vestnik-bio-msuВестник Московского университета. Серия 16. БиологияVestnik Moskovskogo universiteta. Seriya 16. Biologiya0137-0952Lomonosov Moscow State University, School of Biology10.55959/MSU0137-0952-16-78-3-6vestnik-bio-msu-1260Research ArticleОРИГИНАЛЬНОЕ ИССЛЕДОВАНИЕRESEARCH ARTICLEПервичные процессы фотосинтеза Thalassiosira weissflogii при воздействии ципрофлоксацинаPrimary photosynthetic processes of Thalassiosira weissflogii under the effect of ciprofloxacinhttps://orcid.org/0000-0002-7344-0256ТодоренкоД. А.TodorenkoD. A.

Тодоренко Дарья Алексеевна – канд. биол. наук, науч. сотр. кафедры биофизики биологического факультета. Тел.: 8-495-939-35-03

119234, г. Москва, Ленинские горы, д. 1, стр. 12

Department of Biophysics, Faculty of Biology

1–12 Leninskie gory, Moscow, 119234

todorenko@mail.bio.msu.ruhttps://orcid.org/0009-0001-0451-8718СидоченкоН. Д.SidochenkoN. D.

Сидоченко Никита Дмитриевич – студент. Тел.: 8-495-952-89-01

117198, г. Москва, ул. Миклухо-Маклая, д. 6

6 Miklukho-Maklaya st., Moscow, 117198

ssddnikita@gmail.comhttps://orcid.org/0000-0001-9737-4516БайжумановА. А.BaizhumanovA. A.

Байжуманов Адиль Ануарович – канд. биол. наук, ст. науч. сотрудник кафедры биофизики биологического факультета. Тел.: 8-495-939-35-03

119234, г. Москва, Ленинские горы, д. 1, стр. 12

Department of Biophysics, Faculty of Biology

1–12 Leninskie gory, Moscow, 119234

adilbayzhumanov@biophys.msu.ruhttps://orcid.org/0000-0002-0511-7983БратковскаяЛ. Б.BratkovskayaL. B.

Братковская Любовь Борисовна – канд. биол. наук, вед. науч. сотр. кафедры общей экологии и гидробиологии биологического факультета. Тел.: 8-495-939-25-18

119234, г. Москва, Ленинские горы, д. 1, стр. 12

Department of General Ecology and Hydrobiology, Faculty of Biology

1–12 Leninskie gory, Moscow, 119234

profkom-bio@mail.ruhttps://orcid.org/0000-0002-6164-5625МаторинД. Н.MatorinD. N.

Маторин Дмитрий Николаевич – докт. биол. наук, проф., вед. науч. сотр. кафедры биофизики биологического факультета. Тел.: 8-495-939-35-03

119234, г. Москва, Ленинские горы, д. 1, стр. 12

Department of Biophysics, Faculty of Biology

1–12 Leninskie gory, Moscow, 119234

dnmatorin@mail.ruМосковский государственный университет имени М.В. ЛомоносоваРоссияLomonosov Moscow State UniversityRussian FederationРоссийский университет дружбы народовРоссияPeoples’ Friendship University of RussiaRussian Federation202320112023783186194Copyright © Тодоренко Д.А., Сидоченко Н.Д., Байжуманов А.А., Братковская Л.Б., Маторин Д.Н., 20232023Тодоренко Д.А., Сидоченко Н.Д., Байжуманов А.А., Братковская Л.Б., Маторин Д.Н.Todorenko D.A., Sidochenko N.D., Baizhumanov A.A., Bratkovskaya L.B., Matorin D.N.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://vestnik-bio-msu.elpub.ru/jour/article/view/1260

Фторхинолоновые антибиотики, такие как ципрофлоксацин, активно использовались в медицинской практике, в том числе в пандемию COVID-19, для подавления побочных бактериальных инфекций. Широкое применение и неправильная утилизация приводят к появлению антибиотиков в окружающей среде, что может оказывать воздействие на природные водные организмы, включая фитопланктон. Воздействие фторхинолоновых антибиотиков на процессы фотосинтеза диатомовых микроводорослей, которые являются основными продуцентами в морских экосистемах, мало изучено. В работе исследовано воздействие антибиотика ципрофлоксацина на первичные процессы фотосинтеза морской диатомовой микроводоросли Thalassiosira weissflogii. Показано, что ципрофлоксацин воздействует на работу фотосистемы II (ФСII), препятствуя передаче поглощенной энергии от возбужденных молекул хлорофилла антенны к реакционному центру (РЦ) ФСII (φDo). При воздействии ципрофлоксацина выявлено снижение эффективности донирования электрона к Р680+ (FV / FO), ингибирование квантового выхода ФСII (FV / FM), снижение доли активных РЦ (ABS / RC) и увеличение диссипации поглощенной энергии на РЦ (DIo / RC). Показано, что механизм действия ципрофлоксацина связан с повреждением РЦ ФСII. Ципрофлоксацин усиливает светочувствительность микроводорослей и вызывает увеличение количества продуктов перекисного окисления липидов. Предлагается использование параметров флуоресценции хлорофилла для анализа воздействия антибиотиков на микроводоросли.

Fluoroquinolone antibiotics such as ciprofloxacin have been actively used in medical practice, including the COVID-19 pandemic, to suppress adverse bacterial infections. Widespread application and improper disposal have resulted in the ubiquity of antibiotics in the environment, which can affect aquatic life, including phytoplankton. The effect of fluoroquinolone antibiotics on the photosynthetic processes of marine diatoms, which are the main producers in marine ecosystems, has been little studied. In this work the effect of the antibiotic ciprofloxacin on the primary photosynthetic processes in the marine diatom Thalassiosira weissflogii was studied. It has been shown that ciprofloxacin affects the functioning of PSII, preventing the transfer of absorbed energy from the excited antenna chlorophyll molecules to the PSII RC (φDo). Under the influence of ciprofloxacin, a decrease in the efficiency of electron donation to P680+ (FV / FO), inhibition of the quantum yield of PSII (FV / FM), a decrease in the proportion of active RCs (ABS / RC), and an increase in the dissipation of absorbed energy in RCs (DIo / RC) were revealed. It has been shown that the mechanism of action of ciprofloxacin is associated with damage of PSII RC. Ciprofloxacin enhances the photosensitivity of microalgae and causes an increase in lipid peroxidation products. It is proposed to apply the parameters of chlorophyll fluorescence analyzing the effect of antibiotics on microalgae.

морские диатомовые микроводоросликривые OJIPфторхинолоновые антибиотикифотосистема IIфлуоресценция хлорофиллафотоингибированиеmarine diatomsOJIP curvesfluoroquinolone antibioticsphotosystem IIchlorophyll fluorescencephotoinhibitionИсследование выполнено при финансовой поддержке Российского научного фонда (проект № 22-11-00009).The research was funded by Russian Science Foundation, project number 22-11-00009.ReferencesVan Doorslaer X., Dewulf J., Van Langenhove H., Demeestere K. Fluoroquinolone antibiotics: An emerging class of environmental micropollutants. Sci. Total Environ. 2014;500–501:250–269.Van Doorslaer X., Dewulf J., Van Langenhove H., Demeestere K. Fluoroquinolone antibiotics: An emerging class of environmental micropollutants. Sci. Total Environ. 2014;500–501:250–269.Eregowda T., Mohapatra S. Fate of micropollutants in engineered and natural environment. Resilience, response, and risk in water systems. Eds. M. Kumar, F. Munoz-Arriola, H. Furumai, and T. Chaminda. Singapore: Springer; 2020:283–301.Eregowda T., Mohapatra S. Fate of micropollutants in engineered and natural environment. Resilience, response, and risk in water systems. Eds. M. Kumar, F. Munoz-Arriola, H. Furumai, and T. Chaminda. Singapore: Springer; 2020:283–301.Omuferen L.O., Maseko B., Olowoyo J.O. Occurrence of antibiotics in wastewater from hospital and convectional wastewater treatment plants and their impact on the effluent receiving rivers: current knowledge between 2010 and 2019. Environ. Monit. Assess. 2022;194(4):306.Omuferen L.O., Maseko B., Olowoyo J.O. Occurrence of antibiotics in wastewater from hospital and convectional wastewater treatment plants and their impact on the effluent receiving rivers: current knowledge between 2010 and 2019. Environ. Monit. Assess. 2022;194(4):306.Lalumera G.M., Calamari D., Galli P. Preliminary investigation on the environmental occurrence and effects of antibiotics used in aquaculture in Italy. Chemosphere. 2004;54(5):661–668.Lalumera G.M., Calamari D., Galli P. Preliminary investigation on the environmental occurrence and effects of antibiotics used in aquaculture in Italy. Chemosphere. 2004;54(5):661–668.Yang S., Carlson K.H. Solid-phase extraction-high performance liquid chromatography-ion trap mass spectrometry for analysis of trace concentrations of macrolide antibiotics in natural and wastewater matrices. J. Chromatogr. A. 2004;1038(1–2):141–155.Yang S., Carlson K.H. Solid-phase extraction-high performance liquid chromatography-ion trap mass spectrometry for analysis of trace concentrations of macrolide antibiotics in natural and wastewater matrices. J. Chromatogr. A. 2004;1038(1–2):141–155.Santos L.H.M.L.M., Araujo A.N., Fachini A., Pena A., Delerue-Matos C., Montenegro M.C.B.S.M. Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. J. Hazard. Mater. 2010;175(1–3):45–95.Santos L.H.M.L.M., Araujo A.N., Fachini A., Pena A., Delerue-Matos C., Montenegro M.C.B.S.M. Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. J. Hazard. Mater. 2010;175(1–3):45–95.Kümmerer K. Drugs in the environment, emission of drugs, diagnostic aids and disinfectants into wastewater by hospitals in relation to other sources review. Chemosphere. 2001;45(6–7):957–969.Kümmerer K. Drugs in the environment, emission of drugs, diagnostic aids and disinfectants into wastewater by hospitals in relation to other sources review. Chemosphere. 2001;45(6–7):957–969.Kovalakova P., Cizmas L., McDonald T.J., Marsalek B., Feng M., Sharma V.K. Occurrence and toxicity of antibiotics in the aquatic environment: A review. Chemosphere. 2020;251:126351.Kovalakova P., Cizmas L., McDonald T.J., Marsalek B., Feng M., Sharma V.K. Occurrence and toxicity of antibiotics in the aquatic environment: A review. Chemosphere. 2020;251:126351.Vannini C., Domingo G., Marsoni M., Mattia F.D., Labra M., Castiglioni S., Bracale M. Effects of a complex mixture of therapeutic drugs on unicellular algae Pseudokirchneriella subcapitata. Aquat. Toxicol. 2011;101(2):459–465.Vannini C., Domingo G., Marsoni M., Mattia F.D., Labra M., Castiglioni S., Bracale M. Effects of a complex mixture of therapeutic drugs on unicellular algae Pseudokirchneriella subcapitata. Aquat. Toxicol. 2011;101(2):459–465.Karampela I., Dalamaga M. Could respiratory fluoroquinolones, levofloxacin and moxifloxacin, prove to be beneficial as an adjunct treatment in COVID-19? Arch. Med. Res. 2020;51(7):741–742.Karampela I., Dalamaga M. Could respiratory fluoroquinolones, levofloxacin and moxifloxacin, prove to be beneficial as an adjunct treatment in COVID-19? Arch. Med. Res. 2020;51(7):741–742.Hughes S.R., Kay P., Brown L.E. Global synthesis and critical evaluation of pharmaceutical data sets collected from river systems. Environ. Sci. Technol. 2013;47(2):661–677.Hughes S.R., Kay P., Brown L.E. Global synthesis and critical evaluation of pharmaceutical data sets collected from river systems. Environ. Sci. Technol. 2013;47(2):661–677.Liu B.Y., Nie X.P., Liu W.Q., Snoeijs P., Guan C., Tsui M.T.K. Toxic effects of erythromycin, ciprofloxacin and sulfamethoxazole on photosynthetic apparatus in Selenastrum capricornutum. Ecotoxicol. Environ. Saf. 2011;74(4):1027–1035.Liu B.Y., Nie X.P., Liu W.Q., Snoeijs P., Guan C., Tsui M.T.K. Toxic effects of erythromycin, ciprofloxacin and sulfamethoxazole on photosynthetic apparatus in Selenastrum capricornutum. Ecotoxicol. Environ. Saf. 2011;74(4):1027–1035.Nie X.P., Liu B.Y., Yu H.J., Liu W.Q., Yang Y.F. Toxic effects of erythromycin, ciprofloxacin and sulfamethoxa- zole exposure to the antioxidant system in Pseudokirchneriella subcapitata. Environ. Pollut. 2013;172:23–32.Nie X.P., Liu B.Y., Yu H.J., Liu W.Q., Yang Y.F. Toxic effects of erythromycin, ciprofloxacin and sulfamethoxa- zole exposure to the antioxidant system in Pseudokirchneriella subcapitata. Environ. Pollut. 2013;172:23–32.Xiong J., Kurade M.B., Kim J.R., Roh H., Jeon B. Ciprofloxacin toxicity and its co-metabolic removal by a freshwater microalga Chlamydomonas mexicana. J. Hazard. Mater. 2017;323(Part A):212–219.Xiong J., Kurade M.B., Kim J.R., Roh H., Jeon B. Ciprofloxacin toxicity and its co-metabolic removal by a freshwater microalga Chlamydomonas mexicana. J. Hazard. Mater. 2017;323(Part A):212–219.Strasser R.J., Tsimilli-Michael M., Srivasta A. Analysis of the chlorophyll a fluorescence transient. Chloro- phyll a fluorescence. Advances in photosynthesis and respira- tion, vol. 19. Eds. G. Papageorgiou and R. Govindjee. Dordrecht: Springer; 2004:321–362.Strasser R.J., Tsimilli-Michael M., Srivasta A. Analysis of the chlorophyll a fluorescence transient. Chloro- phyll a fluorescence. Advances in photosynthesis and respira- tion, vol. 19. Eds. G. Papageorgiou and R. Govindjee. Dordrecht: Springer; 2004:321–362.Schreiber U. Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: an overview. Chlorophyll a fluorescence. Advances in photosynthesis and respiration, vol. 19. Eds. G. Papageorgiou and R. Govindjee. Dordrecht: Springer; 2004:279–319.Schreiber U. Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: an overview. Chlorophyll a fluorescence. Advances in photosynthesis and respiration, vol. 19. Eds. G. Papageorgiou and R. Govindjee. Dordrecht: Springer; 2004:279–319.Stewart R.R.C., Bewley J.D. Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol. 1980;65(2):245–248.Stewart R.R.C., Bewley J.D. Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol. 1980;65(2):245–248.Yang L.H., Ying G.G., Su H.C., Stauber J.L., Adams M.S., Binet M.T. Growth-inhibiting effects of 12 antibacterial agents and their mixtures on the freshwater microalga Pseudokirchneriella subcapitata. Environ. Toxicol. Chem. 2008;27(5):1201–1208.Yang L.H., Ying G.G., Su H.C., Stauber J.L., Adams M.S., Binet M.T. Growth-inhibiting effects of 12 antibacterial agents and their mixtures on the freshwater microalga Pseudokirchneriella subcapitata. Environ. Toxicol. Chem. 2008;27(5):1201–1208.Chen Q., Zhang L., Han Y., Fang J., Wang H. Degradation and metabolic pathways of sulfamethazine and enrofloxacin in Chlorella vulgaris and Scenedesmus obliquus treatment systems. Environ. Sci. Pollut. Res. 2020;27:28198–28208.Chen Q., Zhang L., Han Y., Fang J., Wang H. Degradation and metabolic pathways of sulfamethazine and enrofloxacin in Chlorella vulgaris and Scenedesmus obliquus treatment systems. Environ. Sci. Pollut. Res. 2020;27:28198–28208.Genty B., Briantais J.M., Baker N.R. The relation- ship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta. 1989;990(1):87–92.Genty B., Briantais J.M., Baker N.R. The relation- ship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta. 1989;990(1):87–92.Антал Т.К., Гpаевcкая Е.Э., Матоpин Д.Н., Волгушева А.А., Оcипов В.А., Кpенделева Т.Е., Pубин А.Б. Исследование влияния ионов метилртути и меди на первичные процессы фотосинтеза у зеленой водоросли Chlamydomonas moewusii с использованием параметров кинетических кривых переменной флуоресценции хлорофилла. Биофизика. 2009;54(4):681–687.Антал Т.К., Гpаевcкая Е.Э., Матоpин Д.Н., Волгушева А.А., Оcипов В.А., Кpенделева Т.Е., Pубин А.Б. Исследование влияния ионов метилртути и меди на первичные процессы фотосинтеза у зеленой водоросли Chlamydomonas moewusii с использованием параметров кинетических кривых переменной флуоресценции хлорофилла. Биофизика. 2009;54(4):681–687.Pan X., Zhang D., Chen X., Mu G., Li L., Bao A. Effects of levofloxacin hydrochlordie on photosystem II activity and heterogeneity of Synechocystis sp. Chemosphere. 2009;77(3):413–418.Pan X., Zhang D., Chen X., Mu G., Li L., Bao A. Effects of levofloxacin hydrochlordie on photosystem II activity and heterogeneity of Synechocystis sp. Chemosphere. 2009;77(3):413–418.Kalaji H.M., Jajoo A., Oukarroum A., Brestic M., Zivcak M., Samborska I.A., Cetner M.D., Łukasik I., Goltsev V., Ladle, R.J. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol. Plant. 2016;38:102.Kalaji H.M., Jajoo A., Oukarroum A., Brestic M., Zivcak M., Samborska I.A., Cetner M.D., Łukasik I., Goltsev V., Ladle, R.J. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol. Plant. 2016;38:102.Joshi M.K., Mohanty P. Chlorophyll a fluorescence as a probe of heavy metal Ion toxicity in plants. Chlorophyll a fluorescence. Advances in photosynthesis and respiration, vol. 19. Eds. G. Papageorgiou and R. Govindjee. Dordrecht: Springer; 2004:637–661.Joshi M.K., Mohanty P. Chlorophyll a fluorescence as a probe of heavy metal Ion toxicity in plants. Chlorophyll a fluorescence. Advances in photosynthesis and respiration, vol. 19. Eds. G. Papageorgiou and R. Govindjee. Dordrecht: Springer; 2004:637–661.Lazár D. The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct. Plant Biol. 2006;33(1):9–30.Lazár D. The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct. Plant Biol. 2006;33(1):9–30.Aristilde L., Melis A., Sposito G. Inhibition of photosynthesis by a fluoroquinolone antibiotic. Environ. Sci. Technol. 2010;44(4):1444–1450.Aristilde L., Melis A., Sposito G. Inhibition of photosynthesis by a fluoroquinolone antibiotic. Environ. Sci. Technol. 2010;44(4):1444–1450.Murata N., Takahashi S., Nishiyama Y., Allakhverdiev S.I. Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta. 2007;1767(6):414–421.Murata N., Takahashi S., Nishiyama Y., Allakhverdiev S.I. Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta. 2007;1767(6):414–421.Tyystjärvi E. Photoinhibition of Photosystem II. Int. Rev. Cell Mol. Biol. 2013;300:243–303.Tyystjärvi E. Photoinhibition of Photosystem II. Int. Rev. Cell Mol. Biol. 2013;300:243–303.Pätsikkä E., Aro E.-M., Tyystjärvi E. Increase in the quantum yield of photoinhibition contributes to copper toxicity in vivo. Plant Physiol. 1998;117(2):619–627.Pätsikkä E., Aro E.-M., Tyystjärvi E. Increase in the quantum yield of photoinhibition contributes to copper toxicity in vivo. Plant Physiol. 1998;117(2):619–627.Rintamäki E., Salo R., Lehtonen E., Aro E.-M. Regulation of D1-protein degradation during photoinhibition of photosystem II in vivo: phosphorylation of the D1 protein in various plant groups. Planta. 1995;195(3):379–386.Rintamäki E., Salo R., Lehtonen E., Aro E.-M. Regulation of D1-protein degradation during photoinhibition of photosystem II in vivo: phosphorylation of the D1 protein in various plant groups. Planta. 1995;195(3):379–386.Pinto E., Sigaud-kutner T.K.S., Leitão M.A.S., Okamoto O.K., Morse D., Colepicolo P. Heavy metal–induced oxidative stress in algae. J. Phycol. 2003;39(6):1008–1018.Pinto E., Sigaud-kutner T.K.S., Leitão M.A.S., Okamoto O.K., Morse D., Colepicolo P. Heavy metal–induced oxidative stress in algae. J. Phycol. 2003;39(6):1008–1018.

The authors declare that there are no conflicts of interest present.