Isolation, Identification and Survival Strategy of Dietzia maris MX2 Halotolerant Strain from the Yakshinskoe Mineral Salts Deposit

Cover Page

Cite item

Full Text

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

Abstract

Halophilic and halotolerant microorganisms have a high biotechnological potential. They are producers of biologically active substances, stress-protective agents, hydrolytic enzymes, and are used for environmental bioremediation. At the same time, the characterization of novel halotolerant bacteria and the disclosure of their salt tolerance strategy are topical fundamental problems. In the present work, a new strain MX2 was isolated from the salt well brine of the Yakshinskoe potassium-magnesium salt deposit. The isolate is represented by aerobic gram-positive non-motile bacteria that do not produce spores. The cell morphology varies from cocci to short rods that are capable of producing V-shaped forms. Colonies on the surface of agar nutrient medium were circular with an entire edge and raised center, glistening and orange. Bacteria of strain MX2 are halotolerant microorganisms capable of growing at NaCl concentrations up to 9%. Strain MX2 was sequenced. Its size was estimated at 3747717 b. p., the number of protein-coding genes — 3562. Strain MX2 was identified as belonging to the species Dietzia maris based on analysis of 16S rRNA, gyrB, rpoB, recA, ppk gene sequences and using time-of-flight mass spectrometry (MALDI-TOF-MS). D. maris MX2 has complete metabolic pathways for the synthesis of ectoine, hydroxyectoine, and trehalose, as well as transport systems for ectoine, hydroxyectoine, trehalose, glycerol, glycerol-3-phosphate, L-proline, and glycine-betaine. Thus, to ensure the osmotic balance, D. maris MX2 uses the strategy of accumulating compatible organic solutes.

Full Text

Restricted Access

About the authors

M. A. Kharitonova

Kazan (Volga region) Federal University

Author for correspondence.
Email: Maya_Kharitonova@mail.ru
Russian Federation, Kazan

F. G. Kupriyanova-Ashina

Kazan (Volga region) Federal University

Email: Maya_Kharitonova@mail.ru
Russian Federation, Kazan

T. R. Shakirov

JSC “Central Research Institute of Geology of Non-Metallic Mineral Resources”

Email: Maya_Kharitonova@mail.ru
Russian Federation, Kazan

M. S. Vafina

JSC “Central Research Institute of Geology of Non-Metallic Mineral Resources”

Email: Maya_Kharitonova@mail.ru
Russian Federation, Kazan

O. N. Ilinskaya

Kazan (Volga region) Federal University

Email: Maya_Kharitonova@mail.ru
Russian Federation, Kazan

References

  1. Вишняков А. К., Вафина М. С., Игнатович О. О. Строение и условия формирования калийных солей западной части Верхнепечорского соленосного бассейна // Отечественная геология. 2018. № 2. С. 70–78.
  2. Vishnyakov A. K., Vafina M. S., Ignatovich O. O. Structure and formation conditions of potash salts, western part of verkhnepechorsky salt-bearing basin // Otechestvennaya geologiya (National Geology). 2018. № 2. P. 70–78. (In Russian).
  3. Корсакова Е. С., Ананьина Л. Н., Назаров А. В., Бачурин Б. А., Плотникова Е. Г. Разнообразие бактерий семейства Halomonadaceae района разработок Верхнекамского месторождения солей // Микробиология. 2013. Т. 82. С. 247–250.
  4. Korsakova E. S., Anan’ina L.N., Nazarov A. V., Bachurin B. A., Plotnikova E. G. Diversity of bacteria of the family Halomonadaceae at the mining area of the Verkhnekamsk salt deposit // Microbiology (Moscow). 2013. V. 82. P. 249–252.
  5. Литовский В. В. Мировые минеральные ресурсы: калийные соли Прикамья и фундаментальные проблемы геобиогенеза. Екатеринбург: Изд-во Урал. гос. ун-та путей сообщения, 2008. 162 с.
  6. Litovskiy V. V. World mineral resources: potassium salts of the Prikamye and fundamental problems of geobiogenesis. Yekaterinburg: Publishing house of the Ural State University of Railway Transport, 2008. 162 p. (In Russian).
  7. Плотникова Е. Г., Алтынцева О. В., Демаков В. А., Кошелева И. А., Пунтус И. Ф., Филонов А. Е., Гавриш Е. Ю., Боронин А. М. Бактериальные деструкторы полициклических ароматических углеводородов, выделенных из засоленных почв и донных отложений в районах добычи соли // Микробиология. 2001. T. 70. C. 61–69.
  8. Plotnikova E. G., Altyntseva O. V., Demakov V. A., Kosheleva I. A., Puntus I. F., Filonov A. E., Gavrish E. Yu., Boronin A. M. Bacterial degraders of poly cyclic aromatic hydrocarbons isolated from salt-contaminated soils and bottom sediments in salt mining areas // Microbiology (Moscow). 2001. V. 70. P. 51–58.
  9. Пьянкова А. А., Плотникова Е. Г., Шанина С. Н. Бактериальное сообщество рассолов, извлекаемых при подземном растворении калийно-магниевых солей Якшинского месторождения (Республика Коми) // Учен. зап. Казан. ун-та. Сер. Естеств. науки. 2022. Т. 164. кн. 3. С. 457–474.
  10. Pyankova A. A., Plotnikova E. G., Shanina S. N. Bacterial community of the brines extracted during the underground dissolution of potassium-magnesium salts of the Yakshinskoe deposit (Komi Republic, Russia) // Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki. 2022. V. 164. № 3. P. 457–474. (In Russian)
  11. Шанина С. Н., Галамай А. Р., Игнатович О. О., Бурдельная Н. С., Валяева О. В. Органическое вещество соляной толщи южной части Якшинского месторождения калийно-магниевых солей // Геохимия. 2018. T. 56. № 7. С. 693–708.
  12. Shanina S. N., Burdelnaya N. S., Valyaeva O. V., Galamay A. R., Ignatovich O. O. Organic matter of the salt sequence in the southern part of the Yakshinskoe potassium–magnesium salt deposit // Geochem. Int. 2018. V. 56. С. 719–734.
  13. Ястребова О. В., Плотникова Е. Г. Филогенетическое разнообразие бактерий семейства Micrococcaceae, выделенных из биотопов с различным антропогенным воздействием // Вестн. Пермского ун-та. Сер. Биология. 2020. Вып. 4. С. 321–333.
  14. Yastrebova O. V., Plotnikova E. G. Phylogenetic diversity of bacteria of the Micrococcaceae family, isolated from biotopes with different anthropogenic impacts // Bulletin of the Perm University. Series Biology. 2020. Iss. 4. P. 321–333. (In Russian).
  15. Alvarez H. M., Silva R. A., Cesari A. C., Zamit A. L., Peressutti S. R., Reichelt R., Keller U., Malkus U., Rasch C., Maskow T., Mayer F., Steinbüchel A. Physiological and morphological responses of the soil bacterium Rhodococcus opacus strain PD630 to water stress // FEMS Microbiol. Ecol. 2004. V. 50. P. 75–86.
  16. Bursy J., Pierik A. J., Pica N., Bremer E. Osmotically induced synthesis of the compatible solute hydroxyectoine is mediated by an evolutionarily conserved ectoine hydroxylase // J. Biol. Chem. 2007. V. 282. P. 31147–31155.
  17. Cohan F. M. Bacterial species and speciation // Syst. Biol. 2001. V. 50. P. 513‒524.
  18. Fang H., Xu J. B., Nie Y., Wu X. L. Pan-genomic analysis reveals that the evolution of Dietzia species depends on their living habitats // Environ. Microbiol. 2021. V. 23. P. 861–877.
  19. Gharibzahedi S. M.T., Razavi S. H., Mousavi M. Potential applications and emerging trends of species of the genus Dietzia: a review // Ann. Microbiol. 2014. V. 64. P. 421–429.
  20. Goodfellow M., Maldonado L. A. The Families Dietziaceae, Gordoniaceae, Nocardiaceae and Tsukamurellaceae // The Prokaryotes / Eds. Dworkin M., Falkow S., Rosenberg E., Schleifer KH., Stackebrandt E. N.Y.: Springer, 2006. P. 843–889.
  21. Gunde-Cimerman N., Plemenitaš A., Oren A. Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations // FEMS Microbiol. Rev. 2018. V. 42. P. 353–375.
  22. Hagemann M. Coping with high and variable salinity: molecular aspects of compatible solute accumulation // The physiology of microalgae. Developments in applied phycology / Eds. Borowitzka M., Beardall J., Raven J. Cham: Springer, 2016. V. 6. P. 359–372.
  23. Kalscheuer R., Weinrick B., Veeraraghavan U., Besra G. S., Jacobs W. R. Jr. Trehalose-recycling ABC transporter LpqY-SugA-SugB-SugC is essential for virulence of Mycobacterium tuberculosis // Proc. Natl. Acad. Sci. USA. 2010. V. 107. P. 21761–21766.
  24. Kanehisa M., Goto S. KEGG: Kyoto encyclopedia of genes and genomes // Nucl. Acids Res. 2000. V. 28. P. 27–30.
  25. LeBlanc J.C., Gonçalves E. R., Mohn W. W. Global response to desiccation stress in the soil actinomycete Rhodococcus jostii RHA1 // Appl. Environ. Microbiol. 2008. V. 74. P. 2627–2636.
  26. Lorente-Leal V., Liandris E. Bezos J., Pérez-Sancho M., Romero B., de Juan L. MALDI-TOF mass spectrometry as a rapid screening alternative for non-tuberculous mycobacterial species identification in the veterinary laboratory // Front. Vet. Sci. 2022. V. 9. P. 827702.
  27. Nesterenko O. A., Nogina T. M., Kasumova S. A., Kvasnikov E. I., Batrakov S. G. Rhodococcus luteus nom. nov. and Rhodococcus maris nom. nov. // Int. J. Syst. Bacteriol. 1982. V. 32. P. 1‒14.
  28. Oren A. Life in Hypersaline Environments // Their world: A diversity of microbial environments. Advances in Environmental Microbiology / Eds. Hurst C. Cham: Springer, 2016. V. 1. P. 301–339.
  29. Pastor J. M., Salvador M., Argandoña M., Bernal V., Reina-Bueno M., Csonka L. N., Iborra J. L., Vargas C., Nieto J. J., Cánovas M. Ectoines in cell stress protection: uses and biotechnological production // Biotechnol. Adv. 2010. V. 8. P. 782.
  30. Rainey S., Klatte S., Kroppenstedt R. M. Dietzia, a newgenus including Dietzia maris comb. nov., formerly Rhodococcus maris // Int. J. Syst. Bacteriol. 1995. V. 45. P. 32–36.
  31. Rodriguez-R L.M., Konstantinidis K. T. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes // PeerJ Preprints. 2016. V. 4. e1900v1.
  32. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0 // Mol. Biol. Evol. 2013. V. 30. P. 2725–2729.
  33. Tischler D., Niescher S., Kaschabek S. R., Schlömann M. Trehalose phosphate synthases OtsA1 and OtsA2 of Rhodococcus opacus 1CP // FEMS Microbiol. Lett. 2013. V. 342. P. 113–122.
  34. van Beilen J. B., Funhoff E. G. Alkane hydroxylases involved in microbial alkane degradation // Appl. Microbiol. Biotechnol. 2007. V. 74. P. 13‒21.
  35. Ventosa A., Nieto J. J., Oren A. Biology of moderately halophilic aerobic bacteria // Microbiol. Mol. Biol. Rev. 1998. V. 62. P. 504–544.
  36. Waditee-Sirisattha R., Kageyama H., Takabe T. Halophilic microorganism resources and their applications in industrial and environmental biotechnology // AIMS Microbiol. 2016. V. 2. P. 42–54.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Images of borehole brine sample obtained by scanning electron microscopy at 50x (a) and 200x magnification (b). Length of scale marks: 1 mm (a), 200 μm (b)

Download (892KB)
Indexing metadata
3. Fig. 2. IR spectra of well brine sample fractions obtained by differential filtration through Schott filters

Download (386KB)
Indexing metadata
4. Fig. 3. Detection of microorganisms in well brine: direct microscopy of a fixed preparation of a well brine sample (a); microscopy of D. maris MX2 (b); colonies of D. maris MX2 on agarized GRM medium (c). maris MX2 on agarized GRM medium (c). The length of the scale marker is 5 μm

Download (163KB)
Indexing metadata
5. Fig. 4. Effect of different NaCl concentrations on the growth of D. maris MX2. K - cultivation in mineral salt medium MCC containing 0.1% NaCl

Download (162KB)
Indexing metadata
6. Fig. 5. Unrooted phylogenetic trees constructed by maximum likelihood method based on the results of comparative analysis of (a) nucleotide sequences of gyrB genes and (b) amino acid sequences of L-ectoinsynthase of strains D. maris MX2, D. maris IEGM 44, D. maris p3-SID1051, D. kunjamensis ssp. schimae DSM 45139T. maris MX2, D. maris IEGM 44, D. maris p3-SID1051, D. kunjamensis ssp. schimae DSM 45139T, D. kunjamensis DSM 44907T, D. kunjamensis 313, D. lutea YIM 80766T, D. psychralcaliphila ILA-1T, Dietzia sp. oral taxon 368, Dietzia sp. JS16-p6b, D. timorensis ID05-A0528T, Rhodococcus jostii RHA1, Nocardiopsis dassonvillei DSM 43111T, Brevibacterium linens BS258. Numbers indicate the statistical significance of branching order (in %) determined by bootstrap analysis of 500 alternative trees. Scale marker is 0.05 substitutions per nucleotide position

Download (688KB)
Indexing metadata

Copyright (c) 2024 Russian Academy of Sciences

This website uses cookies

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

About Cookies