Adaptation to growth at low temperature of psychrotrophic bacteria isolated from soil of the northern region of the Perm Krai

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Halotolerant bacteria of the genera Bacillus, Microbacterium, Glutamicibacter, Brevibacterium, Rhodococcus, Pseudomonas, Thalassospira, as well as halophilic bacteria of the genus Halomonas, previously isolated from saline ecotopes of the northern region of Perm Krai, were studied for their ability to grow at low temperatures. It was found that strains of bacteria of the genera Rhodococcus, Glutamicibacter, Microbacterium, Pseudomonas, Brevibacterium, Thalassospira and Halomonas grew at a temperature of 5°C. Bacteria belonging to the genera Brevibacterium and Rhodococcus grew at 0°C. Cryoprotective substances were studied using proton magnetic resonance spectroscopy. Since in natural habitats bacterial cells can attach to the surfaces of solid particles and form microcolonies, cryoprotectors were studied by growing bacterial strains on the surface of an agar medium. Using the psychrotrophic culture of Rhodococcus sp. SMB38 as an example, the dependence of the osmolyte composition on cultivation conditions was studied. When grown on an agar medium without adding sodium chloride at 25°C, the cells of the strain Rhodococcus sp. SMB38 synthesized ectoine, hydroxyectoine, trehalose and alanine. The proportion of trehalose was higher than other compounds and amounted to 48%. With a decrease in temperature, the intracellular amount of trehalose, ectoine and alanine increased. In this case, the proportion of trehalose was higher than other compounds and was equal to 55%. The same patterns were noted when growing the strain on a dense medium containing 2% NaCl. However, under cold conditions, a change in the ratio of compounds was revealed: the largest share, equal to 48%, belonged to ectoine. In this regard, the study of cryoprotective substances was carried out by culturing cold-resistant strains on a dense medium containing 2% NaCl. It was shown that the cells of bacteria of the genera Halomonas and Thalassospira accumulated ectoine. In the cells of bacteria of the genera Glutamicibacter and Pseudomonas, trehalose performed the function of a cryoprotector. Psychrotrophic culture of the genus Brevibacterium accumulated trehalose, ectoine and alanine in cells. In this work, an increase in the amount of alanine in bacterial cells with a decrease in temperature is described for the first time, which may indicate the participation of this amino acid in adaptation to cold.

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L. Anan’ina

Perm Federal Research Center of the UB RAS

编辑信件的主要联系方式.
Email: ludaananyina@mail.ru

Institute of Ecology and Genetics of Microorganisms UB RAS

俄罗斯联邦, 614081, Perm

A. Gorbunov

Perm Federal Research Center of the UB RAS

Email: ludaananyina@mail.ru

Institute of Technical Chemistry UB RAS

俄罗斯联邦, 6614013, Perm

V. Aleev

Perm Federal Research Center of the UB RAS

Email: ludaananyina@mail.ru

Institute of Ecology and Genetics of Microorganisms UB RAS

俄罗斯联邦, 614081, Perm

O. Yastrebova

Perm Federal Research Center of the UB RAS

Email: ludaananyina@mail.ru

Institute of Ecology and Genetics of Microorganisms UB RAS

俄罗斯联邦, 614081, Perm

参考

  1. Ананьина Л. Н. Филогенетическое положение галотолерантного штамма Brevibacterium sp. U1, выделенного из засоленной почвы, в системе рода Brevibacterium // Вестник Пермского университета. Серия: Биология. 2019. № 4. С. 459–463.
  2. Ананьина Л. Н., Горбунов А. А., Шестакова Е. А., Пьянкова А. А., Плотникова Е. Г. Совместимые вещества, накапливаемые клетками штамма Glutamicibacter sp. SMB32 в ответ на действие абиотических факторов окружающей среды // Микробиология. 2023. Т. 92. С. 490–499.
  3. Anan’ina L.N., Gorbunov A. A.,Shestakova E.A., Pyankova A. A., Plotnikova E. G. Compatible solutes accumulated by Glutamicibacter sp. strain SMB32 in response to abiotic environmental factors // Microbiology (Moscow). 2023. V. 92. P. 650–657.
  4. Ананьина Л. Н., Плотникова Е. Г., Гавриш Е. Ю., Демаков В. А., Евтушенко Л. И. Salinicola socius gen. nov., sp. noV. умеренно галофильная бактерия из ассоциации микроорганизмов, утилизирующей нафталин // Микробиология. 2007. Т. 76. С. 369–376.
  5. Anan’ina L.N., Plotnikova E. G., Demakov V. A., Gavrish E.Yu., Evtushenko L. I. Salinicola socius gen. nov., sp. nov., a moderately halophilic bacterium from a naphthalene-utilizing microbial association // Microbiology (Moscow). 2007. V. 76. P. 324–330.
  6. Василец Е. А. Условия промерзания почвы в Пермском крае // XV Всероссийская конф. студентов, аспирантов и молодых ученых “Географическое изучение территориальных систем”. Пермь, 2021. С. 153–157.
  7. Савин И. Ю., Виндекер Г. В. Некоторые особенности использования оптических свойств поверхности почв для определения их влажности // Почвоведение. 2021. № 7. С. 806–814.
  8. Комарова Т. И., Коронелли Т. В., Тимохина Е. А. Роль низкомолекулярных азотистых соединений в осмотолерантности бактерий родов Rhodococcus и Arthrobacter // Микробиология. 2002. Т. 71. С. 166–170.
  9. Komarova. T.I., Koronelli T. V., Timokhina E. A. The role of low-molecular-weight nitrogen compounds in the osmotolerance of Rhodococcus erythropolis and Arthrobacter globiformis // Microbiology (Moscow). 2002. V. 71. P. 139–142.
  10. 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.
  11. 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. https://doi.org/10.1134/S0026261713020070
  12. Плакунов В. К., Журина М. В., Беляев С. С. Устойчивость нефтеокисляющего микроорганизма, Dietzia sp. к гиперосмотическому шоку в реконструированных биопленках // Микробиология. 2008. Т. 77. С. 581–589.
  13. Plakunov V. K., Zhurina M. V., Belyaev S. S. Resistance of the oil-oxidazing vicroorganism Dietzia sp. to hyper osmotic shok in reconstructed biofilms // Microbiology (Moscow). 2008. V. 77. P. 515–522.
  14. Плотникова Е. Г. Ястребова О. В. Кошелева И. А. Пунтус И. Ф. Филонов А. Е. Гавриш Е. Ю. Демаков В. А. Боронин А. М. Бактерии-деструкторы полициклических ароматических углеводородов, выделенные из почв и донных отложений района солеразработок // Микробиология. 2001. T. 70. С. 61–69.
  15. 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 polycyclic aromatic hydrocarbons isolated from salt-contaminated soils and bottom sediments in salt mining areas // Microbiology (Moscow). 2001. V. 70. P. 61–69. https://doi.org/10.1023/A:1004892804670
  16. Стрелкова Е. А., Позднякова Н. В., Журина М. В., Плакунов В. К., Беляев С. С. Роль внеклеточного полимерного матрикса в устойчивости бактериальных биопленок к экстремальным факторам среды // Микробиология. 2013. Т. 82. С. 131–138.
  17. Strelkova E. A., Pozdnyakova N. V., Zhurina M. V., Plakunov V. K., Belyaev S. S. Role of the extracellular polymer matrix in resistance of bacterial biofilms to extreme environmental factors // Microbiology (Moscow). 2013. V. 82. P. 119–125.
  18. Ястребова О. В., Ананьина Л. Н., Плотникова Е. Г. Бактерии рола Bacillus, выделенные из почв района солеразработок // Вестник Пермского университета. 2008. № 9 (25). С. 58–62.
  19. Ястребова О. В., Пьянкова А. А., Плотникова Е. Г. Бактерии-деструкторы фталатов, выделенные из района промышленной добычи и переработки калийно-магниевых соей // Прикл. биохимия и микробиология. 2019. Т. 55. С. 378–385.
  20. Yastrebova O. V., Pyankova A. A., Plotnikova E. G. Phthalate-degrading bacteria isolated from an industrial mining area and the processing of potassium and magnesium salts // Appl. Biochem. Microbiol. 2019. V. 55. P. 397–404. https://doi.org/10.1134/S000368381904015X http://accident.perm.ru/index.php/spravochnyj-razdel/opasnye-meteorologicheskie-yavleniya/409-zamorozki-i-snegopady-v-teplyj-period-goda
  21. 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. https://doi.org/10.1016/j.femsec.2004.06.002
  22. Anan’ina L.N., Gorbunov A. A., Pyankova A. A. Physiological response of the moderately halophilic psychrotolerant strain Chromohalobacter sp. N1 to salinity change and low temperature // Can. J. Microbiol. 2021. V. 67. P. 342–348. https://doi.org/10.1139/cjm-2020-0299
  23. Anan’ina L.N., Kosheleva I. А., Plotnikova E. G. Bacterial consortium as a model for studying the response of the microbial community of the Verkhnekamsk salt mining region to combined pollution // Теор. и прикл. экология. 2022. № 2. С. 116–123.
  24. Bernard T., Jebbar M., Rassouli Y., Himdi-Kabbab S., Hamelin J., Blanco C. Ectoine accumulation and osmotic regulation in Brevibacterium linens // J. Gen. Microbiol. 1993. V. 139. P. 129–136.
  25. Chen X. M., Jiang Y., Li Y. T., Zhang H. H., Li J., Chen X., Zhao Q., Zhao J., Si J., Lin Z. W., Zhang H., Dyson P., An L. Z. Regulation of expression of trehalose-6-phosphate synthase during cold shock in Arthrobacter strain A3 // Extremophiles. 2011. V. 15. P. 499–508. https://doi.org/10.1007/s00792-011-0380-5
  26. Chenu C., Sotzky G. Interactions between soil particles and microorganisms. Edition: IUPAC series of Applied Chemistry Chapter. Wiley & Sons. 2002. P. 3–40.
  27. De Santi C., Leiros H. K., Di Scala A., de Pascale D., Altermark B., Willassen N. P. Biochemical characterization and structural analysis of a new cold-active and salt-tolerant esterase from the marine bacterium Thalassospira sp. // Extremophiles. 2016. V. 20. P. 323–336. https://doi.org/10.1007/s00792-016-0824-z
  28. Goordial J., Raymond-Bouchard I., Zolotarov Y., de Bethencourt L., Ronholm J., Shapiro N., Woyke T., Stromvik M., Greer C. W., Bakermans C., Whyte L. Cold adaptive traits revealed by comparative genomic analysis of the eurypsychrophile Rhodococcus sp. JG3 isolated from high elevation McMurdo Dry Valley permafrost, Antarctica // FEMS Microbiol. Ecol. 2016. V. 92. https://doi.org/10.1093/femsec/fiv154
  29. Guro P., Karaevskaya E., Kuznetsova I., Karlov D., Sazanova A., Safronova V. Complete genome sequence of Glutamicibacter sp. strain M10, isolated from an Arctic permafrost sample // Microbiol. Resour. Announc. 2023. V. 12. Art. e0112022. https://doi.org/10.1128/mra.01120-22
  30. Harishchandra R. K., Wulff S., Lentzen G., Neuhaus T., Galla H. J. The effect of compatible solute ectoines on the structural organization of lipid monolayer and bilayer membranes // Biophys. Chem. V. 150. P. 37–46. https://doi.org/10.1016/j.bpc.2010.02.007
  31. Ivanova V., Lyutskanova D., Stoilova-Disheva M., Kolarova M., Aleksieva K., Raykovska V., Peltekova V., Laatsch H. Isolation and identification of α,α-trehalose and glycerol from an arctic psychrotolerant Streptomyces sp. SB9 and their possible role in the strain’s survival // Prep. Biochem. Biotechnol. 2009. V. 39. P. 46–56. https://doi.org/10.1080/10826060802589585
  32. Jeanson S., Floury J., Gagnaire V., Lortal S., Thierry A. Bacterial colonies in solid media and foods: a review on their growth and interactions with the micro-environment // Front. Microbiol. 2015. V. 6. Art. 1284. https://doi.org/10.3389/fmicb.2015.01284
  33. Jousse C., Dalle C., Canet I., Lagrйe M., Traпkia M., Lyan B., Mendes C., Sancelme M., Amato P., Delort A.-M. Metabolomic study of the response to cold shock in a strain of Pseudomonas syringae isolated from cloud water // Metabolomics. 2018. V. 14. Art. 11 https://doi.org/10.1007/s11306-017-1295-7
  34. Kanapathipillai M., Lentzen G., Sierks M., Park C. B. Ectoine and hydroxyectoine inhibit aggregation and neurotoxicity of Alzheimer’s β-amyloid // FEBS Lett. 2005. V. 579. P. 4775–4780. https://doi.org/10.1016/j.febslet.2005.07.057
  35. Kandror O., DeLeon A., Goldberg A. L. Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures // Proc. Natl. Acad. Sci. USA. 2002. V. 99. P. 9727–9732. https://doi.org/10.1073/pnas.142314099
  36. Kaye J. Z., Baross J. A. Synchronous effects of temperature, hydrostatic pressure, and salinity on growth, phospholipid profiles, and protein patterns of four Halomonas species isolated from deep-sea hydrothermal-vent and sea surface environments // Appl. Environ. Microbiol. 2004. V. 70. P. 6220–6229. https://doi.org/10.1128/AEM.70.10.6220-6229.2004
  37. Kuhlmann A. U., Bursy J., Gimpel S., Hoffmann T., Bremer E. Synthesis of the compatible solute ectoine in Virgibacillus pantothenticus is triggered by high salinity and low growth temperature // Appl. Environ. Microbiol. 2008. V. 74. P. 4560–4563. https://doi.org/10.1128/AEM.00492-08
  38. Ma Y., Wang Q., Xu W., Liu X., Gao X., Zhang Y. Stationary phase-dependent accumulation of ectoine is an efficient adaptation strategy in Vibrio anguillarum against cold stress // Microbiol. Res. 2017. V. 205. P. 8–18. https://doi.org/10.1016/j.micres.2017.08.005
  39. Mari E., Ricci C., Pieraccini S., Spinozzi F., Mariani P., Ortore M. G. Trehalose effect on the aggregation of model proteins into amyloid fibrils // Life (Basel). 2020. V. 10. Art. 60. https://doi.org/10.3390/life10050060
  40. Mei Y. Z., Huang P. W., Liu Y., He W., Fang W. W. Cold stress promoting a psychrotolerant bacterium Pseudomonas fragi P121 producing trehaloase // World J. Microbiol. Biotechnol. 2016. V. 32. Art. 134. https://doi.org/10.1007/s11274-016-2097-1
  41. Mikami K., Takahashi M., Hirata R., Yokoyama T., Taniguchi M., Saga N., Mori T. Alanine is a possible compatible solute involved in cold acclimation in the marine red alga Porphyra yezoensis // Seaweed: Ecology, Nutrient Composition and Medicinal Uses / Ed. Pomin V. H. New York: Nova Science Publishers, 2011. 1–14 p.
  42. Nedwell D. B., Rutter M. Influence of temperature on growth rate and competition between two psychrotolerant Antarctic bacteria: low temperature diminishes affinity for substrate uptake // Appl. Environ. Microbiol. 1994. V. 60. P. 1984–1992.
  43. Plotnikova E. G., Anan’ina L.N., Krausova V. I., Ariskina E. V., Prisyazhnaya N. V., Lebedev A. T., Demakov V. A., Evtushenko L. I. Thalassospira permensis sp. nov., a new terrestrial halotolerant bacterium isolated from a naphthalene-utilizing microbial consortium // Microbiology (Moscow). 2011. V. 80. P. 691–699.
  44. Ramasamy K. P., Mahawar L., Rajasabapathy R., Rajeshwari K., Miceli C., Pucciarelli S. Comprehensive insights on environmental adaptation strategies in Antarctic bacteria and biotechnological applications of cold adapted molecules // Front. Microbiol. 2023. V. 14. Art. 1197797. https://doi.org/10.3389/fmicb.2023.1197797
  45. Raymond-Bouchard I., Goordial J., Zolotarov Y., Ronholm J., Stromvik M., Bakermans C., Whyte L. G. Conserved genomic and amino acid traits of cold adaptation in subzero-growing Arctic permafrost bacteria // FEMS Microbiol. Ecol. 2018. V. 94. https://doi.org/10.1093/femsec/fiy023. PMID: 29528411
  46. Raza A., Bhardwaj S., Rahman M. A., García-Caparrós P., Habib M., Saeed F., Charagh S., Foyer C. H., Siddique K. H.M., Varshney R. K. Trehalose: A sugar molecule involved in temperature stress management in plants // Crop J. 2024. V. 12. P. 1–16. http://dx.doi.org/10.1016/j.cj.2023.09.010
  47. Reddy G. S.N., Matsumoto G. I., Schumann P., Stackebrandt E., Shivaji S. Psychrophilic pseudomonads from Antarctica: Pseudomonas antarctica sp. nov., Pseudomonas meridiana sp. noV. and Pseudomonas proteolytica sp. nov. // Int. J. Syst. Evol. Microbiol. 2004. V. 54. P. 713–719. https://doi.org/10.1099/ijs.0.02827-0
  48. Takeyama N., Huang M., Sato K., Galipon J., Arakawa K. Complete genome sequence of Halomonas hydrothermalis strain Slthf2, a halophilic bacterium isolated from a deep-sea hydrothermal-vent environment // Microbiol. Resour. Announc. 2020. V. 9. Art. e00294-20. https://doi.org/10.1128/MRA.00294-20
  49. Uhlırova E., Santruckova H. Growth rate of bacteria is affected by soil texture and extraction procedure // Soil Biol. Biochem. 2003. V. 35. P. 217–224.

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2. Fig. 1. Amounts of osmolytes accumulated by Rhodococcus sp. SMB38 cells under different cultivation conditions. Incubation was carried out on a solid medium. Glucose served as a source of carbon and energy. Cultivation conditions (medium salinity, temperature): 1 – without sodium chloride, 25°C; 2 – without sodium chloride, 5°C; 3 – 2% NaCl, 25°C; 4 – 2% NaCl, 5°C.

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3. Fig. 2. 1H NMR spectra of ethanol extracts from cells of cold-resistant bacterial strains isolated from the VMKMS area of ​​Perm Krai. The bacterial strains were cultured at 5°C on a dense medium containing 2% sodium chloride. Legend: alanine (A); glutamate (G); glutamine (Q); trehalose (T); ectoine (E); unidentified compound (X); monodeuterium water (HDO); tert-butyl alcohol (t-BuOH); SMB31, SMB32, SMB34, SMB38, SN101, U1 – designations of bacterial strains.

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4. Fig. 3. Sections of the 1H NMR spectra of ethanol extracts from cells of the Pseudomonas sp. SN101 strain grown at 5°C on an agar medium containing 2% sodium chloride (a) and without it (b). Glucose served as a source of carbon and energy in both variants. Legend: glutamate (G); trehalose (T); unidentified compounds (X, Y).

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