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

Kurt A. Gust, Fares Z. Najar, Tanwir Habib, Guilherme R. Lotufo, Alan M. Piggot, Bruce W. Fouke, Jennifer G. Laird, Mitchell S. Wilbanks, Arun Rawat, Karl J. Indest, Bruce A. Roe, Edward J. Perkins

Research output: Contribution to journalArticle

12 Citations (Scopus)

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.

Original languageEnglish
Article number591
JournalBMC Genomics
Volume15
Issue number1
DOIs
Publication statusPublished - 12 Jul 2014
Externally publishedYes

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Anthozoa
Glycolysis
Electron Transport
Taiwan
Energy Metabolism
cyclonite
Gene Expression
Glucuronosyltransferase
Architectural Accessibility
Gene Regulatory Networks
Photosynthesis
Seawater
Gene Expression Profiling
Xenobiotics
Cytochrome P-450 Enzyme System
Libraries

Keywords

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

ASJC Scopus subject areas

  • Biotechnology
  • Genetics

Cite this

Gust, K. A., Najar, F. Z., Habib, T., Lotufo, G. R., Piggot, A. M., Fouke, B. W., ... Perkins, E. J. (2014). Coral-zooxanthellae meta-transcriptomics reveals integrated response to pollutant stress. BMC Genomics, 15(1), [591]. https://doi.org/10.1186/1471-2164-15-591

Coral-zooxanthellae meta-transcriptomics reveals integrated response to pollutant stress. / Gust, Kurt A.; Najar, Fares Z.; Habib, Tanwir; Lotufo, Guilherme R.; Piggot, Alan M.; Fouke, Bruce W.; Laird, Jennifer G.; Wilbanks, Mitchell S.; Rawat, Arun; Indest, Karl J.; Roe, Bruce A.; Perkins, Edward J.

In: BMC Genomics, Vol. 15, No. 1, 591, 12.07.2014.

Research output: Contribution to journalArticle

Gust, KA, Najar, FZ, Habib, T, Lotufo, GR, Piggot, AM, Fouke, BW, Laird, JG, Wilbanks, MS, Rawat, A, Indest, KJ, Roe, BA & Perkins, EJ 2014, 'Coral-zooxanthellae meta-transcriptomics reveals integrated response to pollutant stress', BMC Genomics, vol. 15, no. 1, 591. https://doi.org/10.1186/1471-2164-15-591
Gust KA, Najar FZ, Habib T, Lotufo GR, Piggot AM, Fouke BW et al. Coral-zooxanthellae meta-transcriptomics reveals integrated response to pollutant stress. BMC Genomics. 2014 Jul 12;15(1). 591. https://doi.org/10.1186/1471-2164-15-591
Gust, Kurt A. ; Najar, Fares Z. ; Habib, Tanwir ; Lotufo, Guilherme R. ; Piggot, Alan M. ; Fouke, Bruce W. ; Laird, Jennifer G. ; Wilbanks, Mitchell S. ; Rawat, Arun ; Indest, Karl J. ; Roe, Bruce A. ; Perkins, Edward J. / Coral-zooxanthellae meta-transcriptomics reveals integrated response to pollutant stress. In: BMC Genomics. 2014 ; Vol. 15, No. 1.
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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.",
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AU - Gust, Kurt A.

AU - Najar, Fares Z.

AU - Habib, Tanwir

AU - Lotufo, Guilherme R.

AU - Piggot, Alan M.

AU - Fouke, Bruce W.

AU - Laird, Jennifer G.

AU - Wilbanks, Mitchell S.

AU - Rawat, Arun

AU - Indest, Karl J.

AU - Roe, Bruce A.

AU - Perkins, Edward J.

PY - 2014/7/12

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N2 - 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.

AB - 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.

KW - Acropora

KW - Coral holobiont

KW - Marine pollution

KW - Meta-transcriptomics

KW - Next generation sequencing

KW - RDX

KW - Symbiosis

KW - Transcriptional network

KW - Zooxanthellae

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