Coral-zooxanthellae meta-transcriptomics reveals integrated response to pollutant stress

Abstract

BackgroundCorals represent symbiotic meta-organisms that require harmonization among the coral animal, photosynthetic zooxanthellae and associated microbes to survive environmental stresses. We investigated integrated-responses among coral and zooxanthellae in the scleractinian coral Acropora formosa in response to an emerging marine pollutant, the munitions constituent, 1,3,5-trinitro-1,3,5 triazine (RDX; 5 day exposures to 0 (control), 0.5, 0.9, 1.8, 3.7, and 7.2 mg/L, measured in seawater).ResultsRDX accumulated readily in coral soft tissues with bioconcentration factors ranging from 1.1 to 1.5. Next-generation sequencing of a normalized meta-transcriptomic library developed for the eukaryotic components of the A. formosa coral holobiont was leveraged to conduct microarray-based global transcript expression analysis of integrated coral/zooxanthellae responses to the RDX exposure. Total differentially expressed transcripts (DET) increased with increasing RDX exposure concentrations as did the proportion of zooxanthellae DET relative to the coral animal. Transcriptional responses in the coral demonstrated higher sensitivity to RDX compared to zooxanthellae where increased expression of gene transcripts coding xenobiotic detoxification mechanisms (i.e. cytochrome P450 and UDP glucuronosyltransferase 2 family) were initiated at the lowest exposure concentration. Increased expression of these detoxification mechanisms was sustained at higher RDX concentrations as well as production of a physical barrier to exposure through a 40% increase in mucocyte density at the maximum RDX exposure. At and above the 1.8 mg/L exposure concentration, DET coding for genes involved in central energy metabolism, including photosynthesis, glycolysis and electron-transport functions, were decreased in zooxanthellae although preliminary data indicated that zooxanthellae densities were not affected. In contrast, significantly increased transcript expression for genes involved in cellular energy production including glycolysis and electron-transport pathways was observed in the coral animal.ConclusionsTranscriptional network analysis for central energy metabolism demonstrated highly correlated responses to RDX among the coral animal and zooxanthellae indicative of potential compensatory responses to lost photosynthetic potential within the holobiont. These observations underscore the potential for complex integrated responses to RDX exposure among species comprising the coral holobiont and highlight the need to understand holobiont-species interactions to accurately assess pollutant impacts.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-591) contains supplementary material, which is available to authorized users.

Review and synthesis of evidence regarding environmental risks posed by munitions constituents (MC) in aquatic systems

“…The presence of TNT and its transformation products in the bile may be suitable as a direct marker of TNT exposure in fish at contaminated sites (Ek et al 2005). Gust et al (2014) demonstrated increased expression of cytochrome P450 in coral (Acropora formosa) that was exposed to RDX as a mechanism of detoxification. In addition, potential insult to coral health was evidenced by the significant increase of coral mucocyte densities at the maximum RDX exposure (7.2 mg/L).…”

“…Exposure to RDX at 28 mg/L or higher concentrations failed to elicit mortality in adult mussels, Dungeness crabs, mysid shrimp, polychaetes, cnidarians, midges, amphipods, cladocerans, and copepods (Peters et al 1991;Burton et al 1993;Dave et al 2000;Nipper et al 2001;ENSR International 2005;Rosen and Lotufo 2007a). Exposure to RDX at 7.2 mg/L failed to elicit mortality of the coral Acropora formosa (Gust et al 2014). …”

Caribbean yellow band disease compromises the activity of catalase and glutathione S-transferase in the reef-building coral Orbicella faveolata exposed to anthracene

“…The stability of these associations plays an important role in coral health (Mouchka et al 2010); therefore, a permanent or a transitory impairment of these relationships might also disrupt the mechanisms of defense of corals to xenobiotic compounds. For example, it is widely accepted that zooxanthellae play an important role in the detoxification and bioaccumulation process, in some cases exhibiting higher activity levels for some antioxidant, anti xenobiotic enzymes and higher concentration of accumulated compounds compared to the coral polyp (Kennedy et al 1992, Gust et al 2014. In other experiments, the exposure of Porites divaricata to fluoranthene (another PAH similar to anthracene) at concentrations similar to the ones we used led to a diminished photosynthetic efficiency and eventually to bleaching in branches exposed to sunlight (Guzmán-Martínez et al 2007).…”

“…Thus, these enzymes are very important as they protect corals from the deleterious effects of different stressors. While different studies have shown that healthy corals increase the activity of these enzymes when exposed to pollutants (Venn et al 2009, Gust et al 2014, no studies have determined whether diseased corals fail to activate these mechanisms under controlled exposure to xenobiotic compounds.…”

Molecular mechanisms of acclimation to long‐term elevated temperature exposure in marine symbioses

“…The glyceraldehyde-3-phosphate pathway, which culminates in glycerol production, was also significantly affected by sublethal elevated temperature (30°C) exposure in the reef coral P. damicornis (Mayfield et al, 2014). Pollutant exposure also altered the expression of genes involved in carbohydrate metabolism, albeit only in the coral host compartment (and not in Symbiodiniaceae) in another study (Gust et al, 2014). Admittedly, we did not assess the proportion of energy derived from autotrophy herein, which ranges widely (from 25% to up to 100%) and is dependent on the species and/or life history stage in the Tridacna genus (Fisher, Fitt, & Trench, 1985;Klumpp et al, 1992;Klumpp & Griffiths, 1994); shifts from autotrophy to heterotrophy, and vice versa, are likely to affect host gene expression patterns.…”