Heat-stress and light-stress induce different cellular pathologies in the symbiotic dinoflagellate during coral bleaching

PLoS One. 2013 Dec 4;8(12):e77173. doi: 10.1371/journal.pone.0077173. eCollection 2013.

Abstract

Coral bleaching is a significant contributor to the worldwide degradation of coral reefs and is indicative of the termination of symbiosis between the coral host and its symbiotic algae (dinoflagellate; Symbiodinium sp. complex), usually by expulsion or xenophagy (symbiophagy) of its dinoflagellates. Herein, we provide evidence that during the earliest stages of environmentally induced bleaching, heat stress and light stress generate distinctly different pathomorphological changes in the chloroplasts, while a combined heat- and light-stress exposure induces both pathomorphologies; suggesting that these stressors act on the dinoflagellate by different mechanisms. Within the first 48 hours of a heat stress (32°C) under low-light conditions, heat stress induced decomposition of thylakoid structures before observation of extensive oxidative damage; thus it is the disorganization of the thylakoids that creates the conditions allowing photo-oxidative-stress. Conversely, during the first 48 hours of a light stress (2007 µmoles m(-2) s(-1) PAR) at 25°C, condensation or fusion of multiple thylakoid lamellae occurred coincidently with levels of oxidative damage products, implying that photo-oxidative stress causes the structural membrane damage within the chloroplasts. Exposure to combined heat- and light-stresses induced both pathomorphologies, confirming that these stressors acted on the dinoflagellate via different mechanisms. Within 72 hours of exposure to heat and/or light stresses, homeostatic processes (e.g., heat-shock protein and anti-oxidant enzyme response) were evident in the remaining intact dinoflagellates, regardless of the initiating stressor. Understanding the sequence of events during bleaching when triggered by different environmental stressors is important for predicting both severity and consequences of coral bleaching.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anthozoa / radiation effects*
  • Chlorophyll / metabolism
  • Chloroplasts / radiation effects*
  • Chloroplasts / ultrastructure
  • Coral Reefs
  • Dinoflagellida / radiation effects*
  • Dinoflagellida / ultrastructure
  • Gene Expression
  • Heat-Shock Proteins / genetics
  • Heat-Shock Proteins / metabolism
  • Hot Temperature
  • Intracellular Membranes / radiation effects*
  • Intracellular Membranes / ultrastructure
  • Light
  • Microscopy, Electron, Transmission
  • Oxidation-Reduction
  • Oxidative Stress
  • Photolysis
  • Protozoan Proteins / genetics
  • Protozoan Proteins / metabolism
  • Stress, Physiological
  • Symbiosis
  • Temperature

Substances

  • Heat-Shock Proteins
  • Protozoan Proteins
  • Chlorophyll

Grants and funding

This study was supported by ISF grants 511/02 and 1169/07. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.