High natural gene expression variation in the reef-building coral Acropora millepora: potential for acclimative and adaptive plasticity

Background: Ecosystems worldwide are suffering the consequences of anthropogenic impact. The diverse ecosystem of coral reefs, for example, are globally threatened by increases in sea surface temperatures due to global warming. Studies to date have focused on determining genetic diversity, the sequence variability of genes in a species, as a proxy to estimate and predict the potential adaptive response of coral populations to environmental changes linked to climate changes. However, the examination of natural gene expression variation has received less attention. This variation has been implicated as an important factor in evolutionary processes, upon which natural selection can act. Results: We acclimatized coral nubbins from six colonies of the reef-building coral Acropora millepora to a common garden in Heron Island (Great Barrier Reef, GBR) for a period of four weeks to remove any site-specific environmental effects on the physiology of the coral nubbins. By using a cDNA microarray platform, we detected a high level of gene expression variation, with 17% (488) of the unigenes differentially expressed across coral nubbins of the six colonies (jsFDR-corrected, p < 0.01). Among the main categories of biological processes found differentially expressed were transport, translation, response to stimulus, oxidation-reduction processes, and apoptosis. We found that the transcriptional profiles did not correspond to the genotype of the colony characterized using either an intron of the carbonic anhydrase gene or microsatellite loci markers. Conclusion: Our results provide evidence of the high inter-colony variation in A. millepora at the transcriptomic level grown under a common garden and without a correspondence with genotypic identity. This finding brings to our attention the importance of taking into account natural variation between reef corals when assessing experimental gene expression differences. The high transcriptional variation detected in this study is interpreted and discussed within the context of adaptive potential and phenotypic plasticity of reef corals. Whether this variation will allow coral reefs to survive to current challenges remains unknown.

Acclimatization of the tropical reef coral Acropora millepora to hyperthermal stress

The demise of reef-building corals potentially lies on the horizon, given ongoing climate change amid other anthropogenic environmental stressors. If corals cannot acclimatize or adapt to changing conditions, dramatic declines in the extent and health of the living reefs are expected within the next half century. The primary and proximal global threat to corals is climate change. Reef-building corals are dependent upon a nutritional symbiosis with photosynthetic dinoflagellates belonging to the group Symbiodinium. . The symbiosis between the cnidarian host and algal partner is a stress-sensitive relationship; temperatures just 1°C above normal thermal maxima can result in the breakdown of the symbiosis, resulting in coral bleaching (the loss of Symbiodinium and/or associated photopigments) and ultimately, colony death. As ocean temperatures continue to rise, corals will either acclimatize or adapt to changing conditions, or will perish. By experimentally preconditioning the coral Acropora millepora via sublethal heat treatment, the coral acquired thermal tolerance, resisting bleaching during subsequent hyperthermal stress. The complex nature of the coral holobiont translates to multiple possible explanations for acclimatization: acquired thermal tolerance could potentially originate from the host itself, the Symbiodinium, or from the bacterial community associated with the coral. By examining the type of in hospite Symbiodinium and the bacterial community prior acclimation and after thermal challenge, it is shown that short-term acclimatization is not due to a distinct change in the dinoflagellate or prokaryote community. Though the microbial partnerships remain without considerable flux in preconditioned corals, the host transcriptome is dynamic. One dominant pattern was the apparent tuning of gene expression observed between preconditioned and non-preconditioned treatments, showing a modulated transcriptomic response to stress. Additionally several genes were upregulated in association with thermal tolerance, including antiapoptotic genes, lectins, and oxidative stress response genes. Upstream of two of these thermal tolerance genes, inhibitor of NFκB and mannose-binding lectin, DNA polymorphisms were identified which vary significantly between the northern and southern Great Barrier Reef. The impact of these mutations in putative promoter regions remains to be seen, but variation across thermally-disparate geography serves to generate hypotheses regarding the role of regulatory element evolution in a coral adaptation context.