Taxonomic and functional diversity of bacteria isolated from technogenic alkaline reservoir | Vestnik Tomskogo gosudarstvennogo universiteta. Biologiya - Tomsk State University Journal of Biology. 2024. № 65. DOI: 10.17223/19988591/65/2

Taxonomic and functional diversity of bacteria isolated from technogenic alkaline reservoir

Currently, more and more attention is paid to the study of microorganisms living in various extreme environments and those characterized by high salinity and alkalinity, in particular. The microbial communities of natural halo-alkaline ecosystems have been studied well. However, there is insufficient knowledge about the microorganisms of artificial ecosystems formed under the influence of technogenic factors. This work was aimed to study the diversity of cultivated bacteria in the microbial community of the bottom sediments of an alkaline technogenic reservoir located on the territory of the Verkhnekamsk potassium-magnesium salt deposit (Perm Krai, Russia). The studied reservoir is an extreme ecosystem characterized by a high content of water-soluble salts, heavy metals, and alkalinity of the environment. Various organic pollutants, namely, aromatic and aliphatic compounds can be found there as well. In this regard, the study was aimed to search for haloalkaliphilic destructor bacteria that are promising for bioremediation of saline/alkaline media (soils, water bodies) contaminated with toxic organic compounds. Thirty-three strains of alkalitolerant and halophilic/halotolerant bacteria were isolated from the bottom sediments of the alkaline technogenic reservoir. Based on the analysis of the nucleotide sequences of the 16S rRNA gene, the isolated strains belonged to the classes Bacilli, Gammaproteobacteria, Alphaproteobacteria, and Actinomycetes. The dominant group among the identified cultivated microorganisms were bacteria of the Bacillaceae family (13 strains), represented by the genera Evansella, Oceanobacillus, Bacillus, Alkalihalobacillus, Paralkalibacillus, Salipaludibacillus, Cytobacillus and Exiguobacterium. Most of the isolates were extremophiles capable of growing at high concentrations of NaCl (up to 250 g/l) and pH 7-11. Strains Microbacterium sp. СXP-56, Brachybacterium sp. CXP-58, Salipaludibacillus sp. CX3-6 and Alkalihalobacillus sp. CX2-3.1 were obligate alkalophiles which grow in the pH range of 9.5-10.5. Alkalihalobacillus spp. CX2-3 and CX2-3.1, Salipaludibacillus sp. CX3-6 may be described as new taxa because these new strains had low percentage of similarity in 16S rRNA genes (97.27; 97.12 and 97.75%) with closely related type strains. Most of the isolated strains had biodegradable properties and were able to use naphthalene, biphenyl, ortho-phthalic, benzoic acids, and diesel fuel as the sole source of carbon and energy. The destructor strains, which carry out effective decomposition of aromatic compounds at high alkalinity and salinity of the environment, presented interest, namely, Kocuria sp. CXP-33, Evansella sp. СX2-1, Halomonas sp. CX2-8,Micrococcus sp. CXP-15, Brevibacterium spp. CXP-21, CXP-53, and Brachybacterium spp. CXP-46, CXP-58. The results obtained in this study are of fundamental importance and of interest for possible practical application in the restoration of saline/alkaline soils and water bodies contaminated with various organic compounds. Data on the identification of the bacterial strains and on their ecological and physiological characteristics are available in supplements on the journal’s website: https://journals.tsu.ru/biology/&journal_page=archive&id=2383 The article contains 2 Figures, 2 Supplements, 58 References. The Authors declare no conflict of interest.

Download file

Counter downloads: 12

Download attachment archive

Counter downloads: 9

Keywords

alkaline waste stabilization ponds, alkalophilic bacteria, halophilic and halotolerant bacteria, Verkhnekamsk salt deposit

Authors

Name	Organization	E-mail
Nechaeva Yulia I.	Institute of Ecology and Genetics of Microorganisms, UB RAS; Perm State University	ulia-2012@mail.ru
Aleev Vladislav S.	Institute of Ecology and Genetics of Microorganisms, UB RAS	v1.vvv132@yandex.ru
Shestakova Elena A.	Institute of Ecology and Genetics of Microorganisms, UB RAS	shestakova.e@iegm.ru
Pyankova Anna A.	Institute of Ecology and Genetics of Microorganisms, UB RAS	annpjankva@mail.ru
Plotnikova Elena G.	Institute of Ecology and Genetics of Microorganisms, UB RAS; Perm State University	peg_el@mail.ru

Всего: 5

References

Fathepure B.Z. Recent studies in microbial degradation of petroleum hydrocarbons in hypersaline environments // Frontiers in microbiology. 2014. Vol. 5. P. 173.

СП 3.3686-21 "Санитарно-эпидемиологические требования по профилактике инфекционных болезней" от 28 января 2021 г.

Gharibzahedi S.M.T., Razavi S.H., Mousavi S.M. Characterization of bacteria of the genus Dietzia: an updated review // Annals of microbiology. 2014. Vol. 64, № 1. PP. 1-11.

De la Haba R.R., Arahal D.R., Sanchez-Porro C., Ventosa A. The family Halomonadaceae // The Prokaryotes / eds by E. Rosenberg, E.F. DeLong, S. Lory, E. Stackebrandt, F. Thompson. Springer, Berlin, Heidelberg, 2014. PP. 325-360.

Gao L., Fang B.Z., Liu Y.H., Huang Y., Jiao J.Y., Li L., Li W.J. Ornithinimicrobium sediminis sp. nov., a novel actinobacterium isolated from a saline lake sediment // Archives of microbiology. 2022. Vol. 204, № 5. P. 277.

Ali N., Dashti N., Al-Mailem D., Eliyas M., Radwan S. Indigenous soil bacteria with the combined potential for hydrocarbon consumption and heavy metal resistance // Environmental science and pollution research. 2012. Vol. 19. PP. 812-820.

Pei S., Xie F., Niu S., Ma L., Zhang R., Zhang G. Brevibacteriumprofundi sp. nov., isolated from deep-sea sediment of the Western Pacific Ocean // International journal of systematic and evolutionary microbiology. 2020. Vol. 70, № 11. PP. 5818-5823.

Takeuchi M., Fang C.X., Yokota A. Taxonomic study of the genus Brachybacterium: proposal of Brachybacterium conglomeratum sp. nov., nom. rev., Brachybacterium paraconglomeratum sp. nov., and Brachybacterium rhamnosum sp. nov // International journal of systematic and evolutionary microbiology. 1995. Vol. 45, № 1. PP. 160-168.

Buczolits S., Schumann P., Weidler G., Radax C., Busse H.J. Brachybacterium muris sp. nov., isolated from the liver of a laboratory mouse strain // International journal of systematic and evolutionary microbiology. 2003. Vol. 53. PP. 1955-1960.

Harboul K., Alouiz I, Hammani K., El-Karkouri A. Isotherm and kinetics modeling of biosorption and bioreduction of the Cr (VI) by Brachybacterium paraconglomeratum ER41 // Extremophiles. 2022. Vol. 26, № 3. P. 30.

Tuo L., Yan X.R., Li F.N., Bao Y.X., Shi H.C., Li H.Y., Sun C.H. Brachybacterium endophyticum sp. nov., a novel endophytic actinobacterium isolated from bark of Scutellaria baicalensis Georgi // International journal of systematic and evolutionary microbiology. 2018. Vol. 68, № 11. PP. 3563-3568.

Li W.J., Chen H.H., Kim C.J., Park D.J., Tang S.K., Lee J.C., Jiang C.L. Microbacterium halotolerans sp. nov., isolated from a saline soil in the west of China // International journal of systematic and evolutionary microbiology. 2005. Vol. 55, № 1. PP. 67-70.

Zhu Q.H., Yang C.L., Luo X.X., Zhang L.L., Xia Z.F. Microbacterium karelineae sp. nov. isolated from a halophyte plant in the Taklamakan desert // International Journal of systematic and evolutionary microbiology. 2021. Vol. 71, № 2. P. 004629.

Xu Y., Minhazul K.A., Wang X., Liu X., Li X., Meng Q., Sun B. Biodegradation of phthalate esters by Paracoccus kondratievae BJQ0001 isolated from Jiuqu (Baijiu fermentation starter) and identification of the ester bond hydrolysis enzyme // Environmental pollution. 2020. Vol. 263. P. 114506.

Gan X., Teng Y., Zhao L., Ren W., Chen W., Hao J., Luo Y. Influencing mechanisms of hematite on benzo (a) pyrene degradation by the PAH-degrading bacterium Paracoccus sp. strain HPD-2: insight from benzo (a) pyrene bioaccessibility and bacteria activity // Journal of hazardous materials. 2018. Vol. 359. PP. 348-355.

Xue H., Piao C.G., Guo M.W., Wang L.F., Li Y. Paracoccus aerius sp. nov., isolated from air // International journal of systematic and evolutionary microbiology. 2017. Vol. 67, № 8. PP. 2586-2591.

Zhang G., Xian W., Yang J., Liu W., Jiang H., Li W. Paracoccus gahaiensis sp. nov. isolated from sediment of Gahai Lake, Qinghai-Tibetan Plateau, China // Archives of microbiology. 2016. Vol. 198. PP. 227-232.

Kovacs G., Burghardt J., Pradella S., Schumann P., Stackebrandt E., Marialigeti K. Kocuria palustris sp. nov. and Kocuria rhizophila sp. nov., isolated from the rhizoplane of the narrow-leaved cattail (Typha angustifolia) // International journal of systematic and evolutionary microbiology. 1999. Vol. 49, № 1. PP. 167-173.

Tvrzova L., Schumann P., Sedlacek I., Pacova Z., Sproer C., Verbarg S., Kroppenstedt R.M. Reclassification of strain CCM 132, previously classified as Kocuria varians, as Kocuria carniphila sp. nov // International journal of systematic and evolutionary microbiology. 2005. Vol. 55, № 1. PР. 139-142.

Mulla S.I., Talwar M.P., Bagewadi Z.K., Hoskeri R.S., Ninnekar H.Z. Enhanced degradation of 2-nitrotoluene by immobilized cells of Micrococcus sp. strain SMN-1 // Chemosphere. 2013. Vol. 90, № 6. PP. 1920-1924.

Jegan J., Vijayaraghavan K., Senthilkumar R., Velan M. Naphthalene degradation kinetics of Micrococcus sp., isolated from activated sludge // CLEAN-Soil, Air, Water. 2010. Vol. 38, № 9. PP. 837-842.

Dastager S., Krishnamurthi S., Rameshkumar N., Dharne M. The Family Micrococcaceae // The Prokaryotes / eds by E. Rosenberg, E.F. DeLong, S. Lory, E. Stackebrandt, F. Thompson. Springer, Berlin, Heidelberg, 2014. PP. 455-498.

Maroof L., Khan I., Hassan H., Azam S., Khan W. Microbial degradation of low density polyethylene by Exiguobacterium sp. strain LM-IK2 isolated from plastic dumped soil // World journal of microbiology and biotechnology. 2022. Vol. 38, № 11. P. 197.

Lopez M.C., Galan B., Carmona M., Navarro Llorens J.M., Pereto J., Porcar M., Garda J.L. Xerotolerance: a new property in Exiguobacterium genus // Microorganisms. 2021. Vol. 9, № 12. P. 2455.

Ningthoujam R., Satiraphan M., Sompongchaiyakul P., Bureekul S., Luadnakrob P., Pinyakong O. Bacterial community shifts in a di-(2-ethylhexyl) phthalate-degrading enriched consortium and the isolation and characterization of degraders predicted through network analyses // Chemosphere. 2023. Vol. 310. P. 136730. 10.1016/j. chemosphere.2022.136730.

Tarasov K., Yakhnenko A., Zarubin M., Gangapshev A., Potekhina N.V., Avtukh A.N., Kravchenko E. Cytobacillus pseudoceanisediminis sp. nov., a novel facultative methylotrophic bacterium with high heavy metal resistance isolated from the deep underground saline spring // Current microbiology. 2023. Vol. 80, № 1. P. 31. 10.1007/ s00284-022-03141-8.

Patel S., Gupta R.S. A phylogenomic and comparative genomic framework for resolving the polyphyly of the genus Bacillus: proposal for six new genera of Bacillus species, Peribacillus gen. nov., Cytobacillus gen. nov., Mesobacillus gen. nov., Neobacillus gen. nov., Metabacillus gen. nov. and Alkalihalobacillus gen. nov // International journal of systematic and evolutionary microbiology. 2020. Vol. 70, № 1. PP. 406-438.

Wang S., Dong L., Zhao B., Zhang X., Xu S., Wu K., Wang H. Salipaludibacillus keqinensis sp. nov., a moderately halophilic bacterium isolated from a saline-alkaline lake // Antonie van Leeuwenhoek. 2019. Vol. 112. PP. 897-903.

Chen Y.G., Zhang Y.Q., Wang Y.X., Liu Z.X., Klenk H.P., Xiao H.D., Li W.J. Bacillus neizhouensis sp. nov., a halophilic marine bacterium isolated from a sea anemone // International journal of systematic and evolutionary microbiology. 2009. Vol. 59, № 12. PP. 3035-3039.

Hirota K., Nishita M., Matsuyama H., Yumoto I. Paralkalibacillus indicireducens gen., nov., sp. nov., an indigo-reducing obligate alkaliphile isolated from indigo fermentation liquor used for dyeing // International journal of systematic and evolutionary microbiology. 2017. Vol. 67, № 10. PP. 4050-4056.

Yumoto I., Yamaga S., Sogabe Y., Nodasaka Y., Matsuyama H., Nakajima K., Suemori A. Bacillus krulwichiae sp. nov., a halotolerant obligate alkaliphile that utilizes benzoate and m-hydroxybenzoate // International journal of systematic and evolutionary microbiology. 2003. Vol. 53, № 5. PP. 1531-1536.

Krishna P., Raghunathan S., Prakash J.Comparative genome analysis of Alkalihalobacillus okhensis Kh10-101T reveals insights into adaptive mechanisms for halo-alkali tolerance // 3 Biotech. 2021. Vol. 11. PP. 1-18.

Joshi A., Thite S., Karodi P., Joseph N., Lodha T. Alkalihalobacterium elongatum gen. nov. sp. nov.: an antibiotic-producing bacterium isolated from Lonar Lake and reclassification of the genus Alkalihalobacillus into seven novel genera // Frontiers in microbiology. 2021. Vol. 12. P. 722369.

Kumar A.G., Rajan N.N., Kirubagaran R., Dharani G. Biodegradation of crude oil using self-immobilized hydrocarbonoclastic deep sea bacterial consortium // Marine pollution bulletin. 2019. Vol. 146. PP. 741-750.

Hirota K., Aino K., Nodasaka Y., Yumoto I. Oceanobacillus indicireducens sp. nov., a facultative alkaliphile that reduces an indigo dye // International journal of systematic and evolutionary microbiology. 2013. Vol. 63, № 4. PP. 1437-1442.

OuYang Y., Li M.M., Lv A.P., Jin P.J., Liu L., Liu Z.T., Wang S. Oceanobacillus saliphilus sp. nov., isolated from saline-alkali soil in Heilongjiang province, China // Current microbiology. 2022. Vol. 79, № 10. P. 301.

Yongchang O., Xiang W., Wang G. Oceanobacillus bengalensis sp. nov., a bacterium isolated from seawater of the Bay of Bengal // Antonie Van Leeuwenhoek. 2015. Vol. 108. PP. 1189-1196.

Zhu W.Y., Yang L., Shi Y.J., Mu C.G., Wang Y., Kou Y.R., Tang S.K. Oceanobacillus halotolerans sp. nov., a bacterium isolated from salt lake in Xinjiang province, north-west China // Archives of microbiology. 2020. Vol. 202. PP. 1545-1549.

Mandic-Mulec I., Stefanic P., van Elsas J.D. Ecology ofBacillaceae // The bacterial spore: from molecules to systems / eds by A. Driks, P. Eichenberger. New York: Wiley, 2016. PP. 59-85.

Liu G.H., Narsing Rao M.P., Chen Q.Q., Che J.M., Shi H., Liu B., Li W.J. Evansella halocellulosilytic a sp. nov., an alkali-halotolerant and cellulose-dissolving bacterium isolated from bauxite residue // Extremophiles. 2022. Vol. 26, № 2. P. 19. 10.1007/ s00792-022-01267-y.

List of Prokaryotic names with Standing in Nomenclature. URL: https://lpsn.dsmz.de (дата обращения: 14.07.2023).

EzBioCloud Database. Avaliable at: http://www.ezbiocloud.net (дата обращения: 14.07.2023).

The National Center for Biotechnology Information. URL: http://www.ncbi.nlm.nih.gov (дата обращения: 14.07.2023).

Tamura K, Stecher G., Kumar S. MEGA11: molecular evolutionary genetics analysis version 11 // Molecular biology and evolution. 2021. Vol. 38, № 7. PP. 3022-3027.

Lane D.J. 16S/23S rRNA sequencing // Nucleic acid techniques in bacterial systematic / eds by E. Stackebrandt, M. Goodfellow. N.Y.: John Wiley & Sons, 1991. P. 115-175.

Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. Short Protocols in molecular biology. New York: Wiley, 1995. 900 p.

Нетрусов А.И., Егорова М.А., Захарчук Л.М. Практикум по микробиологии: учеб. пособие для студ. высш. учеб. заведений. М.: Академия, 2005. 608 с.

Pfennig N., Biebl H. Desulfuromonas acetoxidans gen. nov. and sp. nov., a new anaerobic, sulfur-reducing, acetate-oxidizing bacterium // Archives of Microbiology. 1976. Vol. 110, № 1. PP. 3-12.

Chattopadhyay S., Sachan S. Biodegradation of polycyclic aromatic hydrocarbons and the impact of various genes for their enhanced degradation // Letters in applied microbiology. 2023. Vol. 76, № 2. P. ovac062.

Thacharodi A., Hassan S., Singh T., Mandal R., Khan H.A., Hussain M.A., Pugazhendhi A. Bioremediation of polycyclic aromatic hydrocarbons: an updated microbiological review // Chemosphere. 2023. Vol. 328. P. 138498.

Ястребова О.В., Пьянкова А.А., Плотникова Е.Г. Бактерии-деструкторы фталатов, выделенные из района промышленной добычи и переработки калийно-магниевых солей // Прикладная биохимия и микробиология. 2019. Т. 55, № 4. С. 378-385.

Yastrebova O.V., Plotnikova E.G., Ananina L.N., Demakov V.A. Aerobic spore-forming bacteria from the region of salt mining // Russian journal of ecology. 2009. Vol. 40. PP. 516-521.

Ястребова О.В., Плотникова Е.Г. Филогенетическое разнообразие бактерий семейства Micrococcaceae, выделенных из биотопов с различным антропогенным воздействием // Вестник Пермского университета. Серия: Биология. 2020. Т. 4. С. 321-333.

Плотникова Е.Г., Ястребова О.В., Корсакова Е.С., Пьянкова А.А., Ананьина Л.Н. Изучение бактерий-деструкторов моно(поли)ароматических соединений семейства Micrococcaceae, перспективных для разработки биотехнологий очистки промышленных территорий Пермского края // Вестник Пермского федерального исследовательского центра. 2022. № 2. С. 47-55.

Пьянкова А.А., Плотникова Е.Г. Бактерии-деструкторы бензойной кислоты семейства Halomonadaceae, выделенные из района солеразработок: видовое разнообразие и анализ benA-генов // Микробиология. 2022. Т. 91, № 1. С. 102-115.

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, № 2. С. 247247.

Нечаева Ю.И., Белкин П.А., Плотникова Е.Г. Анализ структуры микробных сообществ донных осадков техногенного водоема (г. Березники, Пермский край) // Симбиоз-Россия 2022: сборник статей XIII Международной конференции ученых-биологов (г. Пермь, ПГНИУ, 24-25 октября 2022 г.). Пермь, 2023. С. 833-837.

Martinez G.M., Pire C., Martinez-Espinosa R.M. Hypersaline environments as natural sources of microbes with potential applications in biotechnology: the case of solar evaporation systems to produce salt in Alicante County (Spain) // Current research in microbial sciences. 2022. Vol. 3. P. 100136.