Opinion
Cell biology in model systems as the key to understanding corals

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Corals provide the foundation of important tropical reef ecosystems but are in global decline for multiple reasons, including climate change. Coral health depends on a fragile partnership with intracellular dinoflagellate symbionts. We argue here that progress in understanding coral biology requires intensive study of the cellular processes underlying this symbiosis. Such study will inform us on how the coral symbiosis will be affected by climate change, mechanisms driving coral bleaching and disease, and the coevolution of this symbiosis in the context of other host–microbe interactions. Drawing lessons from the broader history of molecular and cell biology and the study of other host–microbe interactions, we argue that a model-systems approach is essential for making effective progress in understanding coral cell biology.

Introduction

Reef-building corals are composed of mutualistic partnerships, or symbioses, between cnidarian hosts, their photosynthetic dinoflagellate endosymbionts and a complex community of microbes. These partnerships form the trophic and structural foundations of the coral reef ecosystem (Figure 1a) [1]. Much is known about the ecology and evolution of corals 1, 2. There has also been significant progress during the past 15 years in understanding the cnidarian–dinoflagellate symbiosis, especially in the areas of host and symbiont diversity, phylogenetics and population structure 3, 4. Furthermore, recently launched functional-genomic studies hold the promise of providing an enormous amount of information about patterns of gene expression both during healthy symbiosis and during stress 5, 6, 7. However, there has been little recent progress in the understanding of host–symbiont interactions at the cellular and molecular levels, such as the mechanisms of recognition and specificity and the modes of inter-partner communication and regulation (e.g. of nutrient exchange and cell division). Gaining detailed insight into these mechanisms has now become critical to our understanding of the response of corals to environmental stresses.

Coral reefs are declining globally, owing to multiple factors that include reduced water quality, over-exploitation of key coral reef species and climate change, which has driven increasingly destructive mass bleaching and mortality events since 1979 [8]. Even in relatively unstressed oceans, such as the Pacific, coral cover has declined by 2% per year over the past 10 years [9]. Climate change is affecting coral reefs in at least two fundamental ways. The first is through ocean acidification, arising from increased concentrations of atmospheric carbon dioxide entering the ocean and decreasing the oceanic concentrations of carbonate ions, and hence reducing coral calcification which is dependent on carbonate [10]. The second way that climate change is affecting coral reefs is via increased sea temperatures that have driven increasingly intense and frequent coral bleaching across thousands of square miles of reefs (Figure 1b) [8]. Coral bleaching occurs when the symbiosis becomes dysfunctional and algal symbionts are lost from the coral tissues [11]. It results in decreased growth, increased susceptibility to disease and dramatically increased mortality 8, 11. We still have very little insight into the underlying cellular mechanisms responsible for bleaching.

Here we argue that we need to develop and use genomic and cell biology resources in the study of cnidarian–dinoflagellate symbiosis and that such an effort will provide insight into the ecology and evolution of this critically important symbiosis. (Our views were crystallized by a recent international workshop that brought coral biologists together with cell biologists and host–microbe interaction biologists to examine the challenges and opportunities in the study of coral cell biology.) We will (i) illustrate how knowledge of the cell biology of cnidarian–dinoflagellate symbioses can inform the study of their ecology and evolution, (ii) explain the value of experimentally tractable model systems in cell biology in general and in host–microbe interactions in particular, (iii) outline the current status of coral cell biology and argue for the adoption of a model-systems approach and (iv) identify key research priorities in the field.

Section snippets

Host–symbiont specificity and flexibility

Thousands of species of cnidarians engage in symbiosis with a large diversity of dinoflagellates from the genus Symbiodinium (Box 1). With the advent of molecular tools, the biodiversity of the separate partners has become increasingly well documented 3, 12, but the diversity of host–symbiont combinations is astonishingly complex and still poorly understood 13, 14. Considerable effort has been devoted to sampling symbiont types in corals across a variety of spatial and temporal scales [14].

Model systems for the study of cell biology

The past 50 years have seen enormous progress in molecular, cell and developmental biology. Much of this progress has come from studies in a small number of intensively studied model organisms: the bacterium Escherichia coli and its viruses, the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe, the nematode worm Caenorhabditis elegans, the fruit fly Drosophila melanogaster, the small mustard plant Arabidopsis thaliana, the mouse Mus musculus and a few lines of cultured mammalian

Current status of technique development

We believe that progress in understanding the cellular mechanisms underlying the cnidarian–dinoflagellate symbiosis will depend on the resources and tools that are available at both the molecular (including genomic) and cellular levels and on a move toward the use of model systems. Table 2 presents the current status of genomic and cell biological technique development in cnidarian–dinoflagellate symbioses and Box 2 illustrates how these tools can be used to examine their cell biology. These

Future research priorities

In summary, we believe that rapid progress in the study of coral cell biology will greatly contribute to an understanding of coral ecology and evolution. Below we outline key priorities for future research.

Acknowledgements

The information and opinions provided by the 50 participants at the international workshop entitled ‘New Frontiers in Cellular Interactions in Cnidarian–Dinoflagellate Symbioses,’ held in January 2007 at Heron Island Research Station, Australia, contributed greatly to the development of our perspectives on coral cell biology as expressed in this article. The workshop was funded by grants from (i) the US National Science Foundation (OISE:0605804), (ii) the Australian Research Council Centre of

References (72)

  • D. Zoccola

    Molecular cloning and localization of a PMCA P-type calcium ATPase from the coral Stylophora pistillata

    Biochim. Biophys. Acta

    (2004)
  • H. Yokouchi

    In situ identification of symbiotic dinoflagellates, the genus Symbiodinium with fluorescence-labeled rRNA-targeted oligonucleotide probes

    J. Microbiol. Methods

    (2003)
  • T. Hunter

    The energetics of asexual reproduction: pedal laceration in the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943)

    J. Exp. Mar. Biol. Ecol.

    (1984)
  • Z. Dubinsky

    Coral Reefs

    (1990)
  • C. Birkeland

    Life and Death of Coral Reefs

    (1996)
  • J.N. Underwood

    Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching

    Mol. Ecol.

    (2007)
  • M. Rodriguez-Lanetty

    Transcriptome analysis of a cnidarian–dinoflagellate mutualism reveals complex modulation of host gene expression

    BMC Genomics

    (2006)
  • Schwarz, J.A. et al. (2006) Coral reef genomics: developing tools for functional genomics of coral symbiosis. In...
  • W. Leggat

    Analysis of an EST library from the dinoflagellate (Symbiodinium sp.) symbiont of reef-building corals

    J. Phycol.

    (2007)
  • O. Hoegh-Guldberg

    Climate change, coral bleaching and the future of the world's coral reefs

    Mar. Freshwater Res.

    (1999)
  • J.F. Bruno et al.

    Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons

    PLoS ONE

    (2007)
  • J. Raven

    Ocean Acidification Due to Increasing Atmospheric Carbon Dioxide

    (2005)
  • B.E. Brown

    Coral bleaching: causes and consequences

    Coral Reefs

    (1997)
  • S.V. Vollmer et al.

    Hybridization and the evolution of reef coral diversity

    Science

    (2002)
  • A.C. Baker

    Flexibility and specificity in coral-algal symbiosis: diversity, ecology and biogeography of Symbiodinium

    Annu. Rev. Ecol. Evol. Syst.

    (2003)
  • T.L. Goulet

    Most corals may not change their symbionts

    Mar. Ecol. Prog. Ser.

    (2006)
  • R. Berkelmans et al.

    The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change

    Proc. Biol. Sci.

    (2006)
  • A.C. Baker

    Ecosystems: reef corals bleach to survive change

    Nature

    (2001)
  • O. Hoegh-Guldberg

    Ecology (communication arising): is coral bleaching really adaptive?

    Nature

    (2002)
  • E.M. Wood-Charlson

    Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis

    Cell. Microbiol.

    (2006)
  • C.A. Belda-Baillie

    Specificity of a model cnidarian–dinoflagellate symbiosis

    Biol. Bull.

    (2002)
  • A.F. Little

    Flexibility in algal endosymbioses shapes growth in reef corals

    Science

    (2004)
  • R.D. Gates

    Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching

    Biol. Bull.

    (1992)
  • S.R. Dunn

    Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose

    Proc. Biol. Sci.

    (2007)
  • S.R. Dunn

    Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration

    Cell Death Differ.

    (2004)
  • S. Perez et al.

    Nitric oxide and cnidarian bleaching: an eviction notice mediates the breakdown of symbiosis

    J. Exp. Biol.

    (2006)
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