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Open Access Research article

Protein evolution in two co-occurring types of Symbiodinium: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D

Jason T Ladner*, Daniel J Barshis and Stephen R Palumbi

Author Affiliations

Department of Biology, Stanford University, Hopkins Marine Station, 93950, Pacific Grove, CA USA

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BMC Evolutionary Biology 2012, 12:217  doi:10.1186/1471-2148-12-217

Published: 12 November 2012

Abstract

Background

The symbiosis between reef-building corals and photosynthetic dinoflagellates (Symbiodinium) is an integral part of the coral reef ecosystem, as corals are dependent on Symbiodinium for the majority of their energy needs. However, this partnership is increasingly at risk due to changing climatic conditions. It is thought that functional diversity within Symbiodinium may allow some corals to rapidly adapt to different environments by changing the type of Symbiodinium with which they partner; however, very little is known about the molecular basis of the functional differences among symbiont groups. One group of Symbiodinium that is hypothesized to be important for the future of reefs is clade D, which, in general, seems to provide the coral holobiont (i.e., coral host and associated symbiont community) with elevated thermal tolerance. Using high-throughput sequencing data from field-collected corals we assembled, de novo, draft transcriptomes for Symbiodinium clades C and D. We then explore the functional basis of thermal tolerance in clade D by comparing rates of coding sequence evolution among the four clades of Symbiodinium most commonly found in reef-building corals (A-D).

Results

We are able to highlight a number of genes and functional categories as candidates for involvement in the increased thermal tolerance of clade D. These include a fatty acid desaturase, molecular chaperones and proteins involved in photosynthesis and the thylakoid membrane. We also demonstrate that clades C and D co-occur within most of the sampled colonies of Acropora hyacinthus, suggesting widespread potential for this coral species to acclimatize to changing thermal conditions via ‘shuffling’ the proportions of these two clades from within their current symbiont communities.

Conclusions

Transcriptome-wide analysis confirms that the four main Symbiodinium clades found within corals exhibit extensive evolutionary divergence (18.5-27.3% avg. pairwise nucleotide difference). Despite these evolutionary distinctions, many corals appear to host multiple clades simultaneously, which may allow for rapid acclimatization to changing environmental conditions. This study provides a first step toward understanding the molecular basis of functional differences between Symbiodinium clades by highlighting a number of genes with signatures consistent with positive selection along the thermally tolerant clade D lineage.

Keywords:
Symbiodinium; Thermal tolerance; Coral; Symbiosis; Dinoflagellate; Transcriptome; Zooxanthellae; High-throughput sequencing; Symbiont shuffling