK, Matsumi R, Lebedinsky AV, Sokolova TG, Kozhevnikova DA, Cha SS, Kim SJ, Kwon KK, Imanaka T, Atomi H, Bonch-Osmolovskaya EA, Lee JH, Kang SG. Formate-driven growth coupled with H(2) production. Nature. 2010 Sep 16;467(7313):352-5. doi: 10.1038/nature09375.

International cooperation

We have many national and international collaborations with various Universities, Institutes and other organizations, among which are:

  • Lomonosov Moscow State University, Russia
  • Institute of General and Experimental Biology SB RAS, Ulan-Ude, Russia
  • Tomsk State University
  • Immanuel Kant Baltic Federal University, Kaliningrad, Russia
  • Gubkin Russian State University of Oil and Gas, Moscow, Russia
  • University of Duisburg-Essen, Germany
  • University of Alberta, Canada
  • Institute for Marine Coastal Environments, CNR, Italy
  • University of the Free State, Bloemfontein, South Africa
  • INRA, Nantes, France
  • University of Exeter, UK
  • University of Münster, Germany
  • Universidad de Santiago de Chile, Chile
  • IFREMER, Brest, France

 

The following international projects are (were) conducted:

Funding organization Acronym Project Time period Participant Web-page of the project
1 FP7 Hotzyme Systematic screening for novel hydrolases from hot environments 2011-2014 10 Universities and Institutions, 1 SEM and 2 companies: Novozymes and Sigma-Aldrich https://www.exeter.ac.uk
/media/universityofexeter

/schoolofbiosciences

/biocatalysiscentre
/documents
/Hotzyme_poster_official.pdf
2 The ERA.Net RUS Thermogene Novel thermostable enzymes for industrial biotechnology 2013-2016 Great Britain, Germany, Norway,
Russia
https://www.era-learn.eu/ network-information/networks/ era-ib-2/3rd-era-ib-joint-call/novel-thermostable-enzymes-for-industrial-biotechnology
3 The Ministry of Education and Science of the Russian Federation Hotsolute Thermophilic bacterial and archaeal chassis for extremolyte production 2017-2021 UK,
Germany,
Italy,
South Africa,
Russia
http://hotsolute.com/
4 Russian Science Foundation ExploCarb Exploration of carbohydrate metabolism in hyperthermophilic archaea: novel approaches, enzymes and metabolic pathways 2018-2020 Germany,
Russia
5 Russian Foundation for Basic Research EXPATH Exploring the diversity of pathways of autotrophic carbon assimilation in thermophilic prokaryotes 2020-2022 Germany,

Russia,

6 Russian Foundation for Basic Research Discovery of novel thermostable hydrolases from archaea of the Kuril-Kamchatka Region 2021-2022 UK,
Russia