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Title: Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont

Abstract

Background: The most diverse marine ecosystems, coral reefs, depend upon a functional symbiosis between cnidarian hosts and unicellular dinoflagellate algae. The molecular mechanisms underlying the establishment, maintenance, and breakdown of the symbiotic partnership are, however, not well understood. Efforts to dissect these questions have been slow, as corals are notoriously difficult to work with. In order to expedite this field of research, we generated and analyzed a collection of expressed sequence tags (ESTs) from the sea anemone Aiptasia pallida and its dinoflagellate symbiont (Symbiodinium sp.), a system that is gaining popularity as a model to study cellular, molecular, and genomic questions related to cnidarian-dinoflagellate symbioses. Results: A set of 4,925 unique sequences (UniSeqs) comprising 1,427 clusters of 2 or more ESTs (contigs) and 3,498 unclustered ESTs (singletons) was generated by analyzing 10,285 high-quality ESTs from a mixed host/symbiont cDNA library. Using a BLAST-based approach to predict which unique sequences derived from the host versus symbiont genomes, we found that the contribution of the symbiont genome to the transcriptome was surprisingly small (1.6–6.4%). This may reflect low levels of gene expression in the symbionts, low coverage of alveolate genes in the sequence databases, a small number of symbiont cells relative tomore » the total cellular content of the anemones, or failure to adequately lyse symbiont cells. Furthermore, we were able to identify groups of genes that are known or likely to play a role in cnidarian-dinoflagellate symbioses, including oxidative stress pathways that emerged as a prominent biological feature of this transcriptome. All ESTs and UniSeqs along with annotation results and other tools have been made accessible through the implementation of a publicly accessible database named Aiptasia Base. Conclusion: We have established the first large-scale transcriptomic resource for Aiptasia pallida and its dinoflagellate symbiont. These data provide researchers with tools to study questions related to cnidarian-dinoflagellate symbioses on a molecular, cellular, and genomic level. This groundwork represents a crucial step towards the establishment of a tractable model system that can be utilized to better understand cnidarian-dinoflagellate symbioses. With the advent of next generation sequencing methods, the transcriptomic inventory of A. pallida and its symbiont, and thus the extent of Aiptasia Base, should expand dramatically in the near future.« less

Authors:
 [1];  [1];  [2];  [3];  [4];  [4];  [5];  [1];  [2]
+ Show Author Affiliations
  1. Univ. of California, Merced, CA (United States). School of Natural Sciences
  2. Vassar College, Poughkeepsie, NY (United States). Biology Dept.
  3. Vassar College, Poughkeepsie, NY (United States). Computer Science Dept.
  4. Stanford Univ., CA (United States). Dept. of Genetics
  5. Oregon State Univ., Corvallis, OR (United States). Dept. of Zoology
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1626399
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biotechnology & Applied Microbiology; Genetics & Heredity

Citation Formats

Sunagawa, Shinichi, Wilson, Emily C., Thaler, Michael, Smith, Marc L., Caruso, Carlo, Pringle, John R., Weis, Virginia M., Medina, Mónica, and Schwarz, Jodi A. Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. United States: N. p., 2009. Web. doi:10.1186/1471-2164-10-258.
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Sunagawa, Shinichi, Wilson, Emily C., Thaler, Michael, Smith, Marc L., Caruso, Carlo, Pringle, John R., Weis, Virginia M., Medina, Mónica, & Schwarz, Jodi A. Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. United States. https://doi.org/10.1186/1471-2164-10-258
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Sunagawa, Shinichi, Wilson, Emily C., Thaler, Michael, Smith, Marc L., Caruso, Carlo, Pringle, John R., Weis, Virginia M., Medina, Mónica, and Schwarz, Jodi A. Fri . "Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont". United States. https://doi.org/10.1186/1471-2164-10-258. https://www.osti.gov/servlets/purl/1626399.
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@article{osti_1626399,
title = {Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont},
author = {Sunagawa, Shinichi and Wilson, Emily C. and Thaler, Michael and Smith, Marc L. and Caruso, Carlo and Pringle, John R. and Weis, Virginia M. and Medina, Mónica and Schwarz, Jodi A.},
abstractNote = {Background: The most diverse marine ecosystems, coral reefs, depend upon a functional symbiosis between cnidarian hosts and unicellular dinoflagellate algae. The molecular mechanisms underlying the establishment, maintenance, and breakdown of the symbiotic partnership are, however, not well understood. Efforts to dissect these questions have been slow, as corals are notoriously difficult to work with. In order to expedite this field of research, we generated and analyzed a collection of expressed sequence tags (ESTs) from the sea anemone Aiptasia pallida and its dinoflagellate symbiont (Symbiodinium sp.), a system that is gaining popularity as a model to study cellular, molecular, and genomic questions related to cnidarian-dinoflagellate symbioses. Results: A set of 4,925 unique sequences (UniSeqs) comprising 1,427 clusters of 2 or more ESTs (contigs) and 3,498 unclustered ESTs (singletons) was generated by analyzing 10,285 high-quality ESTs from a mixed host/symbiont cDNA library. Using a BLAST-based approach to predict which unique sequences derived from the host versus symbiont genomes, we found that the contribution of the symbiont genome to the transcriptome was surprisingly small (1.6–6.4%). This may reflect low levels of gene expression in the symbionts, low coverage of alveolate genes in the sequence databases, a small number of symbiont cells relative to the total cellular content of the anemones, or failure to adequately lyse symbiont cells. Furthermore, we were able to identify groups of genes that are known or likely to play a role in cnidarian-dinoflagellate symbioses, including oxidative stress pathways that emerged as a prominent biological feature of this transcriptome. All ESTs and UniSeqs along with annotation results and other tools have been made accessible through the implementation of a publicly accessible database named Aiptasia Base. Conclusion: We have established the first large-scale transcriptomic resource for Aiptasia pallida and its dinoflagellate symbiont. These data provide researchers with tools to study questions related to cnidarian-dinoflagellate symbioses on a molecular, cellular, and genomic level. This groundwork represents a crucial step towards the establishment of a tractable model system that can be utilized to better understand cnidarian-dinoflagellate symbioses. With the advent of next generation sequencing methods, the transcriptomic inventory of A. pallida and its symbiont, and thus the extent of Aiptasia Base, should expand dramatically in the near future.},
doi = {10.1186/1471-2164-10-258},
journal = {BMC Genomics},
number = 1,
volume = 10,
place = {United States},
year = {Fri Jun 05 00:00:00 EDT 2009},
month = {Fri Jun 05 00:00:00 EDT 2009}
}
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ApRab11, a cnidarian homologue of the recycling regulatory protein Rab11, is involved in the establishment and maintenance of the Aiptasia–Symbiodinium endosymbiosis
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Response of the symbiotic cnidarian Anthopleura elegantissima transcriptome to temperature and UV increase
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Hyperthermic stress-induced increase in the expression of glutamate-cysteine ligase and glutathione levels in the symbiotic sea anemone Aiptasia pallida
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A novel Aurelia aurita protein mesoglein contains DSL and ZP domains
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Reef corals bleach to survive change
journal, June 2001

Thermal adaptation in reef coral symbionts
journal, August 2004

Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae
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Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching
journal, July 1999

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journal, June 2006

  • Berkelmans, Ray; van Oppen, Madeleine J. H.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 273, Issue 1599
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Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis
journal, December 2006

Analysis of an EST library from the dinoflagellate ( Symbiodinium sp.) symbiont of reef-building corals 1
journal, October 2007

Flexibility in Algal Endosymbioses Shapes Growth in Reef Corals
journal, June 2004

Flexibility and Specificity in Coral-Algal Symbiosis: Diversity, Ecology, and Biogeography of Symbiodinium
journal, November 2003

EST2uni: an open, parallel tool for automated EST analysis and database creation, with a data mining web interface and microarray expression data integration
journal, January 2008

  • Forment, Javier; Gilabert, Francisco; Robles, Antonio
  • BMC Bioinformatics, Vol. 9, Issue 1
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Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx
journal, January 2009

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

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

  • Schwarz, Jodi A.; Brokstein, Peter B.; Voolstra, Christian
  • BMC Genomics, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2164-9-97

Cellular mechanisms underlying temperature-induced bleaching in the tropical sea anemone Aiptasia pulchella
journal, October 2001

  • Sawyer, Sara J.; Muscatine, Leonard
  • Journal of Experimental Biology, Vol. 204, Issue 20
  • DOI: 10.1242/jeb.204.20.3443

Coral Bleaching as an Adaptive Mechanism
journal, May 1993

  • Buddemeier, Robert W.; Fautin, Daphne G.
  • BioScience, Vol. 43, Issue 5
  • DOI: 10.2307/1312064

Temperature Stress Causes Host Cell Detachment in Symbiotic Cnidarians: Implications for Coral Bleaching
journal, June 1992

  • Gates, R. D.; Baghdasarian, G.; Muscatine, L.
  • The Biological Bulletin, Vol. 182, Issue 3
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Specificity of a Model Cnidarian-Dinoflagellate Symbiosis
journal, February 2002

  • Belda-Baillie, Carmen A.; Baillie, Brett K.; Maruyama, Tadashi
  • The Biological Bulletin, Vol. 202, Issue 1
  • DOI: 10.2307/1543224

Knockdown of Actin and Caspase Gene Expression by RNA Interference in the Symbiotic Anemone Aiptasia pallida
journal, June 2007

  • Dunn, Simon R.; Phillips, Wendy S.; Green, Douglas R.
  • The Biological Bulletin, Vol. 212, Issue 3
  • DOI: 10.2307/25066607

Fidelity and flexibility in coral symbioses
journal, October 2007

  • Baird, Ah; Cumbo, Vr; Leggat, W.
  • Marine Ecology Progress Series, Vol. 347
  • DOI: 10.3354/meps07220

Symbiophagy as a cellular mechanism for coral bleaching
journal, February 2009

  • Downs, Craig A.; Kramarsky-Winter, Esti; Martinez, Jon
  • Autophagy, Vol. 5, Issue 2
  • DOI: 10.4161/auto.5.2.7405
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    journal, October 2011

    The effects of symbiotic state and nutrient availability on the cnidom in the model sea anemone, Exaiptasia diaphana
    journal, January 2019

    Dynamics of herbicide transport and partitioning under event flow conditions in the lower Burdekin region, Australia
    journal, January 2012

    Extensive Differences in Gene Expression Between Symbiotic and Aposymbiotic Cnidarians
    journal, February 2014

    • Lehnert, Erik M.; Mouchka, Morgan E.; Burriesci, Matthew S.
    • G3 Genes|Genomes|Genetics, Vol. 4, Issue 2
    • DOI: 10.1534/g3.113.009084

    Gene Expression Variation Resolves Species and Individual Strains among Coral-Associated Dinoflagellates within the Genus Symbiodinium
    journal, February 2016

    • Parkinson, John E.; Baumgarten, Sebastian; Michell, Craig T.
    • Genome Biology and Evolution, Vol. 8, Issue 3
    • DOI: 10.1093/gbe/evw019

    DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia
    journal, August 2018

    Evidence for miRNA-mediated modulation of the host transcriptome in cnidarian-dinoflagellate symbiosis
    journal, December 2017

    • Baumgarten, Sebastian; Cziesielski, Maha J.; Thomas, Ludivine
    • Molecular Ecology, Vol. 27, Issue 2
    • DOI: 10.1111/mec.14452

    Menthol-induced bleaching rapidly and effectively provides experimental aposymbiotic sea anemones ( Aiptasia sp.) for symbiosis investigations
    journal, November 2015

    • Matthews, Jennifer L.; Sproles, Ashley E.; Oakley, Clinton A.
    • The Journal of Experimental Biology, Vol. 219, Issue 3
    • DOI: 10.1242/jeb.128934

    Symbiodinium Transcriptomes: Genome Insights into the Dinoflagellate Symbionts of Reef-Building Corals
    journal, April 2012

    Isolation of clonal axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity 1
    journal, April 2013

    • Xiang, Tingting; Hambleton, Elizabeth A.; DeNofrio, Jan C.
    • Journal of Phycology, Vol. 49, Issue 3
    • DOI: 10.1111/jpy.12055

    N-Linked Surface Glycan Biosynthesis, Composition, Inhibition, and Function in Cnidarian-Dinoflagellate Symbiosis
    journal, January 2020

    • Tivey, Trevor R.; Parkinson, John Everett; Mandelare, Paige E.
    • Microbial Ecology, Vol. 80, Issue 1
    • DOI: 10.1007/s00248-020-01487-9

    Long-Term Temperature Stress in the Coral Model Aiptasia Supports the “Anna Karenina Principle” for Bacterial Microbiomes
    journal, May 2019

    Transcriptional Activation of c3 and hsp70 as Part of the Immune Response of Acropora millepora to Bacterial Challenges
    journal, July 2013

    Transcriptome Characterization of Reverse Development in Turritopsis dohrnii (Hydrozoa, Cnidaria)
    journal, December 2019

    • Matsumoto, Yui; Piraino, Stefano; Miglietta, Maria Pia
    • G3 Genes|Genomes|Genetics, Vol. 9, Issue 12
    • DOI: 10.1534/g3.119.400487

    Rapid Evolution of Coral Proteins Responsible for Interaction with the Environment
    journal, May 2011

    Microbiota characterization of Exaiptasia diaphana from the Great Barrier Reef
    journal, April 2020

    • Hartman, Leon Michael; van Oppen, Madeleine Josephine Henriette; Blackall, Linda Louise
    • Animal Microbiome, Vol. 2, Issue 1
    • DOI: 10.1186/s42523-020-00029-5

    Gonadal transcriptomics elucidate patterns of adaptive evolution within marine rockfishes (Sebastes)
    journal, September 2015

    Live imaging of Aiptasia larvae, a model system for studying coral bleaching, using a simple microfluidic device
    posted_content, January 2018

    • Treuren, Will Van; Brower, Kara K.; Labanieh, Louai
    • Scientific Reports
    • DOI: 10.1101/370478

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

    Genome-wide polymorphism and signatures of selection in the symbiotic sea anemone Aiptasia
    journal, February 2016

    Exaiptasia diaphana from the great barrier reef: a valuable resource for coral symbiosis research
    journal, February 2020

    Rapid, Precise, and Accurate Counts of Symbiodinium Cells Using the Guava Flow Cytometer, and a Comparison to Other Methods
    journal, August 2015

    Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts
    journal, April 2018

    • Cziesielski, Maha J.; Liew, Yi Jin; Cui, Guoxin
    • Proceedings of the Royal Society B: Biological Sciences, Vol. 285, Issue 1877
    • DOI: 10.1098/rspb.2017.2654

    Are Niemann-Pick type C proteins key players in cnidarian-dinoflagellate endosymbioses?
    journal, September 2014

    • Dani, Vincent; Ganot, Philippe; Priouzeau, Fabrice
    • Molecular Ecology, Vol. 23, Issue 18
    • DOI: 10.1111/mec.12876

    Diurnal and nocturnal transcriptomic variation in the Caribbean staghorn coral, Acropora cervicornis
    journal, August 2015

    • Hemond, Elizabeth M.; Vollmer, Steven V.
    • Molecular Ecology, Vol. 24, Issue 17
    • DOI: 10.1111/mec.13320

    A metabarcoding framework for facilitated survey of endolithic phototrophs with tufA
    journal, March 2016

    Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations
    journal, January 2020

    Photo-movement in the sea anemone Aiptasia influenced by light quality and symbiotic association
    journal, November 2019

    Live imaging of Aiptasia larvae, a model system for coral and anemone bleaching, using a simple microfluidic device
    journal, June 2019

    Is the coral-algae symbiosis really ‘mutually beneficial’ for the partners?
    journal, May 2010

    Differential protein abundance during the first month of regeneration of the Caribbean star coral Montastraea cavernosa
    journal, November 2018

    Distribution of MACPF/CDC Proteins
    book, January 2014

    • Anderluh, Gregor; Kisovec, Matic; Kraševec, Nada
    • MACPF/CDC Proteins - Agents of Defence, Attack and Invasion
    • DOI: 10.1007/978-94-017-8881-6_2

    Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations
    journal, January 2020

    Microinjection to deliver protein, mRNA, and DNA into zygotes of the cnidarian endosymbiosis model Aiptasia sp.
    journal, November 2018

    • Jones, Victor A. S.; Bucher, Madeline; Hambleton, Elizabeth A.
    • Scientific Reports, Vol. 8, Issue 1
    • DOI: 10.1038/s41598-018-34773-1

    Live imaging of Aiptasia larvae, a model system for coral and anemone bleaching, using a simple microfluidic device
    journal, June 2019

    Gene Expression Variation Resolves Species and Individual Strains among Coral-Associated Dinoflagellates within the Genus Symbiodinium
    journal, February 2016

    • Parkinson, John E.; Baumgarten, Sebastian; Michell, Craig T.
    • Genome Biology and Evolution, Vol. 8, Issue 3
    • DOI: 10.1093/gbe/evw019

    Live imaging of Aiptasia larvae, a model system for studying coral bleaching, using a simple microfluidic device
    posted_content, January 2018

    • Treuren, Will Van; Brower, Kara K.; Labanieh, Louai
    • Scientific Reports
    • DOI: 10.1101/370478

    Exaiptasia diaphana from the Great Barrier Reef: a valuable resource for coral symbiosis research
    posted_content, January 2019

    • Dungan, Ashley M.; Hartman, Leon; Tortorelli, Giada
    • Symbiosis
    • DOI: 10.1101/775510

    N-linked surface glycan biosynthesis, composition, inhibition, and function in cnidarian-dinoflagellate symbiosis
    posted_content, January 2019

    • Tivey, Trevor R.; Parkinson, John Everett; Mandelare, Paige E.
    • Microbial Ecology
    • DOI: 10.1101/820894

    DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia
    journal, August 2018

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

    Early transcriptional changes in the reef-building coral Acropora aspera in response to thermal and nutrient stress
    journal, January 2014

    Production of a reference transcriptome and transcriptomic database (EdwardsiellaBase) for the lined sea anemone, Edwardsiella lineata, a parasitic cnidarian
    journal, January 2014

    • Stefanik, Derek J.; Lubinski, Tristan J.; Granger, Brian R.
    • BMC Genomics, Vol. 15, Issue 1
    • DOI: 10.1186/1471-2164-15-71

    Genome-wide polymorphism and signatures of selection in the symbiotic sea anemone Aiptasia
    journal, February 2016

    A comparative genomics study of neuropeptide genes in the cnidarian subclasses Hexacorallia and Ceriantharia
    journal, September 2020

    A metabarcoding framework for facilitated survey of endolithic phototrophs with tufA
    journal, March 2016

    Rapid Evolution of Coral Proteins Responsible for Interaction with the Environment
    journal, May 2011

    Expression of Putative Immune Response Genes during Early Ontogeny in the Coral Acropora millepora
    journal, July 2012

    Comparative Lipid Profiling of the Cnidarian Aiptasia pallida and Its Dinoflagellate Symbiont
    journal, March 2013

    Rapid, Precise, and Accurate Counts of Symbiodinium Cells Using the Guava Flow Cytometer, and a Comparison to Other Methods
    journal, August 2015

    Relative Contributions of Various Cellular Mechanisms to Loss of Algae during Cnidarian Bleaching
    journal, April 2016

    Extensive Differences in Gene Expression Between Symbiotic and Aposymbiotic Cnidarians
    journal, February 2014

    • Lehnert, Erik M.; Mouchka, Morgan E.; Burriesci, Matthew S.
    • G3 Genes|Genomes|Genetics, Vol. 4, Issue 2
    • DOI: 10.1534/g3.113.009084

    Global Shifts in Gene Expression Profiles Accompanied with Environmental Changes in Cnidarian-Dinoflagellate Endosymbiosis
    journal, July 2019

    • Ishii, Yuu; Maruyama, Shinichiro; Takahashi, Hiroki
    • G3 Genes|Genomes|Genetics, Vol. 9, Issue 7
    • DOI: 10.1534/g3.118.201012

    Untargeted metabolomic data collected during a thermal stress experiment using reef building corals collected in Kāne'ohe Bay, O'ahu, Hawai'i.
    dataset, January 2023

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

    Proteomic Basis of Symbiosis: A Heterologous Partner Fails to Duplicate Homologous Colonization in a Novel Cnidarian– Symbiodiniaceae Mutualism
    journal, May 2019

    • Medrano, Emmanuel; Merselis, Daniel G.; Bellantuono, Anthony J.
    • Frontiers in Microbiology, Vol. 10
    • DOI: 10.3389/fmicb.2019.01153

    Partitioning of Respiration in an Animal-Algal Symbiosis: Implications for Different Aerobic Capacity between Symbiodinium spp.
    journal, April 2016

    • Hawkins, Thomas D.; Hagemeyer, Julia C. G.; Hoadley, Kenneth D.
    • Frontiers in Physiology, Vol. 7
    • DOI: 10.3389/fphys.2016.00128

    Impact of El Niño-Southern Oscillation 2015-2016 on the soluble proteomic profile and cytolytic activity of Millepora alcicornis (“fire coral”) from the Mexican Caribbean
    journal, March 2019

    • Olguín-López, Norma; Hérnandez-Elizárraga, Víctor Hugo; Hernández-Matehuala, Rosalina
    • PeerJ, Vol. 7
    • DOI: 10.7717/peerj.6593
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