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Title: Coral Life History and Symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata

Abstract

Scleractinian corals are the foundation of reef ecosystems in tropical marine environments. Their great success is due to interactions with endosymbiotic dinoflagellates (Symbiodinium spp.), with which they are obligately symbiotic. To develop a foundation for studying coral biology and coral symbiosis, we have constructed a set of cDNA libraries and generated and annotated ESTs from two species of corals, Acropora palmata and Montastraea faveolata. Here we generated 14,588 (Ap) and 3,854 (Mf) high quality ESTs from five life history/symbiosis stages (spawned eggs, early-stage planula larvae, late-stage planula larvae either infected with symbionts or uninfected, and adult coral). The ESTs assembled into a set of primarily stage-specific clusters, producing 4,980 (Ap), and 1,732 (Mf) unigenes. The egg stage library, relative to the other developmental stages, was enriched in genes functioning in cell division and proliferation, transcription, signal transduction, and regulation of protein function. Fifteen unigenes were identified as candidate symbiosis-related genes as they were expressed in all libraries constructed from the symbiotic stages and were absent from all of the non symbiotic stages. These include several DNA interacting proteins, and one highly expressed unigene (containing 17 cDNAs) with no significant protein-coding region. A significant number of unigenes (25) encode potential patternmore » recognition receptors (lectins, scavenger receptors, and others), as well as genes that may function in signaling pathways involved in innate immune responses (toll-like signaling, NFkB p105, and MAP kinases). Comparison between the A. palmata and an A. millepora EST dataset identified ferritin as a highly expressed gene in both datasets that appears to be undergoing adaptive evolution. Five unigenes appear to be restricted to the Scleractinia, as they had no homology to any sequences in the nr databases nor to the non-scleractinian cnidarians Nematostella vectensis and Hydra magnipapillata. In conclusion, partial sequencing of 5 cDNA libraries each for A. palmata and M. faveolata has produced a rich set of candidate genes (4,980 genes from A. palmata, and 1,732 genes from M. faveolata) that we can use as a starting point for examining the life history and symbiosis of these two species, as well as to further expand the dataset of cnidarian genes for comparative genomics and evolutionary studies.« less

Authors:
 [1];  [2];  [3];  [2];  [4];  [5];  [6];  [3]
  1. Vassar College, Poughkeepsie, NY (United States). Biology Dept.
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Univ. of California, Merced, CA (United States). School of Natural Sciences
  4. James Cook Univ., Townsville, QLD (Australia). Comparative Genomics Center
  5. Center for Marine Science, Wilmington, NC (United States)
  6. State Univ. of New York (SUNY), Buffalo, NY (United States). Dept. of Geological Sciences
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1407061
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 58 GEOSCIENCES

Citation Formats

Schwarz, Jodi A., Brokstein, Peter B., Voolstra, Christian R., Terry, Astrid Y., Miller, David J., Szmant, Alina M., Coffroth, Mary Alice, and Medina, Monica. Coral Life History and Symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. United States: N. p., 2008. Web. doi:10.1186/1471-2164-9-97.
Schwarz, Jodi A., Brokstein, Peter B., Voolstra, Christian R., Terry, Astrid Y., Miller, David J., Szmant, Alina M., Coffroth, Mary Alice, & Medina, Monica. Coral Life History and Symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. United States. https://doi.org/10.1186/1471-2164-9-97
Schwarz, Jodi A., Brokstein, Peter B., Voolstra, Christian R., Terry, Astrid Y., Miller, David J., Szmant, Alina M., Coffroth, Mary Alice, and Medina, Monica. Mon . "Coral Life History and Symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata". United States. https://doi.org/10.1186/1471-2164-9-97. https://www.osti.gov/servlets/purl/1407061.
@article{osti_1407061,
title = {Coral Life History and Symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata},
author = {Schwarz, Jodi A. and Brokstein, Peter B. and Voolstra, Christian R. and Terry, Astrid Y. and Miller, David J. and Szmant, Alina M. and Coffroth, Mary Alice and Medina, Monica},
abstractNote = {Scleractinian corals are the foundation of reef ecosystems in tropical marine environments. Their great success is due to interactions with endosymbiotic dinoflagellates (Symbiodinium spp.), with which they are obligately symbiotic. To develop a foundation for studying coral biology and coral symbiosis, we have constructed a set of cDNA libraries and generated and annotated ESTs from two species of corals, Acropora palmata and Montastraea faveolata. Here we generated 14,588 (Ap) and 3,854 (Mf) high quality ESTs from five life history/symbiosis stages (spawned eggs, early-stage planula larvae, late-stage planula larvae either infected with symbionts or uninfected, and adult coral). The ESTs assembled into a set of primarily stage-specific clusters, producing 4,980 (Ap), and 1,732 (Mf) unigenes. The egg stage library, relative to the other developmental stages, was enriched in genes functioning in cell division and proliferation, transcription, signal transduction, and regulation of protein function. Fifteen unigenes were identified as candidate symbiosis-related genes as they were expressed in all libraries constructed from the symbiotic stages and were absent from all of the non symbiotic stages. These include several DNA interacting proteins, and one highly expressed unigene (containing 17 cDNAs) with no significant protein-coding region. A significant number of unigenes (25) encode potential pattern recognition receptors (lectins, scavenger receptors, and others), as well as genes that may function in signaling pathways involved in innate immune responses (toll-like signaling, NFkB p105, and MAP kinases). Comparison between the A. palmata and an A. millepora EST dataset identified ferritin as a highly expressed gene in both datasets that appears to be undergoing adaptive evolution. Five unigenes appear to be restricted to the Scleractinia, as they had no homology to any sequences in the nr databases nor to the non-scleractinian cnidarians Nematostella vectensis and Hydra magnipapillata. In conclusion, partial sequencing of 5 cDNA libraries each for A. palmata and M. faveolata has produced a rich set of candidate genes (4,980 genes from A. palmata, and 1,732 genes from M. faveolata) that we can use as a starting point for examining the life history and symbiosis of these two species, as well as to further expand the dataset of cnidarian genes for comparative genomics and evolutionary studies.},
doi = {10.1186/1471-2164-9-97},
journal = {BMC Genomics},
number = 1,
volume = 9,
place = {United States},
year = {Mon Feb 25 00:00:00 EST 2008},
month = {Mon Feb 25 00:00:00 EST 2008}
}

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Multiple Hypothesis Testing to Detect Lineages under Positive Selection that Affects Only a Few Sites
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journal, August 2001


Accuracy and Power of Bayes Prediction of Amino Acid Sites Under Positive Selection
journal, June 2002


Models of amino acid substitution and applications to mitochondrial protein evolution
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Selectivity in phagocytosis and persistence of symbiotic algae by the scyphistoma stage of the jellyfishCassiopeia xamachana
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Diverse staghorn corals ( Acropora ) in high-latitude Eocene assemblages: implications for the evolution of modern diversity patterns of reef corals
journal, January 2006

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Measuring coral reef decline through meta-analyses
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  • Côté, I. M.; Gill, J. A.; Gardner, T. A.
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Base-Calling of Automated Sequencer Traces Using Phred.  I. Accuracy Assessment
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Base-Calling of Automated Sequencer Traces Using Phred. II. Error Probabilities
journal, March 1998


CAP3: A DNA Sequence Assembly Program
journal, September 1999


Invertebrate immune systems - not homogeneous, not simple, not well understood
journal, April 2004


Purification and cDNA Cloning of Ferritin from the Hepatopancreas of the Freshwater Crayfish Pacifastacus leniusculus
journal, March 1996


Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization
journal, July 2007


Sponge Paleogenomics Reveals an Ancient Role for Carbonic Anhydrase in Skeletogenesis
journal, June 2007


Ferritin: Structure, Gene Regulation, and Cellular Function in Animals, Plants, and Microorganisms
journal, June 1987


Marine Genomics: A clearing-house for genomic and transcriptomic data of marine organisms
journal, March 2005


Transcriptome analysis of a cnidarian – dinoflagellate mutualism reveals complex modulation of host gene expression
journal, February 2006

  • Rodriguez-Lanetty, Mauricio; Phillips, Wendy S.; Weis, Virginia M.
  • BMC Genomics, Vol. 7, Issue 1
  • DOI: 10.1186/1471-2164-7-23

Late Larval Development and Onset of Symbiosis in the Scleractinian Coral Fungia scutaria
journal, February 1999

  • Schwarz, J. A.; Krupp, D. A.; Weis, V. M.
  • The Biological Bulletin, Vol. 196, Issue 1
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Early ontogenetic expression of specificity in a cnidarian-algal symbiosis
journal, January 2001

  • Coffroth, Ma; Santos, Sr; Goulet, Tl
  • Marine Ecology Progress Series, Vol. 222
  • DOI: 10.3354/meps222085

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  • DOI: 10.1002/ece3.5576

Holobiont chronobiology: mycorrhiza may be a key to linking aboveground and underground rhythms
journal, June 2019


Coral Thermal Tolerance: Tuning Gene Expression to Resist Thermal Stress
journal, November 2012


Signatures of adaptation and symbiosis in genomes and transcriptomes of Symbiodinium
journal, November 2017


Metabolic co-dependence drives the evolutionarily ancient Hydra–Chlorella symbiosis
journal, May 2018


The past, present, and future of coral heat stress studies
journal, August 2019

  • Cziesielski, Maha J.; Schmidt‐Roach, Sebastian; Aranda, Manuel
  • Ecology and Evolution, Vol. 9, Issue 17
  • DOI: 10.1002/ece3.5576

Signatures of adaptation and symbiosis in genomes and transcriptomes of Symbiodinium
journal, November 2017


Core genes in diverse dinoflagellate lineages include a wealth of conserved dark genes with unknown functions
journal, November 2018

  • Stephens, Timothy G.; Ragan, Mark A.; Bhattacharya, Debashish
  • Scientific Reports, Vol. 8, Issue 1
  • DOI: 10.1038/s41598-018-35620-z

High amino acid diversity and positive selection at a putative coral immunity gene (tachylectin-2)
journal, May 2010

  • Hayes, Marshall L.; Eytan, Ron I.; Hellberg, Michael E.
  • BMC Evolutionary Biology, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2148-10-150

Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx
journal, January 2009


Comprehensive EST analysis of the symbiotic sea anemone, Anemonia viridis
journal, January 2009


Effects of temperature on gene expression in embryos of the coral Montastraea faveolata
journal, December 2009

  • Voolstra, Christian R.; Schnetzer, Julia; Peshkin, Leonid
  • BMC Genomics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2164-10-627

Conjugating effects of symbionts and environmental factors on gene expression in deep-sea hydrothermal vent mussels
journal, October 2011


Production of a reference transcriptome and transcriptomic database (PocilloporaBase) for the cauliflower coral, Pocillopora damicornis
journal, November 2011

  • Traylor-Knowles, Nikki; Granger, Brian R.; Lubinski, Tristan J.
  • BMC Genomics, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2164-12-585

High natural gene expression variation in the reef-building coral Acropora millepora: potential for acclimative and adaptive plasticity
journal, April 2013

  • Granados-Cifuentes, Camila; Bellantuono, Anthony J.; Ridgway, Tyrone
  • BMC Genomics, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2164-14-228

Erratum to: Coral life history and symbiosis: Functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata
journal, September 2008

  • Schwarz, Jodi A.; Brokstein, Peter B.; Voolstra, Christian
  • BMC Genomics, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2164-9-435

Gene Discovery in the Threatened Elkhorn Coral: 454 Sequencing of the Acropora palmata Transcriptome
journal, December 2011


Major Cellular and Physiological Impacts of Ocean Acidification on a Reef Building Coral
journal, April 2012


Coral Thermal Tolerance: Tuning Gene Expression to Resist Thermal Stress
journal, November 2012


Tracking Transmission of Apicomplexan Symbionts in Diverse Caribbean Corals
journal, November 2013


Transcriptome Analysis of the Scleractinian Coral Stylophora pistillata
journal, February 2014


Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease
journal, September 2015

  • Daniels, Camille A.; Baumgarten, Sebastian; Yum, Lauren K.
  • Frontiers in Marine Science, Vol. 2
  • DOI: 10.3389/fmars.2015.00062

A genomic approach to coral-dinoflagellate symbiosis: studies of Acropora digitifera and Symbiodinium minutum
journal, July 2014