Symbiosis induces widespread changes in the proteome of the model cnidarian Aiptasia

Cell Microbiol. 2016 Jul;18(7):1009-23. doi: 10.1111/cmi.12564. Epub 2016 Feb 5.

Abstract

Coral reef ecosystems are metabolically founded on the mutualism between corals and photosynthetic dinoflagellates of the genus Symbiodinium. The glass anemone Aiptasia sp. has become a tractable model for this symbiosis, and recent advances in genetic information have enabled the use of mass spectrometry-based proteomics in this model. We utilized label-free liquid chromatography electrospray-ionization tandem mass spectrometry to analyze the effects of symbiosis on the proteomes of symbiotic and aposymbiotic Aiptasia. We identified and obtained relative quantification of more than 3,300 proteins in 1,578 protein clusters, with 81 protein clusters showing significantly different expression between symbiotic states. Symbiotic anemones showed significantly higher expression of proteins involved in lipid storage and transport, nitrogen transport and cycling, intracellular trafficking, endocytosis and inorganic carbon transport. These changes reflect shifts in host metabolism and nutrient reserves due to increased nutritional exchange with the symbionts, as well as mechanisms for supplying inorganic nutrients to the algae. Aposymbiotic anemones exhibited increased expression of multiple systems responsible for mediating reactive oxygen stress, suggesting that the host derives direct or indirect protection from oxidative stress while in symbiosis. Aposymbiotic anemones also increased their expression of an array of proteases and chitinases, indicating a metabolic shift from autotrophy to heterotrophy. These results provide a comprehensive Aiptasia proteome with more direct relative quantification of protein abundance than transcriptomic methods. The extension of "omics" techniques to this model system will allow more powerful studies of coral physiology, ecosystem function, and the effects of biotic and abiotic stress on the coral-dinoflagellate mutualism.

Keywords: Aiptasia; coral reefs; microbial-cell interaction; model organisms; proteomics; symbiosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chromatography, Liquid / methods
  • Dinoflagellida / physiology*
  • Endocytosis
  • Heterotrophic Processes
  • Lipid Metabolism
  • Nitrogen / metabolism
  • Proteome / analysis*
  • Proteome / metabolism
  • Sea Anemones / physiology*
  • Spectrometry, Mass, Electrospray Ionization / methods
  • Symbiosis*
  • Tandem Mass Spectrometry / methods

Substances

  • Proteome
  • Nitrogen