Deciphering the disturbance mechanism of BaP on the symbiosis of Montipora digitata via 4D-Proteomics approach

Chemosphere. 2023 Jan;312(Pt 1):137223. doi: 10.1016/j.chemosphere.2022.137223. Epub 2022 Nov 10.

Abstract

The coral holobiont is mainly composed of coral polyps, zooxanthellae, and coral symbiotic microorganisms, which form the basis of coral reef ecosystems. In recent years, the severe degradation of coral reefs caused by climate warming and environmental pollution has aroused widespread concern. Benzo(a)pyrene (BaP) is a widely distributed pollutant in the environment. However, the underlying mechanisms of coral symbiosis destruction due to the stress of BaP are not well understood. In this study, diaPASEF proteomics and 16S rRNA amplicon pyrosequencing technology were used to reveal the effects of 50 μg/L BaP on Montipora digitate. Data analysis was performed from the perspective of the main symbionts of M. digitata (coral polyps, zooxanthellae, and coral symbiotic microorganisms). The results showed that BaP impaired cellular antioxidant capacity by disrupting the GSH/GSSG cycle, and sustained stress causes severe impairment of energy metabolism and protein degradation in coral polyps. In zooxanthellae, BaP downregulated the protein expression of SOD2 and mtHSP70, which then resulted in oxidative free radical accumulation and apoptosis. For coral symbiotic microorganisms, BaP altered the community structure of microorganisms and decreased immunity. Coral symbiotic microorganisms adapted to the stress of BaP by adjusting energy metabolism and enhancing extracellular electron transfer. BaP adversely affected the three main symbionts of M. digitata via different mechanisms. Decreased antioxidant capacity is a common cause of damages to coral polyps and zooxanthellae, whereas coral symbiotic microorganisms are able to appropriately adapt to oxidative stress. This study assessed the effects of BaP on corals from a symbiotic perspective, which is more comprehensive and reliable. At the same time, data from the study supports new directions for coral research and coral reef protection.

Keywords: BaP; Coral holobionts; Coral polyps; Coral symbiotic microorganisms; Zooxanthellae.

MeSH terms

  • Animals
  • Anthozoa* / metabolism
  • Antioxidants / metabolism
  • Coral Reefs
  • Ecosystem
  • Proteomics
  • RNA, Ribosomal, 16S / metabolism
  • Symbiosis*

Substances

  • Antioxidants
  • RNA, Ribosomal, 16S