2025 Ecosystem Transformation 8 (4), 189-204

Bioremediation of oil-contaminated soil containing elevated concentrations of sodium chloride and heavy metals

Kuzina E.V. , Mukhamatdyarova S.R., Iskuzhina M.G., Sharipova Yu.Yu., Korshunova T.Yu.

The study of the effect of heavy metals and sodium chloride on the oxidative activity of oil
destructor strains of the genus Acinetobacter showed that the bacteria retain the ability to biodegrade
oil at concentrations of lead and zinc ions up to 1000 and 125 mg/l, respectively, and sodium chloride
up to 3% by weight. The presence of oil (5% by volume) and sodium chloride (3% by weight) did not
affect the synthesis of indolyl-3-acetic acid by microorganisms, the addition of lead and zinc salts to the
nutrient medium stimulated the production of this phytohormone. In a model experiment, the possibility
of using Acinetobacter strains, as well as associations of these bacteria and barley plants, to restore soils
contaminated with oil (50 g/kg), also including (together with other pollutants): lead (200 mg/kg), zinc
(300 mg/kg), and sodium chloride (5 g/kg). The introduction of Acinetobacter strains into contaminated
soil increased the mass of barley shoots by 20.8–38.9% compared with untreated plants. When the
soil was contaminated with oil alone, due to bacterization, the root mass increased by 11.7–23.1%,
and when contaminated with oil and heavy metals – by 23.2–33.5%. In the presence of lead, zinc and
sodium chloride, the efficiency of hydrocarbon biodegradation turned out to be higher than in the variant
where the soil was contaminated only with oil. During 70 days of the experiment, with the combined
use of plants and bacteria, the oil content in the soil decreased from 50.0 g/kg to 8.0–10.5 g/kg of soil.

E. V. Kuzina
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences
Prospekt Oktyabrya St. 69, lit. E, Ufa, 450054 Russia

lab.biotech@yandex.ru

S. R. Mukhamatdyarova
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences
Prospekt Oktyabrya St. 69, lit. E, Ufa, 450054 Russia


M. G. Iskuzhina
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences
Prospekt Oktyabrya St. 69, lit. E, Ufa, 450054 Russia


Yu. Yu. Sharipova
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences
Prospekt Oktyabrya St. 69, lit. E, Ufa, 450054 Russia


T. Yu. Korshunova
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences
Prospekt Oktyabrya St. 69, lit. E, Ufa, 450054 Russia

Angulo-Bejarano, P.I., Puente-Rivera, J., Cruz-Ortega, R., 2021. Metal and metalloid toxicity in plants:
An overview on molecular aspects. Plants 10 (4), 635. https://doi.org/10.3390/plants10040635
Anokhina, T.O., Siunova, T.V., Sizova, O.I., Zakharchenko, N.S., Kochetkov, V.V., 2018. Rizosfernye
bakterii roda Pseudomonas v sovremennykh agrobiotekhnologiiakh [Rhizospheric bacteria of the
genus Pseudomonas in modern agrobiotechnology]. Agrokhimiia [Agrochemistry] 10, 54–66. (In
Russian). http://www.doi.org/10.1134/S0002188118100034
Babayev, E.R., Farzaliyev, V.M., Mamedova, P.Sh., Movsumzadeh, E.M., 2015. Biologicheskaia
utilizatsiia tiazhelykh metallov [Biological utilization of heavy metals]. Neftegazokhimiia [Oil and Gas
Chemistry] 4, 49–51. (In Russian).
Borzenkov, I.A., Milekhina, E.I., Gotoeva, M.T., Rozanova, E.P., Belyaev, S.S., 2006. Svoistva
uglevodorodokisliaiushchikh bakterii, izolirovannykh iz neftianykh mestorozhdenii Tatarstana,
Zapadnoi Sibiri i V'etnama [The properties of hydrocarbon-oxidizing bacteria isolated from the oilfields
of Tatarstan, Western Siberia, and Vietnam]. Mikrobiologiia [Microbiology] 75 (1), 82–89. (In Russian).
Buzoleva, L.S., Krivosheeva, A.M., 2013. Vliianie tiazhelykh metallov na razmnozhenie patogennykh
bakterii [Effects of heavy metals on pathogenic bacteria]. Uspekhi sovremennogo estestvoznaniia
[Advances in Current Natural Sciences] 7, 30–33. (In Russian).
Camacho-Montealegre, C.M., Rodrigues, E.M., Morais, D.K., Tótola, M.R., 2021. Prokaryotic community
diversity during bioremediation of crude oil contaminated oilfield soil: effects of hydrocarbon
concentration and salinity. Brazilian Journal of Microbiology 52, 787–800. https://doi.org/10.1007/
s42770-021-00476-5
Domracheva, L.I., Skugoreva, S.G., Kovina, A.L., Korotkikh, A.I., Starikov, P.A. et al., 2022. Spetsifika
rastitel'no-mikrobnykh kompleksov pri antropogennom zagriaznenii pochvy (obzor) [Specificity of
plant-microbial complexes under anthropogenic soil pollution (review)]. Teoreticheskaia i prikladnaia
ekologiia [Theoretical and Applied Ecology] 3, 14–25. (In Russian). http://www.doi.org/10.25750/1995-
4301-2022-3-014-025
Dzerzhinskaya, I.S., 2008. Pitatel'nye sredy dlia vydeleniia i kul'tivirovaniia mikroorganizmov [Nutrient
media for isolation and cultivation of microorganisms]. Astrakhan State Technical University, Astrakhan,
Russia, 348 p. (In Russian).
El-Agawany, N.I., Kaamoush, M.I., 2023. Role of zinc as an essential microelement for algal growth and
concerns about its potential environmental risks. Environmental Science and Pollution Research 30
(28), 71900–71911. https://doi.org/10.1007/s11356-022-20536-z
Fedorova, Yu.A., Chiglintseva, N.N., Yagafarova, G.G., Yagafarova, D.I., Safarov, A.H., 2015. Podbor
fitomeliorantov dlia rekul'tivatsii neftezasolennykh pochv [Selection of phytoameliorants for recultivation
of the petrosalted soils]. Vestnik Permskogo natsional'nogo issledovatel'skogo politekhnicheskogo
universiteta. Prikladnaia ekologiia. Urbanistika (Bulletin of Perm National Research Polytechnic
University. Applied Ecology. Urban Development] 3 (19), 60–68. (In Russian).
Golovin, A.V., Skrypnik, L.N., Masyutin, Ya.A., 2021. Osobennosti nakopleniia tsinka i nikelia nekotorymi
lekarstvennymi rasteniiami, proizrastaiushchimi na territoriiakh s razlichnoi stepen'iu tekhnogennoi
nagruzki [Particularities of zinc and nickel accumulation by certain medicinal plants in territories with
varying degrees of technological load]. Ekosistemy [Ecosystems] 26, 67–77. (In Russian).
Jiao, S., Chen, W., Wei, G., 2019. Resilience and assemblage of soil microbiome in response to
chemical contamination combined with plant growth. Applied and Environmental Microbiology 85 (6),
e02523-18. https://doi.org/10.1128/AEM.02523-18
Kallas, E.V., Maron, T.A., 2018. Melioratsiia zasolennykh pochv i metody ikh izucheniia [Reclamation of
saline soils and methods of their study]. Publishing House of Tomsk State University, Tomsk, Russia,
138 p. (In Russian).
Klimova, T.A., Barysheva, E.S., 2017. Znachenie essentsial'nykh elementov v zhiznedeiatel'nosti
mikroorganizmov [The importance of essential elements in the vital activity of microorganisms]. Tezisy
dokladov Vserossiiskoi nauchno-metodicheskoi konferentsii Orenburgskogo gosudarstvennogo
universiteta «Universitetskii kompleks kak regional'nyi tsentr obrazovaniia, nauki i kul'tury» [Abstracts
of the All-Russian Scientific and methodological conference of Orenburg State University "University
complex as a regional center of education, science and culture"]. Orenburg, Russia, 1925–1929. (In
Russian).
Khalid, S., Shahid, M., Niazi, N.K., Murtaza, B., Bibi, I. et al., 2017. A comparison of technologies for
remediation of heavy metal contaminated soils. Journal of Geochemical Exploration 182, 247–268.
https://doi.org/10.1016/j.gexplo.2016.11.021
Khudur, L.S., Gleeson, D.B., Ryan, M.H., Shahsavari, E., Haleyur, N. et al., 2018. Implications of cocontamination with aged heavy metals and total petroleum hydrocarbons on natural attenuation
and ecotoxicity in Australian soils. Environmental Pollution 243, 94–102. https://doi.org/10.1016/j.
envpol.2018.08.040
Korshunova, T.Yu., Kuzina, E.V., Mukhamatdyarova, S.R., Sharipova, Yu.Yu., Iskuzhina, M.G.,
2024. Bakterii-destruktory s roststimuliruiushchimi svoistvami dlia ispol'zovaniia v ekologicheskoi
biotekhnologii [Bacteria-destructors with growth-stimulating properties for use in ecological
biotechnology]. Teoreticheskaia i prikladnaia ekologiia [Theoretical and Applied Ecology] 2, 117–124.
(In Russian). http://www.doi.org/10.25750/1995-4301-2024-2-117-124
Kuzina, E., Rafikova, G., Vysotskaya, L., Arkhipova, T., Bakaeva, M. et al., 2021. Influence of
hydrocarbon-oxidizing bacteria on the growth, biochemical characteristics, and hormonal status of
barley plants and the content of petroleum hydrocarbons in the soil. Plants 10 (8), 1745. http://www.
doi.org/10.3390/plants10081745
Kuzina, E.V., Rafikova, G.F., Mukhamatdyarova, S.R., Sharipova, Yu.Yu., Korshunova, T.Yu., 2023.
Biologicheskaia aktivnost' chernozema vyshchelochennogo pri neftianom i khloridno-natrievom
zagriaznenii i vliianie na nee obrabotki galotolerantnymi bakteriiami-neftedestruktorami [Biological
activity of leached chernozem under oil and sodium chloride pollution and the effect of treatment with
halotolerant oil-destructing bacteria]. Pochvovedenie [Eurasian Soil Science] 1, 89–101. (In Russian).
http://www.doi.org/10.31857/S0032180X22600718
Lebedeva, L.A., Arzamazova, A.V., 2010. Vliianie agrokhimicheskikh sredstv na postuplenie svintsa v rasteniia iachmenia pri zagriaznenii dernovo-podzolistoi pochvy etim metallom [The influence of
agrochemicals on the intake of lead into barley plants during contamination of sod-podzolic soil with this
metal.] Problemy agrokhimii i ekologii [Agrochemistry and Ecology Problems] 2, 22–26. (In Russian).
Li, Y., Li, C., Xin, Y., Huang, T., Liu, J., 2022. Petroleum pollution affects soil chemistry and reshapes the diversity and networks of microbial communities. Ecotoxicology and Environmental Safety 246,
114129. https://doi.org/10.1016/j.ecoenv.2022.114129
Mukhamatdyarova, S.R., Kuzina, E.V., Sharipova, Yu.Yu., Iskuzhina, M.G., Kulbaeva, L.A., Korshunova,
T.Yu., 2024. Biotekhnologicheskii potentsial novykh shtammov uglevodorodokisliaiushchikh bakterii
[Biotechnological potential of new strains of hydrocarbon-oxidizing bacteria]. Izvestiia Ufimskogo
nauchnogo tsentra RAN [Proceedings of the RAS Ufa Scientific Centre] 2, 38‒47. (In Russian). http://www.doi.org/10.31040/2222-8349-2024-0-2-38-47
Nosova, M.V, Seredina, V.P., Stovbunik, S.A., 2023. Assessment of soil changes causing contamination
with crude oil and mineralized liquids in the Middle Ob region (Western Siberia). Ecosystem
transformation 6 (2 (20)), 64‒73. http://www.doi.org/10.23859/estr-220718
Patel, M., Surti, M., Ashraf, S.A., Adnan, M., 2021. Physiological and molecular responses to heavy
metal stresses in plants. In: Husen, A. (ed.), Harsh environment and plant resilience. Springer, Cham,
Germany, 171–202.
Pikovskaya, R.I., 1948. Mobilizatsiia fosfora v pochve v sviazi s zhiznedeiatel'nost'iu nekotorykh vidov
mikroorganizmov [Mobilization of phosphorus in soil in connection with vital activity of some microbial
species]. Mikrobiologiia [Microbiology] 17 (5), 362–370. (In Russian).
Pishchik, V.N., Vorob'ev, N.I., Provorov, N.A., Khomyakov, Yu.V., 2016. Mekhanizmy adaptatsii rastenii i
mikroorganizmov v rastitel'no-mikrobnykh sistemakh k tiazhelym metallam [Mechanisms of plant and
microbial adaptation to heavy metals in plant–microbial systems]. Mikrobiologiia [Microbiology] 85 (3),
231–247. (In Russian). http://www.doi.org/10.7868/S0026365 616030113
Plekhanova, I.O., Kulikov, V.O., Shabaev, V.P., 2023. Vliianie rizosfernykh bakterii na produktivnost'
rastenii pshenitsy i postuplenie elementov iz zagriaznennykh pochv [Influence of rhisospheric
bacteria on the productivity of wheat plants and the input of elements from polluted soils]. Vestnik
Moskovskogo universiteta. Pochvovedenie [Moscow University Soil Science Bulletin] 78 (3), 76–82.
(In Russian). http://www.doi.org/10.55959/MSU0137-0944-17-2023-78-3-76-82
Plekhanova, I.O., Zolotareva, O.A., Tarasenko, I.D., Yakovlev, A.S., 2019. Otsenka ekotoksichnosti
pochv v usloviiakh zagriazneniia tiazhelymi metallami [Assessment of ecotoxicity of soils contaminated
by heavy metals]. Pochvovedenie [Eurasian Soil Science] 10, 1243–1258. (In Russian). http://www.
doi.org/10.1134/S0032180X19100083
Porhuntsova, O.A., Bushueva, V.I., Fedorenchik, A.A., Aleshhenkova, Z.M., 2015. Mikrobno-rastitel'naia
assotsiatsiia kak effektivnyi fitoremediant zagriaznennykh nefteproduktami pochv [Microbial-plant
association as an effective phytoremediant of oil-polluted soils]. Vestnik Belorusskoi gosudarstvennoi
sel'skokhoziaistvennoi akademii [Bulletin of the Belarusian State Agricultural Academy] 2, 87–91. (In
Russian).
Prasad, S., Malav, L.C., Choudhary, J., Kannojiya, S., Kundu, M. et al., 2021. Soil microbiomes for
healthy nutrient recycling. In: Yadav, A.N. et al. (eds.), Current trends in microbial biotechnology for
sustainable agriculture. Environmental and microbial biotechnology. Springer, Singapore, 1–21.
Raymond, R.L., 1961. Microbial oxidation of n-paraffinic hydrocarbons. Development Industrial
Microbiology 2 (1), 23–32.
Sazykina, M.A., Minkina, T.M., Konstantinova, E.Y., Khmelevtsova, L.E., Azhogina, T.N. et al., 2022.
Pollution impact on microbial communities composition in natural and anthropogenically modified
soils of Southern Russia. Microbiological Research 254, 126913. https://doi.org/10.1016/j.
micres.2021.126913
Starikov, S.N., Chetverikov, S.P., 2020. Shtamm Enterobacter sp. UOM-3 sposoben k sinkhronnoi
destruktsii galogensoderzhashchikh gerbitsidov i sintezu indol-3-uksusnoi kisloty [Strain Enterobacter
sp. UOM-3 is able to synchronous destruction of halogen-containing herbicides and synthesis
of indol-3-acetic acid]. Ekobiotekh [Ecobiotech] 3 (4), 716–721. (In Russian). http://www.doi.
org/10.31163/2618-964X-2020-3-4-716-721
Suleymanov, R.A., Baktybaeva, Z.B., Valeev, T.K., Rakhmatullin, N.R., Ivanov, D.E. et al., 2018.
Ekologo-gigienicheskaia kharakteristika okruzhaiushchei sredy i sostoianie zdorov'ia naseleniia na
territoriiakh dobychi i transporta nefti [Environmental and hygienic environmental characteristics
and public health on the territories of crude oil production and transportation]. Ul'ianovskii mediko-biologicheskii zhurnal [Ulyanovsk Medico-Biological Journal] 4, 124–142. (In Russian). http://www.
doi.org/10.23648/UMBJ.2018.32.22703
Tafeeva, E.A., Ivanov, A.V., Titova, A.A., Petrov, I.V., 2016. Soderzhanie tiazhelykh metallov i
nefteproduktov v pochve na territorii neftedobyvaiushchikh raionov respubliki Tatarstan [Content of
heavy metals and petroleum products in the soil on the territory of oilproducing areas of the republic
of Tatarstan]. Gigiena i sanitariia [Hygiene and Sanitation] 95 (10), 939–941. (In Russian).
Yastrebova, O.V., Plotnikova, E.G., 2007. Galotolerantnye bakterii-destruktory politsiklicheskikh
aromaticheskikh uglevodorodov roda Arthrobacter [Halotolerant bacteria of the genus Arthrobacter,
capable of growth on polycyclic aromatic hydrocarbons]. Vestnik Permskogo universiteta [Bulletin of
Perm University] 5 (10), 100–106. (In Russian).