Attack of Microcystis aeruginosa bloom on a Ceratophyllum submersum field: Ecotoxicological measurements in real environment with real microcystin exposure

Andrea Zsuzsanna Ujvárosi; Milán Riba; Tamás Garda; Gyöngyi Gyémánt; György Vereb; Márta M-Hamvas; Gábor Vasas; Csaba Máthé

doi:10.1016/j.scitotenv.2019.01.226

Attack of Microcystis aeruginosa bloom on a Ceratophyllum submersum field: Ecotoxicological measurements in real environment with real microcystin exposure

Sci Total Environ. 2019 Apr 20:662:735-745. doi: 10.1016/j.scitotenv.2019.01.226. Epub 2019 Jan 22.

Authors

Andrea Zsuzsanna Ujvárosi¹, Milán Riba¹, Tamás Garda¹, Gyöngyi Gyémánt², György Vereb³, Márta M-Hamvas⁴, Gábor Vasas⁵, Csaba Máthé⁶

Affiliations

¹ University of Debrecen, Egyetem ter 1, H-4032 Debrecen, Hungary; Faculty of Science and Technology, Institute of Biology and Ecology, Department of Botany, Hungary.
² University of Debrecen, Egyetem ter 1, H-4032 Debrecen, Hungary; Faculty of Science and Technology, Institute of Chemistry, Department of Inorganic and Analytical Chemistry, Hungary.
³ University of Debrecen, Egyetem ter 1, H-4032 Debrecen, Hungary; Faculty of Medicine, Department of Biophysics and Cell Biology and Faculty of Pharmacy, Hungary.
⁴ University of Debrecen, Egyetem ter 1, H-4032 Debrecen, Hungary; Faculty of Science and Technology, Institute of Biology and Ecology, Department of Botany, Hungary. Electronic address: hamvas.marta@science.unideb.hu.
⁵ University of Debrecen, Egyetem ter 1, H-4032 Debrecen, Hungary; Faculty of Science and Technology, Institute of Biology and Ecology, Department of Botany, Hungary. Electronic address: vasas.gabor@science.unideb.hu.
⁶ University of Debrecen, Egyetem ter 1, H-4032 Debrecen, Hungary; Faculty of Science and Technology, Institute of Biology and Ecology, Department of Botany, Hungary. Electronic address: mathe.csaba@science.unideb.hu.

PMID: 30703731
DOI: 10.1016/j.scitotenv.2019.01.226

Abstract

Overproduction of toxic cyanobacteria is a type of harmful algal blooms (HABs). The heptapeptide microcystins (MCs) are one of the most common cyanotoxins. There is increasing research concerning the effects of MCs on growth and physiology of vascular plants, however there is a lack of studies on their direct effects on aquatic macrophytes in the real environment. Here we report the occurrence of a MC producing HAB in Lake Bárdos, Hungary in 2012 with harmful effects on cytological, histological and biochemical parameters of Ceratophyllum submersum (soft hornwort) plants naturally growing at the blooming site. Blue-Green Sinapis Test (BGST) showed high toxicity of HAB samples. Cell-free water samples contained a significant amount of MCs (7.31 ± 0.17 μg L^-1) while C. submersum plants contained 1.01 ± 0.21 μg g DW^-1 MCs. Plants showed significant increases of protein content and decreases of anthocyanin content and carotenoid/chlorophyll ratio, indicating physiological stress- as compared to plants from the control (MC free) sampling site of the same water body. Histological and cytological studies showed (i) radial swelling and the abnormal formation of lateral buds at the shoot tip leading to abnormal development; (ii) the fragmentation of nuclei as well as accumulation of phenolics in the nucleus indicating that the HAB induced cell death and stress reactions at the nuclear level. The most relevant effect was the increase of histone H3 phosphorylation in metaphase chromosomes: since MCs are strong inhibitors of protein phosphatases, this alteration is related to the biochemical targets of these toxins. The HAB decreased peroxidase activity, but increased nuclease and protease activities, showing the decreased capacity of plants to face biotic stress and as the cytological changes, the induction of cell death. This study is one of the first to show the complex harmful changes in aquatic plants that co-exist with HABs.

Keywords: Cell death; Ceratophyllum submersum; HAB; Histone H3 phosphorylation; Microcystins; Real exposure.

MeSH terms

Harmful Algal Bloom*
Hungary
Lakes
Magnoliopsida / drug effects*
Magnoliopsida / growth & development
Microcystins / physiology*
Microcystis / physiology*

Substances

Microcystins