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Open Access Research article

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

Kurt A Gust1*, Fares Z Najar2, Tanwir Habib3, Guilherme R Lotufo1, Alan M Piggot45, Bruce W Fouke46, Jennifer G Laird1, Mitchell S Wilbanks1, Arun Rawat7, Karl J Indest1, Bruce A Roe4 and Edward J Perkins1

Author Affiliations

1 US Army Engineer Research and Development Center, Environmental Laboratory, Vicksburg, MS 39180, USA

2 Advanced Center for Genome Technology, University of Oklahoma, Norman, OK 73019, USA

3 Badger Technical Services, San Antonio, TX 71286, USA

4 Department of Geology, Urbana-Champaign, University of Illinois, Urbana-Champaign, IL 31801, USA

5 Division of Marine Geology and Geophysics, University of Miami, Miami, FL 33149, USA

6 University of Illinois, Institute for Genomic Biology, Urbana-Champaign, Illinois, IL 31801, USA

7 Translational Genomics Research Institute, Phoenix, AZ 85004, USA

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BMC Genomics 2014, 15:591  doi:10.1186/1471-2164-15-591

Published: 12 July 2014

Abstract

Background

Corals 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).

Results

RDX 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.

Conclusions

Transcriptional 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.

Keywords:
Coral holobiont; Marine pollution; Meta-transcriptomics; Acropora; Zooxanthellae; RDX; Symbiosis; Transcriptional network; Next generation sequencing