Thermophilic aerobic organoheterotrophic soil bacteria from anthropogenically changed territories of Saint Petersburg and Leningrad region

Cover Page

Cite item

Full Text

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

Abstract

Anthropogenically altered soils of Saint Petersburg and Luga (Leningrad Region) were investigated for the presence of thermophilic aerobic chemoorganoheterotrophic bacteria, potentially capable of decomposing hydrocarbons at elevated temperatures (60°C). 6 strains of pure spore-forming cultures of bacteria were isolated. Analysis of the nucleotide sequences of the 16S rRNA genes showed that they belong to the genera Geobacillus and Aeribacillus. For the first time, we obtained information on the presence of representatives of the genus Aeribacillus, which are typical inhabitants of hot springs and zones with geothermal activity, in the soils of the regions of Saint Petersburg and the Leningrad Region.

About the authors

Anna S. Zhuravleva

Agrophysical Research Institute

Author for correspondence.
Email: zhuravlan@gmail.com
ORCID iD: 0000-0001-7204-9653

junior researcher, PhD student

Russian Federation, 14 Grazhdanskiy pr., Saint Petersburg, 195220

Elena N. Volkova

Saint Petersburg State University of Industrial Technologies and Design, Higher School of Technology and Energy

Email: ele-ven@yandex.ru
ORCID iD: 0000-0001-7429-4046

Dr. Sci. (Agriculture), Professor

Russian Federation, Saint Petersburg

Alexander S. Galushko

Agrophysical Research Institute

Email: galushkoas@inbox.ru
ORCID iD: 0000-0002-0387-7997

PhD, Cand. Sci. (Biol.), Leading Researcher

Russian Federation, 14 Grazhdanskiy pr., Saint Petersburg, 195220

References

  1. Panicker G, Aislabie J, Saul D, Bej AK. Cold tolerance of Pseudomonas sp. 30–3 isolated from oil-contaminated soil, Antarctica. Polar Biol. 2002;25:5–11.
  2. Andreolli M, Albertarelli N, Lampis S, et al. Bioremediation of diesel contamination at an underground storage tank site: a spatial analysis of the microbial community. World J Microbiol Biotechnol. 2016;32:6.
  3. Yan L, Sinkko H, Penttinen P, Lindström K. Characterization of successional changes in bacterial community composition during bioremediation of used motor oil-contaminated soil in a boreal climate. Science of the Total Environment. 2016;542:817–825. doi: 10.1016/j.scitotenv.2015.10.144
  4. Kim DD, O’Farrell C, Toth CRA., et al. Microbial community analyses of produced waters from high-temperature oil reservoirs reveal unexpected similarity between geographically distant oil reservoirs. Microb Biotechnol. 2018;11(4):788–796. doi: 10.1111/1751-7915.13281
  5. Bonch-Osmolovskaja E.A. Termofil’nye mikroorganizmy: obshhij vzgljad. Trudy In-ta mikrobiologii im. S.N. Vinogradskogo. М.: MAKS Press, 2011. P. 5–14. (In Russ.)
  6. Wiegel J. Anaerobic alkalithermophiles, a novel group of extremophiles. Extremophiles. 1998;2:257–267.
  7. Chamkha M, Mnif S, Sayadi S. 2008. Isolation of a thermophilic and halophilic tyrosol-degrading Geobacillus from a Tunisian hightemperature oil field. FEMS Microbiol Lett. 2008;283:23–29. doi: 10.1111/j.1574-6968.2008.01136.x
  8. Saw JH, Mountain BW, Feng L, et al. Encapsulated in silica: genome, proteome and physiology of the thermophilic bacterium Anoxybacillus flavithermus WK1. Genome Biol. 2008;9: R161. doi: 10.1186/gb-2008-9-11-r161
  9. Adiguzel A, Ozkan H, Baris O, et al. Identification and characterization of thermophilic bacteria isolated from hot springs in Turkey. J Microbiol Methods. 2009;79(3):321–328. doi: 10.1016/j.mimet.2009.09.026
  10. Miñana-Galbis D, Pinzón DL, Loren JG, Manresa A, Oliart-Ros RM. Reclassification of Geobacillus pallidus (Scholz et al. 1988) Banat et al. 2004 as Aeribacillus pallidus gen. nov., comb. nov. Int J Syst Evol Microbiol. 2010;60:1600–1604.
  11. Pinzón-Martínez DL, Rodríguez-Gómez C, Miñana-Galbis D, et al. Thermophilic bacteria from Mexican thermal environments: isolation and potential applications. Environ Technol. 2010;31(8–9):957–966. doi: 10.1080/09593331003758797
  12. Yasawong M, Areekit S, Pakpitchareon A, et al. 2011. Characterization of thermophilic halotolerant Aeribacillus pallidus TD1 from Tao Dam Hot Spring, Thailand. Int J MolSci. 2011;12(8):5294–5303. doi: 10.3390/ijms12085294
  13. Zheng C, He J, Wang Y, et al. Hydrocarbon degradation and bioemulsifier production by thermophilic Geobacillus pallidus strains. Bioresour Technol. 2011;102;(9155–9161).
  14. Inan K, Belduz AO, Canakci S. Anoxybacillus kaynarcensis sp. nov., a moderately thermophilic, xylanase producing bacterium. J Basic Microbiol. 2013;53:410–419.
  15. Radchenkova N, Vassilev S, Panchev I, et al. Production and properties of two novel exopolysaccharides synthesized by a thermophilic bacterium Aeribacillus pallidus 418. Appl Biochem Biotechnol. 2013;171:31–43. doi: 10.1007/s12010-013-0348-2
  16. Cihan AC, Cokmus C, Koc M, Ozcan B. Anoxybacillus calidus sp. nov., a thermophilic bacterium isolated from soil near a thermal power plant. Int J Syst Evol Microbiol. 2014;64:211–219.
  17. Palanisamy N, Ramya J, Kumar S, et al. Diesel biodegradation capacities of indigenous bacterial species isolated from diesel contaminated soil. J Environ Heal Sci Eng. 2014;12:1–8. doi: 10.1186/s40201-014-0142-2
  18. Bryanskaya AV, Rozanov AS, Slynko NM, et al. Geobacillus icigianus sp. nov., a thermophilic bacterium isolated from a hot spring. Int J Syst Evol Microbiol. 2015;65:864–869. doi: 10.1099/ijs.0.000029
  19. Delegan JA, Vetrova AA, Chernjavskaja MI, et al. Termotolerantnye aktinomicety kak agenty remediacii neftezagrjaznennyh gruntov i vod v uslovijah zharkogo aridnogo klimata. Izvestiya Tula State University. 2015(4):248–258. (In Russ.)
  20. Filippidou S., Jaussi M., Junier T., et al. Genome sequence of Aeribacillus pallidus strain GS3372, an endospore-forming bacterium isolated in a deep geothermal reservoir. Genome Announc. 2015;3(4); e00981–15. doi: 10.1128/genomeA.00981-15
  21. Delegan JA. Termotolerantnye bakterii-destruktory uglevodorodov nefti [dissertation]. Pushchino: Pushchino State Institute of Natural Science, 2016. (In Russ.) Available from: https://dlib.rsl.ru/01008734496.
  22. Mesbaiah FZ, Eddouaouda K, Badis A, et al. Preliminary characterization of biosurfactant produced by a PAH-degrading Paenibacillus sp. under thermophilic conditions. Environ Sci Pollut Res. 2016;23:14221–14230. doi: 10.1007/s11356-016-6526-3
  23. Poltaraus AB, Sokolova DS, Grouzdev DS, et al. Draft genome sequence of Aeribacillus pallidus strain 8m3, a thermophilic hydrocarbon-oxidizing bacterium isolated from the Dagang oil field (China). Genome Announc. 2016;4(3): e00500–16. doi: 10.1128/genomeA.00500-16
  24. Poltaraus AB, Sokolova DS, Grouzdev DS, et al. Draft genome sequence of Geobacillus subterraneus strain K, a hydrocarbon-oxidizing thermophilic bacterium isolated from a petroleum reservoir in Kazakhstan. Genome Announc. 2016;4(4): e00782–16. doi: 10.1128/genomeA.00782-16
  25. Pugazhendi A, Wazin HA, Qari H, et al. Biodegradation of low and high molecular weight hydrocarbons in petroleum refinery wastewater by a thermophilic bacterial consortium. Environ Tech. 2016:2381–2391. doi: 10.1080/09593330.2016.1262460
  26. Nazina TN, Shestakova NM, Semenova EM, et al. Diversity of metabolically active bacteria in water-flooded high-temperature heavy oil reservoir. Front Microbiol. 2017;8:707. doi: 10.3389/fmicb.2017.00707
  27. Khan IU, Habib N, Xiao M, et al. Anoxybacillus sediminis sp. nov., a novel moderately thermophilic bacterium isolated from a hot spring. Antonie Van Leeuwenhoek. 2018;111(12):2275–2282. doi: 10.1007/s10482-018-1118-5
  28. Panosyan H, Di Donato P, Poli A, Nicolaus B. Production and characterization of exopolysaccharides by Geobacillus thermodenitrificans ArzA-6 and Geobacillus toebii ArzA-8 strains isolated from an Armenian geothermal spring. Extremophiles. 2018;22(5): 725–737. doi: 10.1007/s00792-018-1032-9
  29. Radchenkova N, Vassilev S, Panchev I, et al. Production and properties of two novel exopolysaccharides synthesized by a thermophilic bacterium Aeribacillus pallidus 418. Appl Biochem Biotechnol. 2013;171:31–43. doi: 10.1007/s12010-013-0348-2
  30. Yadav P, Korpole S, Prasad GS, et al. Morphological, enzymatic screening, and phylogenetic analysis of thermophilic bacilli isolated from five hot springs of Myagdi, Nepal. J Appl Biol Biotechnol. 2018;6(3):1–8. doi: 10.7324/JABB.2018.60301
  31. Mantiri FR, Rumende RRH, Sudewi S. Identification of α-amylase gene by PCR and activity of thermostable α-amylase from thermophilic Anoxybacillus thermarum isolated from Remboken hot spring in Minahasa, Indonesia. IOP Conf. Ser.: Earth Environ. 2019;217:012045. doi: 10.1088/1755-1315/217/1/012045
  32. Mechri S, Bouacem K, ZaraîJaouadi N, et al. Identification of a novel protease from the thermophilic Anoxybacillus kamchatkensis M1V and its application as laundry detergent additive. Extremophiles. 2019;23:687–706. doi: 10.1007/s00792-019-01123-6
  33. Elumalai P, Parthipan P, Narenkumar J et al. Role of thermophilic bacteria (Bacillus and Geobacillus) on crude oil degradation and biocorrosion in oil reservoir environment. 3 Biotech. 2019;9:79. doi: 10.1007/s13205-019-1604-0
  34. Yamprayoonswat W, Sittihan S, Jumpathong W, Yasawonga M. Draft genome sequence of thermophilic halotolerant Aeribacillus pallidus TD1, isolated from Tao Dam hot spring, Thailand. Microbiol. 2019;8(17): e00204–19. doi: 10.1128/MRA.00204-19
  35. Harirchi S, Etemadifar Z, Mahboubi A, et al. The efect of calcium/magnesium ratio on the biomass production of a novel thermoalkaliphilic Aeribacillus pallidus strain with highly heat-resistant spores. Curr Microbiol. 2020;77:2565–2574. doi: 10.1007/s00284-020-02010-6
  36. Miyazaki K, Hase E, Tokito N. Complete genome sequence of Geobacillus sp. strain E55-1, isolated from mine geyser in Japan. Microbiol Resour Announc. 2020;9: e00339–20. doi: 10.1128/MRA.00339-20
  37. Puopolo R, Gallo G, Mormone A, et al. Identification of a new heavy-metal-resistant strain of Geobacillus stearothermophilus isolated from a hydrothermally active volcanic area in southern Italy. Int J Environ Res Public Health. 2020;17(8):2678. doi: 10.3390/ijerph17082678
  38. Delegan JA, Vetrova AA, Akimov VN, et al. Thermotolerant oil-degrading bacteria isolated from soil and water of geographically distant regions. Applied biochemistry and microbiology. 2016;52(4):383–391. (In Russ.) doi: 10.7868/S0555109916040024
  39. Volkova EN, Zdorovceva AG, Galushko AS. Poisk termofil’nyh nefterazrushajushhih pochvennyh bakterij na meste nesankcionirovannoj svalki na okraine g. Sankt-Peterburga. Proceedings of the National Scientific and Practical Conference dedicated to the memory of Doctor of Medical Sciences, Professor L.F. Zykin “Zykinskie chtenija”. Larionova OS, Sazonova IA, eds. Saratov: Saratovskij GAU, 2020. P. 41–46. (In Russ.)
  40. Portillo MC, Santana M, Gonzalez JM. Presence and potential role of thermophilic bacteria in temperate terrestrial environments. Naturwissenschaften. 2012;99:43–53. doi: 10.1007/s00114-011-0867-z
  41. Dorzhiev SS, Bazarova EG, Rosenblum MI. Jekologicheskij karkas dlja optimizacii teplovogo rezhima pochvy na aridnyh territorijah. Proceedings of the Russian science conference “Jekologija: vchera, segodnja, zavtra”. 2019:155–160. (In Russ.)
  42. Makhatkov I.D., Ermolov Y.V. The thermal regime of active layer of pit-covered terrain in northern taiga. Mezhdunarodnyj zhurnal prikladnyh i fundamental’nyh issledovanij. 2015(11–3):400–407. (In Russ.)
  43. Wong ML, An D, Caffrey SM, et al. Roles of thermophiles and fungi in bitumen degradation in mostly cold oil sands outcrops. Appl Environ Microbiol. 2015;81:6825–6838.
  44. Shkadova AK. Temperaturnyj rezhim pochv na territorii SSSR. Leningrad; 1979: P. 75–81. (In Russ.)
  45. Marchik TP, Efremov AL. Pochvovedenie s osnovami rastenievodstva. Grodno: GrGU, 2006. 249 p. (In Russ.)
  46. Skvortsova IV, Berezutski MA. Railway embankment flora in the southern Volga height. Povolzhskij jekologicheskij zhurnal. 2008(1):55–64. (In Russ.)
  47. Sudakova SS. Features of railway flora of Ulynovsk Region. I. Yakovlev Chuvash State Pedagogical University Bulletin. 2013;2(78):150–154. (In Russ.)
  48. Voroshilova AA, Dianova EV. Okisljajushhie neft’ bakterii — pokazateli intensivnosti biologicheskogo okislenija nefti v prirodnyh uslovijah. Mikrobiologiya. 1952; ХХI(4):408–415. (In Russ.)
  49. Palatinszky M, Herbold C, Jehmlich N, et al. Cyanate as an energy source for nitrifiers. Nature. 2015;524:105–108. doi: 10.1038/nature14856
  50. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10:512–526.
  51. Chevenet F, Brun C, Banuls AL, et al. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics. 2006;7:439. doi: 10.1186/1471-2105-7-439
  52. Dereeper A, Guignon V, Blanc G, et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008;36(2):465–469. doi: 10.1093/nar/gkn180
  53. Dereeper A, Audic S, Claverie JM, Blanc G. BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol. 2010;10:8. doi: 10.1186/1471-2148-10-8
  54. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;(5):1792–1797. doi: 10.1093/nar/gkh340
  55. Finore I, Gioiello A, Leone L, et al. Aeribacillus composti sp. nov., a thermophilic bacillus isolated from olive mill pomace compost. Int J Syst Evol Microbiol. 2017;67:4830–4835. doi: 10.1099/ijsem.0.002391
  56. Zheng C, Li Z, Su J, et al. Characterization and emulsifying property of a novel bioemulsifier by Aeribacillus pallidus YM-1. J Appl Microbiol. 2012;13(44–51). doi: 10.1111/j.1365-2672.2012.05313.x
  57. Mnif S, Sayadi S, Chamkha M. Biodegradative potential and characterization of a novel aromatic-degrading bacterium isolated from a geothermal oil field under saline and thermophilic conditions. Int Biodeterior Biodegradation. 2014;86(C):258–264. doi: 10.1016/j.ibiod.2013.09.015
  58. Mehetre GT, Dastager SG, Dharne MS. Biodegradation of mixed polycyclic aromatic hydrocarbons by pure and mixed cultures of biosurfactant producing thermophilic and thermo-tolerant bacteria. Sci Total Environ. 2019;679:52–60. doi: 10.1016/j.scitotenv.2019.04.376
  59. Tao W, Lin J, Wang W, et al. Biodegradation of aliphatic and polycyclic aromatic hydrocarbons by the thermophilic bioemulsifier-producing Aeribacillus pallidus strain SL-1. Ecotoxicol Environ Saf. 2020;189:1–9. doi: 10.1016/j.ecoenv.2019.109994
  60. Wang L, Tang Y, Wang S, et al. Isolation and characterization of a novel thermophilic Bacillus strain degrading long-chain n-alkanes. Extremophiles. 2006;10(4):347–356. doi: 10.1007/s00792-006-0505-4
  61. Mechri S, Berrouina MBE, Benmrad M O, et al. Characterization of a novel protease from Aeribacillus pallidus VP3 with potential biotechnological interest. Int J Biol Macromol. 2017;94(A):221–232. doi: 10.1016/j.ijbiomac.2016.09.112
  62. Nazina TN, Lebedeva EV, Poltaraus AB, et al. Geobacillus gargensis sp. nov., a novel thermophile from a hot spring, and the reclassification of Bacillus vulcani as Geobacillus vulcani comb. nov. Int J Syst Evol Microbiol. 2004;(6):2019–2024. doi: 10.1099/ijs.0.02932-0
  63. Rozanov AS, Logacheva MD, Peltek SE. Draft genome sequences of Geobacillus stearothermophilus strains 22 and 53, isolated from the Garga hot spring in the Barguzin river valley of the Russian Federation. Genome Announc. 2014;2(6): e01205–14. doi: 10.1128/genomeA.01205-14
  64. Junicyna OA, Kisil’ OJ, Rudakova VA. Termofil’nye bakterii, vydelennye iz othodov lesopilenija, — producenty ksilanoliticheskih i amiloliticheskih fermentov. Proceedings of the Russian science conference “Tehnologii i oborudovanie himicheskoj, biotehnologicheskoj i pishhevoj promyshlennosti”; May 22–24 2019. Bijsk. P. 433–437. (In Russ.)
  65. Ahtemova GA. Izmenenie struktury mikrobnogo kompleksa pochvy pri ispol’zovanii produktov pererabotki stokov svinootkormochnyh predprijatij v kachestve udobrenija [dissertation]. Saint Petersburg: VNI ISM, 1998. 22 p. (In Russ.) Available from: https://dlib.rsl.ru/01000796688.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. General view of cells and spores: a – L1, b – L2-1, c – L2-2, d – L2-3, e – K2-2, f – K6

Download (216KB)
Indexing metadata
3. Fig. 2. Growth curve of a bacterial culture K2-2 in a liquid VD medium with sodium acetate and without an organic substrate for 2.5 days. OD, optical density of the culture

Download (119KB)
Indexing metadata
4. Fig. 3. Curve of the change in the optical density of the bacterial culture K6 in VD medium with sodium acetate and without an organic substrate for 2.5 days. OD, optical density of the culture

Download (122KB)
Indexing metadata
5. Fig. 4. Phylogenetic tree of closely related strains obtained by applying the neighbor-join and BioNJ algorithms to the matrix of pairwise distances [50–54]. Branch length is presented to scale and is measured by the number of nucleotide substitutions per site

Download (502KB)
Indexing metadata

Copyright (c) 2021 ООО "Эко-Вектор"


 


This website uses cookies

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

About Cookies