On the resistance of the green alga Ulva Lactuca L. and associated microorganisms to the effects of diesel fuel under experimental conditions
- Authors: Pugovkin D.V.1, Ryzhik I.V.1,2, Salakhov D.O.1, Venger M.P.1, Voskoboynikov G.M.1
-
Affiliations:
- Murmansk Marine Biological Institute of the Russian Academy of Sciences (MMBI RAS)
- Murmansk Arctic University (MAU)
- Issue: No 5 (2025)
- Pages: 580–593
- Section: ECOLOGY
- URL: https://genescells.com/1026-3470/article/view/689905
- DOI: https://doi.org/10.31857/S1026347025050099
- ID: 689905
Cite item
Abstract
It has been experimentally observed that Ulva lactuca from the Barents Sea, is capable of surviving in a laboratory environment when the concentration of water soluble fractions of diesel fuel in water is up to 1 mg/l. A concentration of more than 4.9 mg/l was critical for algae. During these treatments, decreases in photosynthetic rate (2-16 times relative to the control) and the amount of photosynthetic pigments (more than 2 times of the control), an increase the hydrogen peroxide content and the activity of superoxide dismutase were observed in macrophytes. The number, biomass and size characteristics of heterotrophic bacteria associated with algae changed significantly. Thus, the high content of petroleum products in the environment limits the spread of U. lactuca algae, however, with minor contamination, they can actively participate in bioremediation processes.
Full Text

About the authors
D. V. Pugovkin
Murmansk Marine Biological Institute of the Russian Academy of Sciences (MMBI RAS)
Author for correspondence.
Email: pugovkin2005@yandex.ru
Russian Federation, Vladimirskaya 17, Murmansk, 183010
I. V. Ryzhik
Murmansk Marine Biological Institute of the Russian Academy of Sciences (MMBI RAS); Murmansk Arctic University (MAU)
Email: pugovkin2005@yandex.ru
Russian Federation, Vladimirskaya 17, Murmansk, 183038; Sportivnaya 13, Murmansk, 183010
D. O. Salakhov
Murmansk Marine Biological Institute of the Russian Academy of Sciences (MMBI RAS)
Email: pugovkin2005@yandex.ru
Russian Federation, Vladimirskaya 17, Murmansk, 183038
M. P. Venger
Murmansk Marine Biological Institute of the Russian Academy of Sciences (MMBI RAS)
Email: pugovkin2005@yandex.ru
Russian Federation, Vladimirskaya 17, Murmansk, 183038
G. M. Voskoboynikov
Murmansk Marine Biological Institute of the Russian Academy of Sciences (MMBI RAS)
Email: pugovkin2005@yandex.ru
Russian Federation, Vladimirskaya 17, Murmansk, 183038
References
- Воскобойников Г. М., Макаров М. В., Рыжик И. В., Малавенда С. В. Влияние абиотических факторов на структуру фитоценозов, морфологические и физиологические особенности водорослей-макрофитов Баренцева моря // Динамика морских экосистем и современные проблемы сохранения биологического потенциала морей России. Владивосток. Дальнаука, 2007. С. 357–386.
- Воскобойников Г. М., Рыжик И. В., Салахов Д. О., Метелькова Л. О., Жаковская З. А., Лопушанская Е. М. Поглощение и преобразование дизельного топлива водорослью Palmaria palmata (Linnaeus) F. Weber et D. Mohr, 1805 (Rhodophyta) и ее возможная роль в биоремедиации морской воды // Биол. моря. 2020. Т. 46. № 2. С. 135–141.
- Ильинский В. В. Гетеротрофный бактериопланктон // Практическая гидробиология: Учеб. для ун-тов. Под ред. В.Д. Федорова и В.И. Капкова. М.: ПИМ, 2006. 367 с.
- Королюк М. А., Иванова Л., Майорова И., Токарев В. Метод определения активности каталазы // Лаб. дело. 1988. № 1. С. 16–19.
- Ли Б. Д. Разделение, идентификация и количественное определение фотосинтетических пигментов макробентосных водорослей // Экологические аспекты фотосинтеза морских растений. Владивосток: ДВНЦ АН СССР. 1978. С. 38–54.
- Очеретяна С. О., Клочкова Н. Г., Клочкова Т. А. Сезонный состав “зеленых приливов” в Авачинской губе и влияние антропогенного загрязнения на физиологию и рост некоторых зеленых водорослей // Вестн. КамчатГТУ. 2015. № 33. С. 30–36.
- Патин С. А. Экологические проблемы освоения нефтегазовых ресурсов морского шельфа. М.: ВНИРО. 1997. 350 с.
- Патин С. А. Нефтяные разливы и их воздействие на морскую среду и биоресурсы. М.: Изд-во ВНИРО. 2008. 508 с.
- Марковская Е. Ф., Малавенда С. В., Рыжик И. В., Сергиенко Л. А., Сонина А. В., Стародубцева А. А., Воскобойников Г. М. Растения и лишайники Мурманского побережья Баренцева моря: полевой атлас. Петрозаводск: Изд-во ПетрГУ. 2016. 191 с.
- Руководство по методам биологического анализа морской воды и донных отложений // Под ред. Цыбань А. В. Л.: Гидрометеоиздат, 1980. 191 с.
- Уикли Б. Электронная микроскопия для начинающих. М.: Мир. 1975. 324 с.
- Aaronson, A. A. Experimental Microbial Ecology. New York and London: Academic Press. 1970. 236 р.
- Bellincampi D., Dipperro N., Salvi, G., Cervcone F., De Lorenzo G. Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the Auxin-Regulated rolB gene expression in tobacco leaf explants. Plant Physiol. 2000. № 122. 1379–1385. https://doi.org/10.1104/pp.122.4.1379
- Brown K. E. King C. K., Kotzakoulakis K., George S. C., Harrison P. L. Assessing fuel spill risks in polar waters: Temporal dynamics and behaviour of hydrocarbons from Antarctic diesel, marine gas oil and residual fuel oil // Mar. Pollut. Bull. 2016. V. 110. №. 1. P. 343–353. https://doi.org/10.1016/j.marpolbul.2016.06.042
- Dominguez H., Loret E. P. Ulva lactuca, a source of troubles and potential riches // Mar. Drugs. 2019. V. 17. №. 6. 357 P. https://doi.org/10.3390/md17060357
- Donlan R. M. Biofilms: microbial life on surfaces // Emerg. Infect. Dis. 2002. Т. 8. №. 9. С. 881.
- El Maghraby D., Hassan I. Photosynthetic and biochemical response of Ulva lactuca to marine pollution by polyaromatic hydrocarbons (PAHs) collected from different regions in Alexandria city, Egypt // Egypt. J. Bot. 2021. V. 61. № 2. P. 467–478. https://doi.org/10.21608/ejbo.2021.37571.1531
- French-McCay D. P. Development and application of an oil toxicity and exposure model, OilToxEx // Environ. Toxicol. Chem. 2002. V. 21. № 10. P. 2080–2094. https://doi.org/10.1002/etc.5620211011
- Giannopolitis C. N., Ries S. K. Superoxide dismutase I. Occurrence in higher plants // Plant Physiol. 1977. № 59. 309–314. https://doi.org/10.1104/pp.59.2.309
- Goecke F., Labes A., Wiese J., Imhoffe J. F. Phylogenetic analysis and antibiotic activity of bacteria isolated from the surface of two cooccurring macroalgae from the Baltic Sea // Eur. J. Phycol. 2013, V. 48, №1. P. 47–60. https://doi.org/10.1080/09670262.2013.767944
- Hokstad J. N., Faksness L.-G., Daling P. S., Buffagni M. Chemical and toxicological characterisation of water accommodated fractions relevant for oil spill situations // WIT Transactions on Ecology and the Environment. 1970. V. 27. https://doi.org/10.2495/OIL980131
- Kusk K. O. Effects of crude oil and aromatic hydrocarbons on the photosinthesis of three species of Acrosiphonia grown in the laboratory // Bot. Mar. 1980. V. 23. P. 587–593. https://doi.org/10.1111/j.1399-3054.1978.tb01558.x
- Liu Y. X, Liu Y., Lou Y. D., Li N. Toxic effect of oil spill on the growth of Ulva pertusa by stable isotope analysis // IOP Conference Series: Earth and Environmental Science. IOP Publishing, 2019. V. 344. № 1. P. 012062. https://doi.org/10.1088/1755-1315/344/1/012062
- Malavenda S., Makarov M., Ryzhik I., Mityaev M., Malavenda S. Occurrence of Ulva lactuca L. 1753 (Ulvaceae, Chlorophyta) at the Murman Сoast of the Barents Sea // Pol. Res. 2018. V. 37. № 1. P. 1503912. https://doi.org/10.1080/17518369.2018.1503912
- Martin M., Portetelle D., Michel G., Vandenbol M. Microorganisms living on macroalgae: diversity, interactions, and biotechnological applications // Appl. Microbiol. Biotechnol. 2014. V. 98. P. 2917–2935. https://doi.org/10.1007/s00253-014-5557-2
- Matsui T., Yamamoto T., Shinzato N., Mitsuta T., Nakano K., Namihira, T. Degradation of oil tank sludge using long-chain alkane-degrading bacteria // Ann. Microbiol. 2014. V. 64. P. 391–395. https://doi.org/10.1007/s13213-013-0643-8
- McArthur D. M., Moss B. L. The ultrastructure of cell walls in Enteromorpha intestinalis (L.) Link // Br. Phycol. J. 1977. V. 12. № 4. P. 359–368. https://doi.org/10.1080/00071617700650381
- Moss B. L. The control of epiphytes by Halidrys siliquosa (L.) Lyngb. (Phaeophyta, Cystoseiraceae) // Phycologia. 1982. V. 21. №. 2. P. 185–188. https://doi.org/10.2216/i0031-8884-21-2-185.1
- Pasmore M., Costerton J. W. Biofilms, bacterial signaling, and their ties to marine biology // J. Ind. Microbiol. Biotechnol. 2003. V. 30. P. 407–413. https://doi.org/10.1007/s10295-003-0069-6
- Pilatti F. K. Ramlov F., Schmidt E. C., Kreusch M., Pereira D. T., Costa C., de Oliveira E. R., Bauer C. M., Rocha M., Z. L. Bouzon, Maraschin, M. In vitro exposure of Ulva lactuca Linnaeus (Chlorophyta) to gasoline–Biochemical and morphological alterations // Chemosphere. 2016. V. 156. P. 428–437. https://doi.org/10.1016/j.chemosphere.2016.04.126
- Porter K. G., Feig Y. S. The use DAPI for identifying and counting of aquatic microflora // Limnol. Oceanogr. 1980. V. 25 № 5 P. 943–948. https://doi.org/10.4319/lo.1980.25.5.0943
- Ryzhik I., Pugovkin D., Makarov M., Roleda M. Y., Basova L., Voskoboynikov G. Tolerance of Fucus vesiculosus exposed to diesel water-accommodated fraction (WAF) and degradation of hydrocarbons by the associated bacteria // Environ. Pollut. 2019. V. 254. P. 113072. https://doi.org/10.1016/j.envpol.2019.113072
- Ryzhik I. V., Pugovkin D. V., Salakhov D. O., Klindukh M. P., Voskoboynikov G. M. Physiological changes and rate of resistance of Acrosiphonia arcta (Dillwyn) Gain upon exposure to diesel fuel // Heliyon. 2022. V. 8. № 8. https://doi.org/10.1016/j.heliyon.2022.e10177
- Ryzhik I., Salakhov D., Makarov M., Menshakova M. Analysis of physiological and biochemical parameters of Acrosiphonia arcta (Dillwyn) Gain cells at the early stage of stress reaction formation under the effect of diesel fuel emulsion // Mar. Biol. J. 2024. V. 9. № 1. P. 86–97. https://doi.org/10.21072/mbj.2024.09.1.07
- Salakhov D., Pugovkin D., Ryzhik I., Voskoboinikov G. The influence of diesel fuel on morpho-functional state of Ulvaria obscura (Chlorophyta) // IOP Conference Series: Earth and Environmental Science. IOP Publishing, 2020. V. 539. № 1. P. 012202. https://doi.org/10.1088/1755-1315/539/1/012202
- Salakhov D., Pugovkin D., Ryzhik I., Voskoboinikov G. The changes in the morpho-functional state of the green alga Ulva intestinalis L. in the Barents Sea under the influence of diesel fuel // IOP Conference Series: Earth and Environmental Science. IOP Publishing, 2021. V. 937. № 2. P. 022059. https://doi.org/10.1088/1755-1315/937/2/022059
- Sand-Jensen K., Borum J. Photosynthetic responses of Ulva lactuca at very low light // Mar. Ecol. Prog. Ser. Oldendorf. 1988. V. 50. №. 1. P. 195–201.
- Seely G. R., Duncan M. J., Vidaver W. E. Preparative and analytical extraction of pigments from brown algae with dimethyl sulfoxide // Mar. Biol. 1972. V. 12. P. 184–188. https://doi.org/10.1007/BF00350754
- Singer, M. M., Aurand, D., Bragin, G. E., Clark, J. R., Coelho, G. M., Sowby, M. L., Tjeerdema R. S. Standardization of the preparation and quantitation of water-accommodated fractions of petroleum for toxicity testing // Mar. Pollut. Bull. V. 40. № 11. P. 1007–1016. https://doi.org/10.1016/S0025-326X(00)00045-X
- Walker J. D., Colwell R. R. Measuring the potential activity of hydrocarbon-degrading bacteria // Appl. Environ. Microbiol. 1976. V. 31. P. 189–197.
- Xia J., Li Y., Zou D. Effects of salinity stress on PSII in Ulva lactuca as probed by chlorophyll fluorescence measurements // Aquatic Botany. 2004. V. 80. № 2. P. 129–137. https://doi.org/10.1016/j.aquabot.2004.07.006
- Zambrano J., Carballeira A. Effects of hydrocarbons on the physiology and growth of Ulva sp. (Chlorophyta) // Bol. Inst. Esp. Oceanogr. – 1999. V. 15. № 1. P. 373–381.
Supplementary files
