Abstract
Ocean acidification (OA) has both detrimental as well as beneficial effects on marine life; it negatively affects calcifiers while enhancing the productivity of photosynthetic organisms. To date, many studies have focused on the impacts of OA on calcification in reef-building corals, a process particularly susceptible to acidification. However, little is known about the effects of OA on their photosynthetic algal partners, with some studies suggesting potential benefits for symbiont productivity. Here, we investigated the transcriptomic response of the endosymbiont Symbiodinium microadriaticum (CCMP2467) in the Red Sea coral Stylophora pistillata subjected to different long-term (2 years) OA treatments (pH 8.0, 7.8, 7.4, 7.2). Transcriptomic analyses revealed that symbionts from corals under lower pH treatments responded to acidification by increasing the expression of genes related to photosynthesis and carbon-concentrating mechanisms. These processes were mostly up-regulated and associated metabolic pathways were significantly enriched, suggesting an overall positive effect of OA on the expression of photosynthesis-related genes. To test this conclusion on a physiological level, we analyzed the symbiont’s photochemical performance across treatments. However, in contrast to the beneficial effects suggested by the observed gene expression changes, we found significant impairment of photosynthesis with increasing pCO2. Collectively, our data suggest that over-expression of photosynthesis-related genes is not a beneficial effect of OA but rather an acclimation response of the holobiont to different water chemistries. Our study highlights the complex effects of ocean acidification on these symbiotic organisms and the role of the host in determining symbiont productivity and performance.
Highlights
Rising levels of anthropogenic carbon dioxide (CO2) are transforming the chemistry of our oceans; the average seawater pH has already decreased by 0.1 pH units since the Industrial Revolution and it is predicted to drop even further by the end of this century (Magnan et al, 2016; Hoegh-Guldberg et al, 2017)
We investigated the in hospite transcriptomic response of S. microadriaticum in the Red Sea coral S. pistillata under long-term (2 years) acidification stress
Based on previous evidence showing beneficial effects from elevated pCO2 on productivity (Strahl et al, 2015; Biscéré et al, 2019), we focused on genes and processes involved in photosynthesis and carbon acquisition, which were enriched in our differential gene expression analysis
Summary
Rising levels of anthropogenic carbon dioxide (CO2) are transforming the chemistry of our oceans; the average seawater pH has already decreased by 0.1 pH units (equivalent to almost 30% increase in acidity) since the Industrial Revolution and it is predicted to drop even further by the end of this century (Magnan et al, 2016; Hoegh-Guldberg et al, 2017). CO2 must be converted to HCO3− (and vice versa) so it can be transported inside the cell and reach RuBisCO, the enzyme that catalyzes the first step of CO2 fixation In hospite, this process is actively regulated by the host (Barott et al, 2015) through proteins like carbonic anhydrases and bicarbonate transporters that catalyze the interconversion of CO2 and bicarbonate and mediate their transport. This implies that the symbiont relies on the host to provide a suitable environment that supports its functioning (e.g., in hospite nutrient availability) so that if the physiological response of the latter is compromised, that of the symbiont will be too. Even if productivity of the holobiont increases under elevated pCO2 (Strahl et al, 2015; Biscéré et al, 2019), its performance and survival are limited by the physiological capabilities of the coral, which can either be negatively impacted (e.g., reduced metabolism, increased oxidative stress, apoptosis, etc.) (Kaniewska et al, 2012) or (seemingly) unaffected (Wall et al, 2014; Tambutté et al, 2015; Davies et al, 2018)
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