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.



Selected publications:

  • Klaus T., Ninck S., Albersmeier A., Busche T., Wibberg D., Jiang J., Elcheninov A.G., Zayulina K., Kaschani F., Braesen C., Overkleeft H.S., Kalinowski J., Kublanov I.V., Kaiser M., Siebers B. Activity-based protein profiling for the identification of novel CAZymes involved in xylan degradation in the hyperthermophilic Euryarchaeon Thermococcus sp. strain 2319x1E, Front. microbiol. 2021, 3868.
  • 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.
  • 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.
  • 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 E. N., Kublanov I. V., Toshchakov S. V., Lunev E. A., Pimenov N. V., Bonch-Osmolovskaya E. A., Lebedinsky A. V., Chernyh N. A. Form III RubisCO-mediated transaldolase variant of the Calvin cycle in a chemolithoatotrophic bacterium. PNAS. 2019. 116 (37), 18638-18646.
  • Aleksei A Korzhenkov, Stepan V Toshchakov, Rafael Bargiela, Huw Gibbard, Manuel Ferrer, Alina V Teplyuk, David L Jones, Ilya V Kublanov, Peter N Golyshin, Olga V Golyshina. Archaea dominate the microbial community in an ecosystem with low-to-moderate temperature and extreme acidity. 2019. Microbiome, volume 7. doi:10.1186/s40168-019-0623-8
  • Camilla L. Nesbø, Rhianna Charchuk, Stephen M. J. Pollo, Karen Budwill, Ilya V. Kublanov, Thomas H. A. Haverkamp, Julia Foght. Genomic analysis of the mesophilic Thermotogae genus Mesotoga reveals phylogeographic structure and genomic determinants of its distinct metabolism. 2019. Environmental Microbiology, Volume 21, pp 456-470. doi:10.1111/1462-2920.14477
  • Dimitry Y. Sorokin, Maria S. Muntyan, Stepan V. Toshchakov, Aleksei Korzhenkov, and Ilya V. Kublanov. Phenotypic and genomic properties of a novel deep-lineage haloalkaliphilic member of the phylum Balneolaeota from soda lakes possessing Na+-translocating proteorhodopsi. Frontiers in microbiolog. 2018. doi:10.3389/fmicb.2018.02672
  • Wohlgemuth R., J. Littlechild, D. Monti, K. Schnorr, T. van Rossum, B. Siebers, P. Menzel, I. V. Kublanov, A. G. Rike, G. Skretas, Z. Szabo, X. Peng, M. J. Young. Discovering novel hydrolases from hot environments. Biotechnology Advances. 2018. doi: 10.1016/j.biotechadv.2018.09.004
  • Kublanov I.V., Sigalova O.M., Gavrilov S.N., Lebedinsky A.V., Rinke C., Kovaleva O., Chernyh N.A., Ivanova N., Daum C., Reddy T.B.K., Klenk H.-P., Spring S., Göker M., Reva O.N., Miroshnichenko M.L., Kyrpides N.C., Woyke T., Gelfand M.S., Bonch-Osmolovskaya E.A. Genomic analysis of Caldithrix abyssi, the thermophilic anaerobic bacterium of the novel bacterial phylum Calditrichaeota. Frontiers Microbiol. 2017. 8:195.
  • Sorokin D, Messina E, Smedile F, Roman P, Sinninghe-Damste J, Golyshin P, Ciordia S, Mena M, Ferrer M, Kublanov I, Samarov N, Toshchakov S., La Cono V and Yakimov M. Discovery of anaerobic lithoheterotrophic haloarchaea, ubiquitous in hypersaline habitats. ISME J. 2017. 11. 1245-1260.
  • Golyshina OV, Toshchakov SV, Makarova KS, Gavrilov SN, Korzhenkov AA, La Cono V, Arcadi E, Nechitaylo TY, Ferrer M, Kublanov IV, Wolf YI, Yakimov MM, Golyshin PN. ‘ARMAN’ archaea depend on association with euryarchaeal host in culture and in situ. Nat Commun. 2017. 8(1): 60.
  • Gavrilov SN, O.A. Podosokorskaya, D.G. Alexeev, A.Y. Merkel, M.A. Khomyakova, M.S. Muntyan, I.A. Altukhov, I.O. Butenko, E.A. Bonch-Osmolovskaya, V. M. Govorun, I.V. Kublanov. Respiratory Pathways Reconstructed by Multi-Omics Analysis in Melioribacter roseus, Residing in a Deep Thermal Aquifer of the West-Siberian Megabasin. Front Microbiol. 2017. 8: 1228.
  • Elcheninov A.G., Menzel P., Gudbergsdottir S.R., Slesarev A.I., Kadnikov V.V., Krogh A., Bonch-Osmolovskaya E.A., Peng X. and Kublanov I.V. Sugar metabolism of the first thermophilic planctomycete Thermogutta terrifontis: comparative genomic and transcriptomic approaches. Front. Microbiol. 2017. 8. 2140. doi: 10.3389/fmicb.2017.02140
  • Gavrilov S. N., Stracke C., Jensen K., Menzel P., Kallnik V., Slesarev A., Sokolova T., Zayulina K., Brasen C., Bonch-Osmolovskaya E. A., Peng X., Kublanov I. V., Siebers B. 2016. Isolation and characterization of the first xylanolytic hyperthermophilic euryarchaeon Thermococcus sp. strain 2319×1 and its unusual multidomain glycosidase. Front Microbiol. 7, 552.
  • 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.
  • Zarafeta D., Moschidi D., Ladoukakis E., Gavrilov S., Chrysina E., Chatziioannou A., Kublanov I., Skretas G., Kolisis F.N. Metagenomic mining for thermostable esterolytic enzymes uncovers a new family of bacterial esterases. Sci. Reports. 2016 In press.
  • Sorokin D., Messina E., Smedile F., Roman P., Sinninghe-Damste J., Golyshin P., Ciordia S., Mena M., Ferrer M., Kublanov I., Samarov N., Toshchakov S., La Cono V. and Yakimov M.. Discovery of anaerobic lithoheterotrophic haloarchaea, ubiquitous in hypersaline habitats. ISME J. 2016. In press.
  • Sorokin D., Kublanov I., Gavrilov S., Rojo D., Roman P., Golyshin P., Slepak V., Smedile F., Messina E., La Cono V., Ferrer M. and Yakimov M. Elemental sulfur and acetate can support life of a novel strictly anaerobic haloarchaeon. ISME J. 2016. 10. 240-252. doi:10.1038/ismej.2015.79.
  • Golyshina O., Kublanov I.V., Hai T., Korzhenkov A., Lunsdorf H., Nechitaylo T., Gavrilov S., Toshchakov S., Golyshin P.N. Biology of archaea from a novel family Cuniculiplasmataceae (Thermoplasmata) ubiquitous in hyperacidic environments. Sci. Reports. 2016. 6: 39034. doi:10.1038/srep39034.
  • Sorokin D.Y., Toshchakov S.V., Kolganova T.V., Kublanov I.V. 2015. Halo(natrono)archaea isolated from hypersaline lakes utilize cellulose and chitin as growth substrates. Frontiers Microbiol. 6: 942.
  • Placido A., Hai T. , Ferrer M., Chernikova T.N., Distaso M., Armstrong D., Yakunin A.F., Toshchakov S.V., Yakimov M.M., Kublanov I.V., Golyshina O.V., Pesole G., Ceci L.R., Golyshin P.N. 2015. Diversity of hydrolases from hydrothermal vent sediments of the Levante Bay, Vulcano Island (Aeolian archipelago) identified by activity-based metagenomics and biochemical characterization of new esterases and an arabinopyranosidase. Appl Microbiol Biotechnol. 99(23): 10031-10046.
  • Menzel P, Gudbergsdottir SR, Rike AG, Lin L, Zhang Q, Contursi P, Moracci M, Kristjansson JK, Bolduc B, Gavrilov S, Ravin N, Mardanov A, Bonch-Osmolovskaya E, Young M, Krogh A, Peng X. 2015. Comparative Metagenomics of Eight Geographically Remote Terrestrial Hot Springs. Microb Ecol. 70(2):411-24. doi:10.1007/s00248-015-0576-9.
  • Sant’Anna FH, Lebedinsky AV, Sokolova TG, Robb FT, Gonzalez JM. Analysis of three genomes within the thermophilic bacterial species Caldanaerobacter subterraneus with a focus on carbon monoxide dehydrogenase evolution and hydrolase diversity. BMC Genomics. 2015. 16:757.
  • Nesbo CL, Swithers K, Dahle H, Haverkamp THA, Birkeland N-K, Sokolova T, Kublanov I, Zhaxybayeva O. Evidence for extensive gene flow and Thermotoga subpopulations in subsurface and marine environments. ISME J. 2014. V. 9. P. 1532-1542. doi:10.1038/ismej.2014.238.
  • Podosokorskaya O.A., Kadnikov V.V., Gavrilov S.N., Mardanov A.V., Merkel A.Y., Karnachuk O.V., Ravin N.V., Bonch-Osmolovskaya E.A., and Kublanov I.V.. 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. 15. 1759-1771. http://onlinelibrary.wiley.com/doi/10.1111/1462-2920.12067/abstract
  • Podosokorskaya O.A., Bonch-Osmolovskaya E.A., Novikov A.A., Kolganova T.V., Kublanov I.V. Ornatilinea apprima gen. nov., sp. nov., a first cellulolytic representative of class Anaerolineae. Int. J. Syst. Evol. Microbiol. 2013. 63: 86-92.
  • Kim Y.J., Lee H.S., Kim E.S., Bae S.S., Lim J.K., Matsumi R., Lebedinsky A.V., Sokolova T.G., Kozhevnikova D.A., Cha S.S., Kim S.J., Kwon K.K., Imanaka T., Atomi H., Bonch-Osmolovskaya E.A., Lee J.H., Kang S.G. Formate-driven growth coupled with H(2) production. Nature. 2010. 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
  • Bangor University, UK
  • 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


2 The ERA.Net RUS Thermogene Novel thermostable enzymes for industrial biotechnology 2013-2016 Great Britain, Germany, Norway,
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,
South Africa,
4 Russian Science Foundation ExploCarb Exploration of carbohydrate metabolism in hyperthermophilic archaea: novel approaches, enzymes and metabolic pathways 2018-2020 Germany,
5 Russian Foundation for Basic Research EXPATH Exploring the diversity of pathways of autotrophic carbon assimilation in thermophilic prokaryotes 2020-2022 Germany,


6 Russian Foundation for Basic Research Discovery of novel thermostable hydrolases from archaea of the Kuril-Kamchatka Region 2021-2022 UK,
7 The Ministry of Education and Science of the Russian Federation HotPETresolve Activity-based protein profiling for the identification of novel thermostable polyethylene terephthalate (PET) degrading enzymes for bio-recycling 2022-2025 Russia,