Anaerobic Thermodesulfovibrio and Aerobic Meiothermus Coexist in Deep Thermal Water

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Abstract

Research on the microorganisms inhabiting deep aquifers is based on sampling the water released from deep wells and is seldom concerned with the physicochemical processes of the water-rock system. The issue of metabolism of aerobic prokaryotes revealed in deep habitats by molecular techniques remains unclear. Cultivation is required for direct determination of relation of prokaryotes to oxygen. In the present work, aerobic and anaerobic bacteria, which were revealed in thermal radon baths of the Belokurikha resort by molecular techniques, were isolated. Profiling by the 16S rRNA gene revealed predominance of members of the Deionococcus-Thermus group belonging to the genus Meiothermus (17.6% reads) and considered strictly aerobic. Anaerobic sulfate-reducing Thermodesulfovibrio were also present in the sample. The habitat was characterized by reductive, alkaline conditions. Target-oriented cultivation revealed aerobically growing Meiothermus sp. 1165, which was closely related to Meiothermus cerbereus. An alkaliphilic anaerobic sulfate reducer Thermodesulfovibrio sp. 1176 was also isolated. The rate of sulfate reduction measured in the Belokurikha water using \({\text{Na}}_{{\text{2}}}^{{{\text{ 35}}}}{\text{S}}{{{\text{O}}}_{{\text{4}}}}\) yielded the value of 41.4 ± 1.06 µm Sred L–1 day–1, or 1.29 nmol S mL–1 day–1. Analysis of the genome of strain 1176 revealed the presence of various mechanisms responsible for its relative resistance to oxygen and oxidative stress, which included superoxide reductase, rubredoxin, a Fe-Mn family superoxide dismutase, a KatG catalase-peroxidase, and a cytochrome bd ubiquinol oxidase. The low redox potential and intense anaerobic sulfate reduction provide evidence for the generally reduced conditions in the Belokurikha deep horizons. Spatial separation of aerobes and anaerobes in the water-rock system, similar to the one occurring in the terrestrial microbial mats, may be hypothesized, as well as occurring of aerobic processes in microniches.

About the authors

A. P. Lukina

Laboratory of Biochemistry and Molecular Biology, Tomsk State University

Email: olga.karnachuk@green.tsu.ru
Russia, 634050, Tomsk

V. V. Kadniko

Winogradsky Institute of Microbiology, Researsch Center of Biotechnology, Russian Academy of Sciences

Email: olga.karnachuk@green.tsu.ru
Russia, 119071, Moscow

I. I. Rusanov

Institute of Bioengineering, Research Center of Biotechnology, Russian Academy of Sciences

Email: olga.karnachuk@green.tsu.ru
Russia, 119071, Moscow

M. R. Avakyan

Laboratory of Biochemistry and Molecular Biology, Tomsk State University

Email: olga.karnachuk@green.tsu.ru
Russia, 634050, Tomsk

A. V. Beletsky

Winogradsky Institute of Microbiology, Researsch Center of Biotechnology, Russian Academy of Sciences

Email: olga.karnachuk@green.tsu.ru
Russia, 119071, Moscow

A. V. Mardanov

Winogradsky Institute of Microbiology, Researsch Center of Biotechnology, Russian Academy of Sciences

Email: olga.karnachuk@green.tsu.ru
Russia, 119071, Moscow

N. V. Pimenov

Institute of Bioengineering, Research Center of Biotechnology, Russian Academy of Sciences

Email: olga.karnachuk@green.tsu.ru
Russia, 119071, Moscow

N. V. Ravin

Winogradsky Institute of Microbiology, Researsch Center of Biotechnology, Russian Academy of Sciences

Email: olga.karnachuk@green.tsu.ru
Russia, 119071, Moscow

O. V. Karnachuk

Laboratory of Biochemistry and Molecular Biology, Tomsk State University

Author for correspondence.
Email: olga.karnachuk@green.tsu.ru
Russia, 634050, Tomsk

References

  1. Джабарова Н.К., Яковенко Э.С., Сидорина Н.Г., Коханенко А.А., Воробьев В.А., Зайцев А.А., Коваленко Т.С., Жиляков И.В. Перспективы развития Белокурихинской курортной зоны Алтайского края // Вопросы курортологии, физиотерапии и лечебной физической культуры. 2016. № 2. С. 43‒47.
  2. Карначук О.В., Пименов Н.В., Юсупов С.К., Франк Ю.А. Пухакка Я.А., Иванов М.В. Распределение, разнообразие и активность сульфатредуцирующих бактерий в водной толще озера Гек-Гель, Азербайджан // Микробиология. 2006. Т. 75. С. 101‒109.
  3. Karnachuk O.V., Pimenov N.V., Yusupov S.K., Frank Yu.A., Puhakka Ya.A., Ivanov M.V. Distribution, diversity, and activity of sulfate-reducing bacteria in the water column in Gek-Gel Lake, Azerbaijan // Microbiology (Moscow). 2006. V. 75. P. 82‒89.
  4. Карначук О.В., Курганская И.А., Авакян М.Р., Франк Ю.А., Иккерт О.П., Филенко Р.А., Данилова Э.В., Пименов Н.В. Ацидофильный Desulfosporosinus из окисленных отходов добычи металлов в Забайкальском крае // Микробиология. 2015. Т. 84. С. 595‒605.
  5. Karnachuk O.V., Kurganskaya I.A., Avakyan M.R., Frank Y.A., Ikkert O.P., Filenko R.A., Danilova E.V., Pimenov N.V. An acidophilic Desulfosporosinus isolated from the oxidized mining wastes in the Transbaikal area // Microbiology (Moscow). 2015. V. 84. P. 677‒686.
  6. Ali N., Khanafer M., Al-Awadhi H. Indigenous oil-degrading bacteria more efficient in soil bioremediation than microbial consortium and active even in super oil-saturated soils // Front. Microbiol. 2022. V. 13. Art. 950051.
  7. Asaf S., Numan M., Khan A.L., Al-Harrasi A. Sphingomonas: from diversity and genomics to functional role in environmental remediation and plant growth // Crit. Rev. Biotechnol. 2020. V. 40. P. 138‒152.
  8. Bar-On Y.M., Phillips R., Milo R. The biomass distribution on Earth // Proc. Natl. Acad. Sci. USA. 2018. V. 115. P. 6506‒6511.
  9. Bell E., Lamminmäki T., Alneberg J., Andersson A.F., Qian C., Xiong W., Hettich R.L., Frutschi M., Bernier-Latmani R. Active sulfur cycling in the terrestrial deep subsurface // ISME J. 2020. V. 14. P. 1260‒1272.
  10. Borgonie G., García-Moyano A., Litthauer D., Bert W., Bester A., van Heerden E., Möller C., Erasmus M., Onstott T.C. Nematoda from the terrestrial deep subsurface of South Africa // Nature. 2011. V. 474. P. 79‒82.
  11. Borisov V.B., Siletsky S.A., Nastasi M.R., Forte E. ROS defense systems and terminal oxidases in bacteria // Antioxidants (Basel). 2021. V. 10. Art. 839.
  12. Brettin T., Davis J.J., Disz T., Edwards R.A., Gerdes S., Olsen G.J., Olson R., Overbeek R., Parrello B., Pusch G.D., Shukla M., Thomason J.A. 3rd, Stevens R., Vonstein V., Wattam A.R., Xia F. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes // Sci. Rep. 2015. V. 5. Art. 8365.
  13. Brown C.T., Hug L.A., Thomas B.C., Sharon I., Castelle C.J., Singh A., Wilkins M.J., Wrighton K.C., Williams K.H., Banfield J.F. Unusual biology across a group comprising more than 15% of domain Bacteria // Nature. 2015. V. 523. P. 208.
  14. Chun J., Oren A., Ventosa A., Christensen H., Arahal D.R., da Costa M.S., Rooney A.P., Yi H., Xu X.W., De Meyer S., Trujillo M.E. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes // Int. J. Syst. Evol. Microbiol. 2018. V. 68. P. 461‒466.
  15. Chung A.P., Rainey F., Nobre M.F., Burghardt J., da Costa M.S. Meiothermus cerbereus sp. nov., a new slightly thermophilic species with high levels of 3-hydroxy fatty acids // Int. J. Syst. Bacteriol. 1997. V. 47. P. 1225‒1230.
  16. Dastager S.G., Lee J.C., Ju Y.J., Park D.J., Kim C.J. Rubellimicrobium mesophilum sp. nov., a mesophilic, pigmented bacterium isolated from soil // Int. J. Syst. Evol. Microbiol. 2008. V. 58. P. 1797‒1800.
  17. Edgar R.C. Search and clustering orders of magnitude faster than BLAST // Bioinformatics 2010. V. 26. P. 2460‒2461.
  18. Finley B.K., Mau R.L., Hayer M., Stone B.W., Morrissey E.M., Koch B.J., Rasmussen C., Dijkstra P., Schwartz E., Hungate B.A. Soil minerals affect taxon-specific bacterial growth // ISME J. 2022. V. 16. P. 1318‒1326.
  19. França L., Albuquerque L., da Costa M.S. Cavicella subterranea gen. nov., sp. nov., isolated from a deep mineral-water aquifer, and emended description of the species Perlucidibaca piscinae // Int. J. Syst. Evol. Microbiol. 2015. V. 65. P. 3812‒3817.
  20. Frank Y.A., Kadnikov V.V., Lukina A.P., Banks D., Beletsky A.V., Mardanov A.V., Sen’kina E.I., Avakyan M.R., Karnachuk O.V., Ravin N.V. Characterization and genome analysis of the first facultatively alkaliphilic Thermodesulfovibrio isolated from the deep terrestrial subsurface // Front. Microbiol. 2016. V. 7. Art. 2000.
  21. Glombitza C., Putman L.I., Rempfert K.R., Kubo M.D., Schrenk M.O., Templeton A.S., Hoehler T.M. Active microbial sulfate reduction in fluids of serpentinizing peridotites of the continental subsurface // Commun. Earth Environ. 2021. V. 2. Art. 84.
  22. Habib N., Khan I.U., Hussain F., Zhou E.M., Xiao M., Dong L., Zhi X.Y., Li W.J. Meiothermus luteus sp. nov., a slightly thermophilic bacterium isolated from a hot spring // Int. J. Syst. Evol. Microbiol. 2017. V. 67. P. 2910‒2914.
  23. Herrmann M., Wegner C.E., Taubert M., Geesink P., Lehmann K., Yan L., Lehmann R., Totsche K.U., Küsel K. Predominance of Cand. Patescibacteria in groundwater is caused by their preferential mobilization from soils and flourishing under oligotrophic conditions // Front. Microbiol. 2019. V. 10. Art. 1407.
  24. Ji M., Williams T.J., Montgomery K., Wong H.L., Zaugg J., Berengut J.F., Bissett A., Chuvochina M., Hugenholtz P., Ferrari B.C. Candidatus eremiobacterota, a metabolically and phylogenetically diverse terrestrial phylum with acid-tolerant adaptations // ISME J. 2021. V. 15. P. 2692‒2707.
  25. Ji Y., Zhang P., Zhou S., Gao P., Wang B., Jiang J. Widespread but poorly understood bacteria: Candidate Phyla Radiation // Microorganisms. 2022. V. 10. Art. 2232.
  26. Jünemann S. Cytochrome bd terminal oxidase // Biochim. Biophys. Acta. 1997. V. 1321. P. 107‒127.
  27. Karnachuk O.V., Frank Y.A., Lukina A.P., Kadnikov V.V., Beletsky A.V., Mardanov A.V., Ravin N.V. Domestication of previously uncultivated Candidatus Desulforudis audaxviator from a deep aquifer in Siberia sheds light on its physiology and evolution // ISME J. 2019. V. 13. P. 1947‒1959.
  28. Karnachuk O.V., Lukina A.P., Kadnikov V.V., Sherbakova V.A., Beletsky A.V., Mardanov A.V., Ravin N.V. Targeted isolation based on metagenome-assembled genomes reveals a phylogenetically distinct group of thermophilic spirochetes from deep biosphere // Environ. Microbiol. 2021. V. 23. P. 3585‒3598.
  29. Kieft T.L., McCuddy S.M., Onstott T.C., Davidson M., Lin L.-H., Mislowack B., Pratt L., Boice E., Lollar B.S., Lippmann-Pipke J., Pfiffner S.M., Phelps T.J., Gihring T., Moser D., van Heerden A. Geochemically generated, energy-rich substrates and indigenous microorganisms in deep, ancient groundwater // Geomicrobiol. J. 2005. V. 22. P. 325–335.
  30. Kim M., Oh H.S., Park S.C., Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rR-NA gene sequence similarity for species demarcation of prokaryotes // Int. J. Syst. Evol. Microbiol. 2014. V. 64. P. 346‒351.
  31. Liu L., Feng Y., Wei L., Zong Z. Genome-based taxonomy of Brevundimonas with reporting Brevundimonas huaxiensis sp. nov. // Microbiol. Spectr. 2021. V. 9. e0011121.
  32. Lovley D.R., Chapelle F.H. Deep subsurface microbial processes // Rev. Geophys. 1995. V. 33. P. 365–381.
  33. Magoc T., Salzberg S.L. FLASH: fast length adjustment of short reads to improve genome assemblies // Bioinformatics. 2011. V. 27. P. 2957–2963.
  34. Masurat P., Fru E.C., Pedersen K. Identification of Meiothermus as the dominant genus in a storage system for spent nuclear fuel // J. Appl. Microbiol. 2005. V. 98. P. 727‒740.
  35. Nelson W.C., Stegen J.C. The reduced genomes of Parcubacteria (OD1) contain signatures of a symbiotic lifestyle // Front. Microbiol. 2015. V. 6. Art. 713.
  36. Nurk S., Bankevich A., Antipov D., Gurevich A.A., Korobeynikov A., Lapidus A., Prjibelski A.D., Pyshkin A., Sirotkin A., Sirotkin Y., Stepanauskas R., Clingenpeel S.R., Woyke T., McLean J.S., Lasken R., Tesler G., Alekseyev M.A., Pevzner P.A. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products // J. Comput. Biol. 2013. V. 20. P. 714‒737.
  37. Parks D.H., Imelfort M., Skennerton C.T., Hugenholtz P., Tyson G.W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes // Genome Res. 2015. V. 25. P. 1043‒1055.
  38. Pedersen K. Exploration of deep intraterrestrial microbial life: current perspectives // FEMS Microbiol. Lett. 2000. V. 185. P. 9‒16.
  39. Planer-Friedrich B., Forberg J., Lohmayer R., Kerl C.F., Boeing F., Kaasalainen H., Stefánsson A. Relative abundance of thiolated species of As, Mo, W, and Sb in hot springs of Yellowstone National Park and Iceland // Environ. Sci. Technol. 2020. V. 54. P. 4295‒4304.
  40. Rajeev L., Garber M.E., Zane G.M., Price M.N., Dubchak I., Wall J.D., Novichkov P.S., Mukhopadhyay A., Kazakov A.E. A new family of transcriptional regulators of tungstoenzymes and molybdate/tungstate transport // Environ. Microbiol. 2019. V. 21. P. 784‒799.
  41. Rawlings D.E., Kusano T. Molecular genetics of Thiobacillus ferrooxidans // Microbiol. Rev. 1994. V. 58. P. 39‒55.
  42. Rempfert K.R., Miller H.M., Bompard N., Nothaft D., Matter J.M., Kelemen P., Fierer N., Templeton A.S. Geological and geochemical controls on subsurface microbial life in the Samail Ophiolite, Oman // Front. Microbiol. 2017. V. 8. Art. 56.
  43. Rognes T., Flouri T., Nichols B., Quince C., Mahé F. VSEARCH: a versatile open source tool for metagenomics // Peer J. Preprints. 2016. V. 4. e2409v1.
  44. Schleheck D., Tindall B.J., Rosselló-Mora R., Cook A.M. Parvibaculum lavamentivorans gen. nov., sp. nov., a novel heterotroph that initiates catabolism of linear alkylbenzenesulfonate // Int. J. Syst. Evol. Microbiol. 2004. V. 54. P. 1489‒1497.
  45. Tindall B.J., Sikorski J., Lucas S., Goltsman E., Copeland A., Glavina Del Rio T., Nolan M., Tice H., Cheng J.F., Han C., Pitluck S., Liolios K., Ivanova N., Mavromatis K., Ovchinnikova G., Pati A., Fähnrich R., Goodwin L, Chen A., Palaniappan K., Land M., Hauser L., Chang Y.J., Jeffries C.D., Rohde M., Göker M., Woyke T, Bristow J., Eisen J.A., Markowitz V., Hugenholtz P., Kyrpides N.C., Klenk H.P., Lapidus A. Complete genome sequence of Meiothermus ruber type strain (21) // Stand. Genomic Sci. 2010. V. 3. P. 26‒36.
  46. Wanger G., Southam G. Onstott T.C. Structural and chemical characterization of a natural fracture surface from 2.8 kilometers below land surface: biofilms in the deep subsurface // Geomicrobiol. J. 2006. V. 23. P. 443‒452.
  47. Weinstein D.J., Allen S.E., Lau M.C.Y., Erasmus M., Asalone K.C., Walters-Conte K., Deikus G., Sebra R., Borgonie G., van Heerden E., Onstott T.C., Bracht J.R. The genome of a subterrestrial nematode reveals adaptations to heat // Nat. Commun. 2019. V. 10. Art. 5268.
  48. Widdel F.F., Bak R. Gram negative mesophilic sulfate reducing bacteria // The Prokaryotes: A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications / Eds. Balows A. et al. Berlin: Springer, 1992. P. 3352–3378.
  49. Woycheese K.M., Meyer-Dombard D.R., Cardace D., Argayosa A.M., Arcilla C.A. Out of the dark: transitional subsurface-to-surface microbial diversity in a terrestrial serpentinizing seep (Manleluag, Pangasinan, the Philippines) // Front. Microbiol. 2015. V. 6. Art. 44.
  50. Zhang Y., Gladyshev V.N. Molybdoproteomes and evolution of molybdenum utilization // J. Mol. Biol. 2008. V. 379. P. 881‒899.
  51. Zhao Q., Guo Q., Luo L., Yan K. Tungsten accumulation in hot spring sediments resulting from preferred sorption of aqueous polytungstates togGoethite // Int. J. Environ. Res. Public Health. 2021. V. 18. P. 12629.

Supplementary files

Supplementary Files
Action
1. JATS XML
2.

Download (177KB)
3.

Download (1MB)
4.

Download (353KB)

Copyright (c) 2023 А.П. Лукина, В.В. Кадников, И.И. Русанов, М.Р. Авакян, А.В. Белецкий, А.В. Марданов, Н.В. Пименов, Н.В. Равин, О.В. Карначук

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies