On the resistance of the green alga Ulva Lactuca L. and associated microorganisms to the effects of diesel fuel under experimental conditions

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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.

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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

  1. 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.
  2. 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.
  3. 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.
  4. Королюк М. А., Иванова Л., Майорова И., Токарев В. Метод определения активности каталазы // Лаб. дело. 1988. № 1. С. 16–19.
  5. 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.
  6. 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.
  7. Патин С. А. Экологические проблемы освоения нефтегазовых ресурсов морского шельфа. М.: ВНИРО. 1997. 350 с.
  8. Патин С. А. Нефтяные разливы и их воздействие на морскую среду и биоресурсы. М.: Изд-во ВНИРО. 2008. 508 с.
  9. 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.
  10. Руководство по методам биологического анализа морской воды и донных отложений // Под ред. Цыбань А. В. Л.: Гидрометеоиздат, 1980. 191 с.
  11. Уикли Б. Электронная микроскопия для начинающих. М.: Мир. 1975. 324 с.
  12. Aaronson, A. A. Experimental Microbial Ecology. New York and London: Academic Press. 1970. 236 р.
  13. 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
  14. 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
  15. 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
  16. Donlan R. M. Biofilms: microbial life on surfaces // Emerg. Infect. Dis. 2002. Т. 8. №. 9. С. 881.
  17. 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
  18. 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
  19. 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
  20. 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
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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
  29. 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
  30. 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
  31. 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
  32. 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
  33. 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
  34. 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
  35. 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
  36. 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
  37. 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.
  38. 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
  39. 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
  40. Walker J. D., Colwell R. R. Measuring the potential activity of hydrocarbon-degrading bacteria // Appl. Environ. Microbiol. 1976. V. 31. P. 189–197.
  41. 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
  42. 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

Supplementary Files
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2. Fig. 1. Gross content of water-soluble fractions of diesel fuel with the addition of 50 mg/l of diesel fuel in the presence of algae and without them.

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3. Fig. 2. Changes in the cellular apparatus of cells during the experiment at different concentrations of diesel fuel: a – control – 0 days; b – 6 days – 5 mg/l. Epiphytic microorganisms are noted at the periphery; c – 6 days – 100 mg/l. Many bacteria are noted at the periphery. The greater part of the section is granular content. d – 10 days – 50 mg/l. b – epiphytic bacteria, p – perinoids, s – starch granules.

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4. Fig. 3. Intensity of photosynthesis of Ulva lactuca during the experiment under the influence of different concentrations of diesel fuel.

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5. Fig. 4. Content of photosynthetic pigments after 10 days of exposure to different concentrations of DT: a – chlorophyll (A and B); b – carotenoids.

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6. Fig. 5. Activity of the antioxidant system under the influence of different DTs after 10 days of the experiment. a – hydrogen peroxide content in U. lactuca cells after 10 days of the experiment; b – SOD activity; c – catalase activity.

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7. Fig. 6. Total bacterial count (TBC), the number of cultivated heterotrophic bacteria (CHB) and the bacterial biomass of epiphytic bacteria of the alga Ulva lactuca.

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