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

Sunagawa, Shinichi; Wilson, Emily C.; Thaler, Michael; Smith, Marc L.; Caruso, Carlo; Pringle, John R.; Weis, Virginia M.; Medina, Mónica; Schwarz, Jodi A.

doi:10.1186/1471-2164-10-258

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

Journal Article · Fri Jun 05 00:00:00 EDT 2009 · BMC Genomics

DOI:https://doi.org/10.1186/1471-2164-10-258· OSTI ID:1626399

Sunagawa, Shinichi ^[1]; Wilson, Emily C. ^[2]; Thaler, Michael ^[3]; Smith, Marc L. ^[4]; Caruso, Carlo ^[5]; Pringle, John R. ^[5]; Weis, Virginia M. ^[6]; Medina, Mónica ^[2]; Schwarz, Jodi A. ^[3]

Univ. of California, Merced, CA (United States). School of Natural Sciences; DOE/OSTI
Univ. of California, Merced, CA (United States). School of Natural Sciences
Vassar College, Poughkeepsie, NY (United States). Biology Dept.
Vassar College, Poughkeepsie, NY (United States). Computer Science Dept.
Stanford Univ., CA (United States). Dept. of Genetics
Oregon State Univ., Corvallis, OR (United States). Dept. of Zoology

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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1626399

Journal Information:: BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 10; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Additional file 12 of Gene expression kinetics of Exaiptasia pallida innate immune response to Vibrio parahaemolyticus infection Seneca, François; Davtian, David; Boyer, Laurent figshare https://doi.org/10.6084/m9.figshare.13212380.v1	dataset	January 2020
Additional file 13 of Gene expression kinetics of Exaiptasia pallida innate immune response to Vibrio parahaemolyticus infection Seneca, François; Davtian, David; Boyer, Laurent figshare https://doi.org/10.6084/m9.figshare.13212383.v1	dataset	January 2020
Additional file 1 of Gene expression kinetics of Exaiptasia pallida innate immune response to Vibrio parahaemolyticus infection Seneca, François; Davtian, David; Boyer, Laurent figshare https://doi.org/10.6084/m9.figshare.13212386.v1	image	January 2020
Additional file 4 of Gene expression kinetics of Exaiptasia pallida innate immune response to Vibrio parahaemolyticus infection Seneca, François; Davtian, David; Boyer, Laurent figshare https://doi.org/10.6084/m9.figshare.13212395	dataset	January 2020
Additional file 6 of Gene expression kinetics of Exaiptasia pallida innate immune response to Vibrio parahaemolyticus infection Seneca, François; Davtian, David; Boyer, Laurent figshare https://doi.org/10.6084/m9.figshare.13212401	dataset	January 2020
Additional file 7 of Gene expression kinetics of Exaiptasia pallida innate immune response to Vibrio parahaemolyticus infection Seneca, François; Davtian, David; Boyer, Laurent figshare https://doi.org/10.6084/m9.figshare.13212404	dataset	January 2020
Additional file 8 of Gene expression kinetics of Exaiptasia pallida innate immune response to Vibrio parahaemolyticus infection Seneca, François; Davtian, David; Boyer, Laurent figshare https://doi.org/10.6084/m9.figshare.13212407	dataset	January 2020
Additional file 9 of Gene expression kinetics of Exaiptasia pallida innate immune response to Vibrio parahaemolyticus infection Seneca, François; Davtian, David; Boyer, Laurent figshare https://doi.org/10.6084/m9.figshare.13212410	dataset	January 2020
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 Olguín-López, Norma; Hérnandez-Elizárraga, Víctor Hugo; Hernández-Matehuala, Rosalina PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6593	journal	March 2019
Is the coral-algae symbiosis really ‘mutually beneficial’ for the partners? Wooldridge, Scott A. BioEssays, Vol. 32, Issue 7 https://doi.org/10.1002/bies.200900182	journal	May 2010
Differential gene expression analysis of symbiotic and aposymbiotic Exaiptasia anemones under immune challenge with Vibrio coralliilyticus Roesel, Charles L.; Vollmer, Steven V. Ecology and Evolution, Vol. 9, Issue 14 https://doi.org/10.1002/ece3.5403	journal	June 2019
Differential carbon utilization and asexual reproduction under elevated p CO ₂ conditions in the model anemone, E xaiptasia pallida , hosting different symbionts: Ocean acidification enhances sea anemone fitness Hoadley, Kenneth D.; Rollison, Dana; Pettay, D. Tye Limnology and Oceanography, Vol. 60, Issue 6 https://doi.org/10.1002/lno.10160	journal	September 2015
Distribution of MACPF/CDC Proteins Anderluh, Gregor; Kisovec, Matic; Kraševec, Nada MACPF/CDC Proteins - Agents of Defence, Attack and Invasion https://doi.org/10.1007/978-94-017-8881-6_2	book	January 2014
The effects of symbiotic state and nutrient availability on the cnidom in the model sea anemone, Exaiptasia diaphana Gundlach, Katrina A.; Watson, Glen M. Marine Biology, Vol. 166, Issue 3 https://doi.org/10.1007/s00227-019-3477-5	journal	January 2019
N-Linked Surface Glycan Biosynthesis, Composition, Inhibition, and Function in Cnidarian-Dinoflagellate Symbiosis Tivey, Trevor R.; Parkinson, John Everett; Mandelare, Paige E. Microbial Ecology, Vol. 80, Issue 1 https://doi.org/10.1007/s00248-020-01487-9	journal	January 2020
Transcriptomic responses to darkness stress point to common coral bleaching mechanisms DeSalvo, M. K.; Estrada, A.; Sunagawa, S. Coral Reefs, Vol. 31, Issue 1 https://doi.org/10.1007/s00338-011-0833-4	journal	October 2011
Differential protein abundance during the first month of regeneration of the Caribbean star coral Montastraea cavernosa Horricks, Ryan A.; Herbinger, Christophe M.; Lillie, Brandon N. Coral Reefs, Vol. 38, Issue 1 https://doi.org/10.1007/s00338-018-01754-9	journal	November 2018
Photo-movement in the sea anemone Aiptasia influenced by light quality and symbiotic association Foo, Shawna A.; Liddell, Lauren; Grossman, Arthur Coral Reefs, Vol. 39, Issue 1 https://doi.org/10.1007/s00338-019-01866-w	journal	November 2019
Exaiptasia diaphana from the great barrier reef: a valuable resource for coral symbiosis research Dungan, Ashley M.; Hartman, Leon M.; Tortorelli, Giada Symbiosis, Vol. 80, Issue 2 https://doi.org/10.1007/s13199-020-00665-0	journal	February 2020
Dynamics of herbicide transport and partitioning under event flow conditions in the lower Burdekin region, Australia Davis, Aaron M.; Lewis, Stephen E.; Bainbridge, Zoë T. Marine Pollution Bulletin, Vol. 65, Issue 4-9 https://doi.org/10.1016/j.marpolbul.2011.08.025	journal	January 2012
Induction of Gametogenesis in the Cnidarian Endosymbiosis Model Aiptasia sp. Grawunder, Désirée; Hambleton, Elizabeth A.; Bucher, Madeline Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep15677	journal	October 2015
Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases Krediet, Cory J.; Ritchie, Kim B.; Paul, Valerie J. Proceedings of the Royal Society B: Biological Sciences, Vol. 280, Issue 1755 https://doi.org/10.1098/rspb.2012.2328	journal	March 2013
Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts Cziesielski, Maha J.; Liew, Yi Jin; Cui, Guoxin Proceedings of the Royal Society B: Biological Sciences, Vol. 285, Issue 1877 https://doi.org/10.1098/rspb.2017.2654	journal	April 2018
Symbiosis induces widespread changes in the proteome of the model cnidarian Aiptasia: Symbiosis and the Aiptasia proteome Oakley, Clinton A.; Ameismeier, Michael F.; Peng, Lifeng Cellular Microbiology, Vol. 18, Issue 7 https://doi.org/10.1111/cmi.12564	journal	February 2016
The magnesium inhibition and arrested phagosome hypotheses: new perspectives on the evolution and ecology of Symbiodinium symbioses Malcolm, Hill; April, Hill Biological Reviews, Vol. 87, Issue 4 https://doi.org/10.1111/j.1469-185x.2012.00223.x	journal	March 2012
Isolation of clonal axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity ¹ Xiang, Tingting; Hambleton, Elizabeth A.; DeNofrio, Jan C. Journal of Phycology, Vol. 49, Issue 3 https://doi.org/10.1111/jpy.12055	journal	April 2013
Population genetic data of a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins Thornhill, Daniel J.; Xiang, Yu; Pettay, D. Tye Molecular Ecology, Vol. 22, Issue 17 https://doi.org/10.1111/mec.12416	journal	August 2013
Are Niemann-Pick type C proteins key players in cnidarian-dinoflagellate endosymbioses? Dani, Vincent; Ganot, Philippe; Priouzeau, Fabrice Molecular Ecology, Vol. 23, Issue 18 https://doi.org/10.1111/mec.12876	journal	September 2014
Diurnal and nocturnal transcriptomic variation in the Caribbean staghorn coral, Acropora cervicornis Hemond, Elizabeth M.; Vollmer, Steven V. Molecular Ecology, Vol. 24, Issue 17 https://doi.org/10.1111/mec.13320	journal	August 2015
The transcriptomic response of the coral Acropora digitifera to a competent Symbiodinium strain: the symbiosome as an arrested early phagosome Mohamed, A. R.; Cumbo, V.; Harii, S. Molecular Ecology, Vol. 25, Issue 13 https://doi.org/10.1111/mec.13659	journal	May 2016
Evidence for miRNA-mediated modulation of the host transcriptome in cnidarian-dinoflagellate symbiosis Baumgarten, Sebastian; Cziesielski, Maha J.; Thomas, Ludivine Molecular Ecology, Vol. 27, Issue 2 https://doi.org/10.1111/mec.14452	journal	December 2017
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Microbiota characterization of Exaiptasia diaphana from the Great Barrier Reef Hartman, Leon Michael; van Oppen, Madeleine Josephine Henriette; Blackall, Linda Louise Animal Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/s42523-020-00029-5	journal	April 2020
Menthol-induced bleaching rapidly and effectively provides experimental aposymbiotic sea anemones ( Aiptasia sp.) for symbiosis investigations Matthews, Jennifer L.; Sproles, Ashley E.; Oakley, Clinton A. The Journal of Experimental Biology, Vol. 219, Issue 3 https://doi.org/10.1242/jeb.128934	journal	November 2015
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Transcriptional Activation of c3 and hsp70 as Part of the Immune Response of Acropora millepora to Bacterial Challenges Brown, Tanya; Bourne, David; Rodriguez-Lanetty, Mauricio PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0067246	journal	July 2013
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Long-Term Temperature Stress in the Coral Model Aiptasia Supports the “Anna Karenina Principle” for Bacterial Microbiomes Ahmed, Hanin Ibrahim; Herrera, Marcela; Liew, Yi Jin Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00975	journal	May 2019
Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses Rädecker, Nils; Raina, Jean-Baptiste; Pernice, Mathieu Frontiers in Physiology, Vol. 9 https://doi.org/10.3389/fphys.2018.00214	journal	March 2018
Metabolic co-dependence drives the evolutionarily ancient Hydra–Chlorella symbiosis Hamada, Mayuko; Schröder, Katja; Bathia, Jay eLife, Vol. 7 https://doi.org/10.7554/elife.35122	journal	May 2018

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

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