L.R. Biktasheva*, A.A. Saveliev**, P.A. Kuryntseva***, S.Y. Selivanovskaya****, P.Y. Galitskaya*****
Kazan Federal University, Kazan, 420008 Russia
E-mail: *biktasheval@mail.ru, **polinazwerewa@yandex.ru, ***Anatoly.Saveliev.aka.saa@gmail.com,
****svetlana.selivanovskaya@kpfu.ru, *****gpolina33@yandex.ru
Received March 12, 2019
DOI: 10.26907/2542-064X.2019.2.255-274
For citation: Biktasheva L.R., Saveliev A.A., Kuryntseva P.A., Selivanovskaya S.Y., Galitskaya P.Y. Assessment of the number of catabolic genes of oil-contaminated soils. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki, 2019, vol. 161, no. 2, pp. 255–274. doi: 10.26907/2542-064X.2019.2.255-274. (In Russian)
Abstract
In this work, laboratory modeling of three levels of oil contamination (60, 120 and 250 g kg–1) was carried out for three types of soil: eutric podzoluvisols, haplic greyzem, and haplic chernozems. It was found that the content of fraction of aliphatic and aromatic hydrocarbons decreased in the samples with low and medium levels of contamination within 120 days. Oil contamination of soil in all concentrations led to a decrease in the total number of bacteria in comparison with uncontaminated soil by 1.2–5.5 times. It was shown that the number of genes belonging to the alkI and GP-PAH groups was in line with the total number of bacteria and decreased after oil contamination. At the same time, the number of alkane-monooxygenase genes belonging to the alkII and alkIII groups, as well as the genes of the GN-PAH group, was higher in the oil-contaminated soils as compared to the uncontaminated ones. Statistical analysis of the results showed that the level of soil contamination is a significant factor for the dynamics of the number of genes belonging to the alkI, alkII, GN-PAH, GP-PAH groups, as well as the duration of the experiment for alkI, alkIII, GN-PAH, GP-PAH groups. Soil type is a significant factor for the dynamics of the number of bacteria and number of genes belonging to the alkIII and GP-PAH groups. For other groups of genes, the type of soil is not a significant factor.
Keywords: oil-contaminated soils, biodegradation, alkane monooxygenase, dioxygenase
Acknowledgments. The study was supported by the Russian Science Foundation (project no. 17-7420183).
Figure Captions
Fig. 1. GC profile of extracted saturates fraction from the SL sample with oil concentration of 120 g kg-1 on the first (a) and 120th (b) day following the contamination.
Fig. 2. Number of bacteria in the soils of different types (a) and with different levels of oil contamination (b) on days 0, 30, 60, and 120 of the experiment (c). The vertical axis represents the number of copies of the genes, the middle of the rectangle represents the mean value, and the rectangle represents the extreme standard deviation.
Fig. 3. Number of genes encoding alkane monooxygenase (a, b, c – alkI group; d, e, f – alkII group; g, h, i – alkIII group) in the soils of different types and with different levels of contamination on days 0, 30, 60, and 120 of the experiment. The vertical axis represents the number of copies of the genes, the middle of the rectangle represents the mean value, the rectangle represents the extreme standard deviation, and the points represent the extremes or outliers.
Fig. 4. Number of genes encoding PAH degradation: a, b, c – genes of the GN-PAH group (gram-negative bacteria); d, e, f – genes of the GP-PAH group (gram-positive bacteria) in soils of different types and with different levels of contamination on days 0, 30, 60, and 120 of the experiment. Designations as in Fig. 3.
References
Liang Y., Zhang X., Wang J., Li G. Spatial variations of hydrocarbon contamination and soil properties in oil exploring fields across China. J. Hazard. Mater., 2012, vols. 241–242, pp. 371–378. doi: 10.1016/j.jhazmat.2012.09.055.
Zhang D.C., Mörtelmaier C., Margesin R. Characterization of the bacterial archaeal diversity in hydrocarbon-contaminated soil. Sci. Total Environ., 2012, vols 421–422, pp. 184–196. doi: 10.1016/j.scitotenv.2012.01.043.
Cappello S., Caruso G., Zampino D., Monticelli L.S., Maimone G., Denaro R., Tripodo B., Troussellier M.,Yakimov M., Giuliano L. Microbial community dynamics during assays of harbour oil spill bioremediation: A microscale simulation study. J. Appl. Microbiol., 2007, vol. 102, no. 1, pp. 184–194. doi: 10.1111/j.1365-2672.2006.03071.x.
Batista S.B., Mounteer A.H, Amorim F.R., Totola M.R. Isolation and characterization of biosurfactant/bioemulsifier-producing bacteria from petroleum contaminated sites. Bioresour. Technol., 2006, vol. 97, no. 6, pp. 868–875. doi: 10.1016/j.biortech.2005.04.020.
Watanabe K., Hamamura N. Molecular and physiological approaches to understanding the ecology of pollutant degradation. Curr. Opin. Biotechnol., 2003, vol. 14, no. 3, pp. 289–295. doi: 10.1016/s0958-1669(03)00059-4.
Margesin R., Labbé D., Schinner F., Greer C. W., Whyte L.G. Characterization of hydrocarbon-degrading microbial populations in contaminated and pristine Alpine soils. Appl. Environ. Microbiol., 2003, vol. 69, no. 6, pp. 3085–3092. doi: 10.1128/aem.69.6.3085-3092.2003.
Vitte I., Duran R., Hernandez-Raquet G., Mounier J., Jézéquel R., Bellet V., Balaguer P., Caumette P., Cravo-Laureau C. Dynamics of metabolically active bacterial communities involved in PAH and toxicity elimination from oil-contaminated sludge during anoxic/oxic oscillations. Appl. Microbiol. Biotechnol., 2013, vol. 97, no. 9, pp. 4199–4211. doi: 10.1007/s00253-012-4219-5.
Sun W., Sun X., Cupples A.M. Presence, diversity and enumeration of functional genes (bssA and bamA) relating to toluene degradation across a range of redox conditions and inoculum sources. Biodegradation, 2014, vol. 25, no. 2, pp. 189–203. doi: 10.1007/s10532-013-9651-4.
Sun W., Sun X., Cupples A.M. Identification of Desulfosporosinus as toluene-assimilating microorganisms from a methanogenic consortium. Int. Biodeterior. Biodegrad., 2014, vol. 88, pp. 13–19. doi: 10.1016/j.ibiod.2013.11.014.
Biktasheva L., Selivanovskaya S., Danilova N., Galitskaya P. Presence and expression of genes encoding hydrocarbon decomposition ability of microbes in different soil types sampled in Tatarstan republic (Russia). Proc. 18th Int. Multidiscip. Sci. GeoConf. SGEM 2018, 2018, book 18, pp. 149–154.
Fuentes S., Méndez V., Aguila P., Seeger M. Bioremediation of petroleum hydrocarbons: 98, no. 11, pp. 4781–4794. doi: 10.1007/s00253-014-5684-9.
Liu Q., Tang J., Bai Z., Hecker M., Giesy J.P. Distribution of petroleum degrading genes and factor analysis of petroleum contaminated soil from the Dagang Oilfield, China. Sci. Rep., 2015, vol. 5, art. 11068, pp. 1–12. doi: 10.1038/srep11068.
Wang W., Shao Z. Genes involved in alkane degradation in the alcanivorax hongdengensis strain A-11-3. Appl. Microbiol. Biotechnol., 2012, vol. 94, no. 2, pp. 437–448. doi: 10.1007/s00253-011-3818-x.
Nie Y., Liang J.L., Fang H., Tang Y.Q., Wu X.L. Characterization of a CYP153 alkane hydroxylase gene in a Gram-positive Dietzia sp. DQ12-45-1b and its “team role” with alkW1 in alkane degradation. Appl. Microbiol. Biotechnol., 2014, vol. 98, no. 1, pp. 163–173. doi: 10.1007/s00253-013-4821-1.
Táncsics A., Szoboszlay S., Kriszt B., Kukolya J., Baka E., Márialigeti K., Révész S. Applicability of the functional gene catechol 1,2-dioxygenase as a biomarker in the detection of BTEX-degrading Rhodococcus species. J. Appl. Microbiol., 2008, vol. 105, no. 4, pp. 1026–1033. doi: 10.1111/j.1365-2672.2008.03832.x.
Kiyohara H., Nagao K., Kouno K., Yano K. Phenanthrene-degrading phenotype of Alcaligenes faecalis AFK2. Appl. Environ. Microbiol., 1982, vol. 43, no. 2, pp. 458–461.
Wald J, Hroudova M., Jansa J., Vrchotova B., Macek T., Uhlik O. Pseudomonads rule degradation of polyaromatic hydrocarbons in aerated sediment. Front. Microbiol., 2015, vol. 6, art. 1268, pp. 1–13. doi: 10.3389/fmicb.2015.01268.
Guo G., Tian F., Effect of a bacterial consortium on the degradation of polycyclic aromatic hydrocarbons and bacterial community composition in Chinese soils. Int. Biodeterior. Biodegrad., 2017, vol. 123, pp. 56–62. doi: 10.1016/j.ibiod.2017.04.022.
Rehfuss M., Urban J. Alcaligenes faecalis subsp. phenolicus subsp. nov. a phenol-degrading, 28, no. 5, pp. 421–429. doi: 10.1016/j.syapm.2005.03.003.
Van Beilen J.B., Li Z., Duetz W.A., Smits T.H.M., Witholt B. Diversity of alkane hydroxylase systems in the environment. Oil Gas Sci. Technol., 2006, vol. 58, no. 4, pp. 427–440. doi: 10.2516/ogst:2003026.
Kohno T., Sugimoto, Y., Sei K., Mori K. Design of PCR primers and gene probes for general detection of alcane-degrading bacteria. Microbes Environ., 2002, vol. 17, no. 3, pp. 114–121. doi: 10.1264/jsme2.17.114.
Kahng H.Y., Malinverni J.C., Majko M.M., Kukor J.J. Genetic and functional analysis of the tbc operons for catabolism of alkyl- and chloroaromatic compounds in Burkholderia sp. Strain JS150. Appl. Environ. Microbiol., 2001, vol. 67, no. 10, pp. 4805–4816. doi: 10.1128/AEM.67.10.4805-4816.2001.
Zylstra G.J., Gibson D.T. Toluene degradation by Pseudomonas putida F1. Nucleotide sequence of the todC1C2BADE genes and their expression in Escherichia coli J. Biol. Chem., 1989, vol. 264, no. 25, pp. 14940–14946.
Furukawa K., Hirose J., Suyama A., Zainki T., Hayashida S. Gene components responsible for discrete substrate specificity in the metabolism of biphenyl (bph operon) and toluene (tod operon). J. Bacteriol., 1993, vol. 175, no. 16, pp. 5224–5232. doi: 10.1128/jb.175.16.5224-5232.1993.
Burlage R.S., Hooper S.W., Sayler G.S. The TOL (pWW0) catabolic plasmid. Appl. Environ. Microbiol., 1989, vol. 55, no. 6, pp. 1323–1328.
Harayama S., Rekik M. Comparison of the nucleotide sequences of the meta-cleavage pathway genes of TOL plasmid pWW0 from Pseudomonas putida with other meta-cleavage genes suggests that both single and multiple nucleotide substitutions contribute to enzyme evolution. MGG Mol. Gen. Genet., 1993, vol. 239, nos. 1–2, pp. 81–89. doi: 10.1007/bf00281605.
Kurkela S., Lehväslaiho H., Palva E.T., Teeri T.H. Cloning, nucleotide sequence and characterization of genes encoding naphthalene dioxygenase of Pseudomonas putida strain NCIB9816. Gene, 1988, vol. 73, no. 2, pp. 355–362. doi: 10.1016/0378-1119(88)90500-8.
Ferrero M., Llobet-Brossa E., Lalucat J., García-Valdés E., Rosselló-Mora R., Bosch R. Coexistence of two distinct copies of naphthalene degradation genes in Pseudomonas strains isolated from the western Mediterranean region. Appl. Environ. Microbiol., 2002, vol. 68, no. 2, pp. 957–962. doi: 10.1128/aem.68.2.957-962.2002.
Afzal M., Yousaf S., Reichenauer T.G., Kuffner M., Sessitsch A. Soil type affects plant colonization, activity and catabolic gene expression of inoculated bacterial strains during phytoremediation of diesel. J. Hazard. Mater., 2011, vol. 186, nos. 2–3, pp. 1568–1575. doi: 10.1016/j.jhazmat.2010.
Kireeva N.A., Bakaeva M.D., Tarasenko Е.М. Integrated biotesting for assessing soil contamination with oil. Ekol. Prom. Ross., 2004, no. 2, pp. 26–29. (In Russian)
Dominguez-Rosado E., Pichtel J., Coughlin M. Phytoremediation of soil contaminated with used motor oil: I. Enhanced microbial activities from laboratory and growth chamber studies. Environ. Eng. Sci., 2004, vol. 21, no. 2, pp. 157–168. doi: 10.1089/109287504773087336.
Schmidt N., Bolter M. Fungal and bacterial biomass in tundra soils along an arctic transect from Taimyr Peninsula, central Siberia. Polar Biol., 2002, vol. 25, no. 12, pp. 871–877. doi: 10.1007/s00300-002-0422-7.
Li X., Lin X., Li P., Liu W., Wang L., Ma F., Chukwuka K. S. Biodegradation of the low concentration of polycyclic aromatic hydrocarbons in soil by microbial consortium during incubation. J. Hazard. Mater., 2009, vol. 172, nos. 2–3, pp. 601–605. doi: 10.1016/j.jhazmat.2009.07.044.
Colloff M.J. Wakelin, S. A., Gomez, D., Rogers, S. L. Detection of nitrogen cycle genes in soils 7, pp. 1637–1645. doi: 10.1016/j.soilbio.2008.01.019.
Anderson T.H., Domsch K.H. Soil microbial biomass: The eco-physiological approach. Soil Biol. Biochem., 2010, vol. 42, no. 12, pp. 2039–2043. doi: 0.1016/j.soilbio.2010.06.026.
Uspenskii V.A. Rukovodstvo po analizu bitumov i rasseyannogo organicheskogo veshchestva gornykh porod [Handbook on Analysis of Bitumens and Dispersed Organic Matter in Rocks]. Leningrad, Nedra, 1966. 315 p. (In Russian)
Khusnutdinov I.Sh., Bukharov S.V., Goncharova I.N. Opredelenie soderzhaniya smolisto-asfal'tovykh veshchestv: Metod. ukazaniya [Determination of Tar-Asphalt Substances: Methodological Guidelines]. Kazan, Kazan. Gos. Tekhnol. Univ., 2006. 43 p. (In Russian)
Muyzer G., De Waal E.C., Uitterlinden A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol., 1993, vol. 59, no. 3, pp. 695–700.
Cébron A., Norini M.P., Beguiristain T., Leyval C. Real-Time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHDα) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J. Microbiol. Methods, 2008, vol. 73, no. 2, pp. 148–159. doi: 10.1016/j.mimet.2008.01.009.
R Core Team. R Development Core Team. R A Lang. Environ. Stat. Comput., 2013, vol. 55, pp. 275–286.
Jia J., Zong S., Hu L., Shi S., Zhai X., Wang B., Li G., Zhang D. The dynamic change of microbial communities in crude oil-contaminated soils from oil fields in China. Soil Sediment Contam., 2017, vol. 26, no. 2, pp. 171–183. doi: 10.1080/15320383.2017.1264923.
Fukuhara Y., Horii S., Matsuno T., Matsumiya Y., Mukai M., Kubo M. Distribution of hydrocarbon-degrading bacteria in the soil environment and their contribution to bioremediation. Appl. Biochem. Biotechnol., 2013, vol. 170, no. 2, pp. 329–339. doi: 10.1007/s12010-013-0170-x.
Rogozina E.A., Morgunov P.A., Timergazina I.F., Shapiro A.I. Biopreparations of the Naftox 2, pp. 1–14. Available at: http://www.ngtp.ru/rub/7/ 16_2013.pdf. (In Russian)
Sokolov S.N., Khadaev I.R. The influence of biological products to reduce the residual concentration of oil hydrocarbons in the soil. Mezhdunar. Nauchn.-Issled. Zh., 2017, no. 6, pt. 2, pp. 130–136. (In Russian)
Kang H., Gao H., Yu W., Yi Y., Wang Y., Ning M. Changes in soil microbial community structure and function after afforestation depend on species and age: Case study in a subtropical alluvial island. Sci. Total Environ., 2018, vol. 625, pp. 1423–1432. doi: 10.1016/j.scitotenv.2017.12.180.
Godbout J., Comeau Y., Greer C. Soil characteristics effects on introduced bacterial survival and 120. (In Russian)
Oudot J., Merlin F.X., Pinvidic P. Weathering rates of oil components in a bioremediation experiment in estuarine sediments. Mar. Environ. Res., 1998, vol. 45, no. 2, pp. 113–125. doi: 10.1016/S0141-1136(97)00024-X.
Morasch B., Annweiler, E., Warthmann, R.J., Meckenstock, R.U. The use of a solid adsorber resin for enrichment of bacteria with toxic substrates and to identify metabolites: Degradation of naphthalene, o-, and m-xylene by sulfate-reducing bacteria. J. Microbiol. Methods, 2001, vol. 44, no. 2, pp. 183–191. doi: 10.1016/S0167-7012(00)00242-6.
Galitskaya P., Biktasheva L., Selivanovskaya S. Response of soil microorganisms to radioactive oil waste: Results from a leaching experiment. Biogeosciences. 2015, vol. 12, no. 12, pp. 3681–3693. doi: 10.5194/bg-12-3681-2015.
Pérez-de-Mora A., Engel M., Schloter M. Abundance and diversity of n-alkane-degrading bacteria genes. Microb. Ecol., 2011, vol. 62, no. 4, pp. 959–972. doi: 10.1007/s00248-011-9858-z.
Yang Y., Wang J., Liao J., Xie S., Huang Y. Abundance and diversity of soil petroleum hydrocarbon-degrading microbial communities in oil exploring areas. Appl. Microbiol. Biotechnol., 2014, vol. 99, no. 4, pp. 1935–1946. doi: 10.1007/s00253-014-6074-z.
Zhang Z., Zhao X., Liang Y., Li G., Zhou J. Microbial functional genes reveal selection of 17. doi: 10.1007/s10311-012-0370-6.
Bengtsson G., Törneman N., de Lipthay J.R., Sørensen S.J. Microbial diversity and PAH catabolic genes tracking spatial heterogeneity of PAH concentrations. Microb. Ecol., 2013, vol. 65, no. 1, pp. 91–100. doi: 10.1007/s00248-012-0112-0.
Ding G.C., Heuer H., Zühlke S., Spiteller M., Pronk G., Heister K., Kögel-Knabner I. Smalla K. Soil type-dependent responses to phenanthrene as revealed by determining the diversity and abundance of polycyclic aromatic hydrocarbon ring-hydroxylating dioxygenase genes by using a novel PCR detection system. Appl. Environ. Microbiol., 2010, vol. 76, no. 14, pp. 4765–4771. doi: 10.1128/AEM.00047-10.
Leys N.M., Ryngaert A., Bastiaens L., Wattiau P., Top E.M., Verstraete W., Springael D. Occurrence and community composition of fast-growing Mycobacterium in soils contaminated with polycyclic aromatic hydrocarbons. FEMS Microbiol. Ecol., 2005, vol. 51, no. 3, pp. 375–388. doi: 10.1016/j.femsec.2004.09.015.
The content is available under the license Creative Commons Attribution 4.0 License.