Influence of Microplastics on the Nutritional and Locomotive Activity of Dinoflagellate Oxyrrhis marina in the Experiment

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Abstract

The incorporation of microplastic particles (MPs) into the microbial food chain and their impact on physiology of consuming organisms has been largely underexplored. The heterotrophic dinoflagellate Oxyrrhis marina serves as a good model for understanding these processes. In this work, flow cytometry methods were used to analyze the dynamics of consumption by this predator of its natural prey, the microalga Isochrysis galbana (ISO), and plastic microspheres (MS) of the same size. In addition, the effect of the diets containing these components on the swimming speed and movement patterns of Oxyrrhis marina cells was evaluated using a computer method for analyzing video recordings of O. marina movement. It was shown that from the first minutes of the experiment, the dinoflagellates actively consumed both the preys, but by the end of the experiment, the number of MS in the medium decreased to a lesser extent, from 4.4 to 2.2 · 105/mL, while Isochrysis galbana cells were almost completely grazed, and their abundance decreased by more than two orders of magnitude, from 4.9 · 105 cells/mL to 2.3 · 103 cells/mL. Such dynamics were associated with compensation for the number of microspheres in the medium due to their excretion and repeated phagocytosis by Oxyrrhis marina. The increase in the size of dinoflagellate cells, which was a consequence of the consumption of plastic microspheres, did not lead to a noticeable decrease in their mobility and impaired locomotion. ‘Unproductive’ feeding of the dinoflagellates on microplastics did not supply them with nutrients and was the reason for a statistically significant decrease in their abundance (compared to the control and experiment with microalgae). This seemed to be due to the unreasonably high energy consumption of their population for constant search, phagocytosis, and excretion of microspheres. There were no signs of the predator’s rejection of such an unproductive nutrition strategy; on the contrary, cell mobility increased over time, which only worsened the situation. Such processes can have far-reaching negative consequences for the entire food chain. In particular, microplastics “packaged” by unicellular organisms can be transported to higher trophic levels and accumulate in mollusks, fish, and larger predators.

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About the authors

T. V. Rauen

A. O. Kovalevsky Institute of Biology of the Southern Seas of Russian Academy of Sciences

Author for correspondence.
Email: taschi@mail.ru
Russian Federation, Sevastopol

V. S. Mukhanov

A. O. Kovalevsky Institute of Biology of the Southern Seas of Russian Academy of Sciences

Email: taschi@mail.ru
Russian Federation, Sevastopol

Iu. S. Baiandina

A. O. Kovalevsky Institute of Biology of the Southern Seas of Russian Academy of Sciences

Email: taschi@mail.ru
Russian Federation, Sevastopol

A. M. Lyakh

A. O. Kovalevsky Institute of Biology of the Southern Seas of Russian Academy of Sciences

Email: taschi@mail.ru
Russian Federation, Sevastopol

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Supplementary files

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2. Рис. 1. Схема приготовления экспериментальных суспензий в контроле (CNRL) и опытах с микроводорослями I. galbana (ISO) и пластиковыми микросферами (MS) из следующих компонентов: m — питательной среды, O.m. — маточной культуры динофлагелляты O. marina, I.g. — маточной культуры I. galbana, ms — суспензии пластиковых микросфер.

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3. Рис. 2. Графики для расчета общей численности (метод гейтинга) гетеротрофной динофлагелляты O. marina (OXY) и ее кормовых объектов — микросфер (MS) и гаптофитовой микроводоросли I. galbana (ISO) на 2-параметрических цитограммах прямого светорассеивания (FS) и флуоресценции в красной (FL4, 675 нм; слева) и зеленой (FL1, 525 нм; справа) областях спектра. OXY* – клетки динофлагеллят, потребляющие I. galbana и микросферы, OXY** – клетки динофлагеллят с микросферами в пищевых вакуолях (Rauen, 2023).

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4. Рис. 3. Клетки динофлагелляты O. marina с одной (а, б) и несколькими (в–е) МS в пищеварительных вакуолях в светлом поле (а, г) и эпифлуоресцентном режиме (б, в, д, е) (Rauen, 2023).

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5. Рис. 4. Трекинг движения динофлагеллят в программе ImageJ (а), набор треков, полученный в одном из экспериментов (б), и схема определения коэффициента спрямленности траектории движения O. marina (в). Обозначения L и l приведены в тексте.

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6. Рис. 5. Динамика численности динофлагеллят O. marina (а), микроводорослей I. galbana (ISO) и пластиковых микросфер (MS) (б), доли клеток O. marina с микросферами в пищеварительных вакуолях (б) (OXY*) и средних размеров (ESD) клеток O. marina (в), в контроле (CNRL), при питании микроводорослями (ISO) и микросферами (MS). Вариабельность представлена границами стандартного отклонения.

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7. Рис. 6. Средние скорости движения клеток (а), доля подвижных клеток (б) и коэффициент спрямленности траекторий движения (в) динофлагеллят O. marina в экспериментальных сосудах с добавлением I. galbana (ISO), пластиковых микросфер (MS) и в контроле (CNRL) в начале эксперимента, через два и шесть часов. Показаны медианы, процентили 25–75% и 5–95%. Точки обозначают выбросы, дуги соединяют статистически не отличающиеся наборы значений, измеренные в одинаковые минуты эксперимента.

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