Metabolic changes in Medaka fish induced by cyanobacterial exposures in mesocosms: an integrative approach combining proteomic and metabolomic analyses

Abstract

Cyanobacterial blooms pose serious threats to aquatic organisms and strongly impact the functioning of aquatic ecosystems. Due to their ability to produce a wide range of potentially bioactive secondary metabolites, so called cyanotoxins, cyanobacteria have been extensively studied in the past decades. Proteomic and metabolomic analyses provide a unique opportunity to evaluate the global response of hundreds of proteins and metabolites at a glance. In this study, we provide the first combined utilization of these methods targeted to identify the response of fish to bloom-forming cyanobacteria. Medaka fish (Oryzias latipes) were exposed for 96 hours either to a MC-producing or to a non-MC-producing strain of Microcystis aeruginosa and cellular, proteome and metabolome changes following exposure to cyanobacteria were characterized in the fish livers. The results suggest that a short-term exposure to cyanobacteria, producing or not MCs, induces sex-dependent molecular changes in medaka fish, without causing any cellular alterations. Globally, molecular entities involved in stress response, lipid metabolism and developmental processes exhibit the most contrasted changes following a cyanobacterial exposure. Moreover, it appears that proteomic and metabolomic analyses are useful tools to verify previous information and to additionally bring new horizons concerning molecular effects of cyanobacteria on fish.

Fish metabolome from sub-urban lakes of the Paris area (France) and potential influence of noxious metabolites produced by cyanobacteria

“…In addition, greater amounts of amino acids, di-peptides and acylcarnitines could be related to higher protein catabolism and betaoxidation in the liver of fish originating from the "Tri/Var/Ver" lakes, hypothetically traducing higher energetic requirements for those organisms. Taken together, these observations are in agreement with the hypothesis of the occurrence of higher stress conditions locally occurring in the Tri, Var and Ver lakes, in correspondence with the local production of potentially noxious metabolites by cyanobacterial proliferation (Sotton et al, 2017a(Sotton et al, , 2017bLe Manach et al, 2018). In general, various genetic or phenotypic factors (such as development stages, contamination levels, predator/parasite pressures, food availability, …) could influence and explain lthe ocal discrepancy of the metabolome of fishes collected from different environments (reviewed in Marie 2020).…”

“…Environmental stressors are known to induce biological variations, concerning the specific physiological, developmental and reproductive capabilities of the different fish species allowing them to colonize and occupy ecosystems (Hamilton et al, 2016). As cyanobacterial blooms are one of the most common stress encountered by organisms living in modern freshwater lentic systems around the world (Harke et al, 2016;Burford et al, 2020), several recent efforts have been attempted to characterize the potential effect of cyanobacteria proliferation on various fish species according to experimentation performed in the lab, in mesocosms, or from field sampling (Amado et al, 2010;Ferrao-Filho et al, 2011;Sotton et al, 2017aSotton et al, , 2017bLe Manach et al, 2018). To this end, we initially investigated the liver metabolome of fish collected from different lakes encountering low or high cyanobacterial proliferation by 1 H NMR technics (Sotton et al, 2019).…”

The metabolic regulation of dietary L‐carnitine in aquaculture nutrition: present status and future research strategies

“…; Sotton et al . ) in exploring biological characteristics and metabolic regulation pathways in nutritional metabolism in animals. Therefore, these technologies should also be applied to explore the effect and mechanism of dietary L‐carnitine on nutritional metabolism in different fish species to explain the controversial results.…”

Fish Pathology Research and Diagnosis in Aquaculture of Farmed Fish; a Proteomics Perspective

“…Like the shotgun proteomic approach of serum proteins from turbot infected by Edwardsiella tarda , showing that immunoglobulins and complement component proteins were important antimicrobial proteins [ 202 ]. Or the study on Infections by Mycrocystis aeruginosa infections on medaka ( Oryzias latipes ) fish, that showed differences in liver proteins such as stress response, lipid metabolism and developmental processes [ 203 ].…”