Bloom-forming planktonic Microcystis and benthic Oscillatoria-induced oxidative stress and inflammatory responses in juvenile silver carp and bighead carp

Huiting Yang; Yujia Yao; Xiaohong Gu; Huihui Chen; Qingfei Zeng; Zhigang Mao; Tao Xiang

doi:10.1016/j.toxicon.2024.108183

Bloom-forming planktonic Microcystis and benthic Oscillatoria-induced oxidative stress and inflammatory responses in juvenile silver carp and bighead carp

Toxicon. 2024 Nov 20:108183. doi: 10.1016/j.toxicon.2024.108183. Online ahead of print.

Authors

Huiting Yang¹, Yujia Yao¹, Xiaohong Gu², Huihui Chen³, Qingfei Zeng³, Zhigang Mao⁴, Tao Xiang³

Affiliations

¹ Key Laboratory of Lake and Watershed Science for Water Security, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China; State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China; University of Chinese Academy of Sciences, Beijing 100049, China.
² Key Laboratory of Lake and Watershed Science for Water Security, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China; State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China; Jiangsu Collaborative Innovation Center of Regional Modern Agriculture & Environmental Protection, Huaiyin Normal University, Huaian 223300, China. Electronic address: xhgu@niglas.ac.cn.
³ Key Laboratory of Lake and Watershed Science for Water Security, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China; State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China.
⁴ Key Laboratory of Lake and Watershed Science for Water Security, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China; State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China. Electronic address: zgmao@niglas.ac.cn.

PMID: 39577703
DOI: 10.1016/j.toxicon.2024.108183

Abstract

As global warming and water eutrophication, the multiple proliferation of harmful cyanobacteria can form algal blooms and cause serious ecological problems. In recent years, the large-scale and persistent cyanobacterial blooms occur frequently worldwide and have attracted widespread attention due to the harmful impacts. Among these harmful bloom-forming cyanobacteria, the ecological and toxicological impacts of planktonic cyanobacteria have been extensively studied. However, research on the ecological risks and adverse effects of harmful benthic cyanobacteria is lagging. Filter-feeding fish could suffer from more toxic stimuli than other fish due to their special feeding habits. To investigate and compare the complex toxic effects of different kinds of harmful cyanobacteria on fish, three different-sized (i.e. small, medium, and large) juvenile silver carp (Hypophthalmichthys molitrix) and bighead carp (Aristichthys nobilis) were exposed to cyanobacterial blooms-related density (1 × 10⁶ cells/mL) of Microcystis aeruginosa ( i.e. generating microcystins) and Oscillatoria sp. (i.e. generating cylindrospermopsin) for 3 d, after which biomarkers of oxidative stress and inflammation in the liver of fish were detected. The silver carp and bighead carp can effectively ingest Microcystis cells but cannot effectively ingest Oscillatoria cells through the measurement of the levels of cyanotoxins. Both Microcystis and Oscillatoria cells can induce different levels of oxidative stress and inflammatory responses in the liver of these juvenile filter-feeding fish via altering the biochemical parameters of the antioxidant system (e.g. superoxide dismutase activity) and immune system (e.g. interleukin-1β level). Therefore, our research identified potential data gaps that how the different types of cyanobacteria induce toxic effects in the liver of juvenile filter-feeding fish in a short time. This study contributes to a better understanding of the short-term adverse effects of different cyanobacterial species on juvenile fish, suggesting that the benthic toxic cyanobacteria-induced ecological and health risks require further attention.

Keywords: Filter-feeding fish; Inflammation; Microcystis aeruginosa; Oscillatoria sp.; Oxidative stress.