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Extensive Differences in Gene Expression Between Symbiotic and Aposymbiotic Cnidarians

Erik M Lehnert, Morgan E Mouchka, Matthew S Burriesci and 3 more

G3 Genes|Genomes|Genetics · 2014

doi:10.1534/g3.113.009084

Abstract

Coral reefs provide habitats for a disproportionate number of marine species relative to the small area of the oceans that they occupy. The mutualism between the cnidarian animal hosts and their intracellular dinoflagellate symbionts provides the nutritional foundation for coral growth and formation of reef structures, because algal photosynthesis can provide >90% of the total energy of the host. Disruption of this symbiosis (“coral bleaching”) is occurring on a large scale due primarily to anthropogenic factors and poses a major threat to the future of coral reefs. Despite the importance of this symbiosis, the cellular mechanisms involved in its establishment, maintenance, and breakdown remain largely unknown. We report our continued development of genomic tools to study these mechanisms in Aiptasia, a small sea anemone with great promise as a model system for studies of cnidarian–dinoflagellate symbiosis. Specifically, we have generated de novo assemblies of the transcriptomes of both a clonal line of symbiotic anemones and their endogenous dinoflagellate symbionts. We then compared transcript abundances in animals with and without dinoflagellates. This analysis identified >900 differentially expressed genes and allowed us to generate testable hypotheses about the cellular functions affected by symbiosis establishment. The differentially regulated transcripts include >60 encoding proteins that may play roles in transporting various nutrients between the symbiotic partners; many more encoding proteins functioning in several metabolic pathways, providing clues regarding how the transported nutrients may be used by the partners; and several encoding proteins that may be involved in host recognition and tolerance of the dinoflagellate.

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References 121

  1. 1.

    Adams Y. Smith S. L. Schwartz-Albiez R. Andrews K. T., 2005 Carrageenans inhibit the in vitro growth of Plasmodium falciparum and cytoadhesion to CD36. Parasitol. Res. 97: 290–294

    Not in our library10.1007/s00436-005-1426-3

  2. 2.

    Ainsworth T. D. Wasmund K. Ukani L. Seneca F. Yellowlees D., 2011 Defining the tipping point. A complex cellular life/death balance in corals in response to stress. Sci. Rep. 1: 160

    Not in our library10.1038/srep00160

  3. 3.

    Altura M. A. Stabb E. Goldman W. Apicella M. McFall-Ngai M. J., 2011 Attenuation of host NO production by MAMPs potentiates development of the host in the squid-Vibrio symbiosis. Cell. Microbiol. 13: 527–537

    Not in our library10.1111/j.1462-5822.2010.01552.x

  4. 4.
  5. 5.

    Areschoug T. Gordon S., 2009 Scavenger receptors: role in innate immunity and microbial pathogenesis. Cell. Microbiol. 11: 1160–1169

    Not in our library10.1111/j.1462-5822.2009.01326.x

  6. 6.

    Ashburner M. Ball C. A. Blake J. A. Botstein D. Butler H., 2000 Gene ontology: tool for the unification of biology. Nat. Genet. 25: 25–29

    Not in our library10.1038/75556

  7. 7.

    Augustin R. Riley J. Moley K. H., 2005 GLUT8 contains a [DE]XXXL[LI] sorting motif and localizes to a late endosomal/lysosomal compartment. Traffic 6: 1196–1212

    Not in our library10.1111/j.1600-0854.2005.00354.x

  8. 8.

    Baldauf S. L., 2003 The deep roots of eukaryotes. Science 300: 1703–1706

    Not in our library10.1126/science.1085544

  9. 9.

    Bang M. L. Centner T. Fornoff F. Geach A. J. Gotthardt M., 2001 The complete gene sequence of titin, expression of an unusual approximately 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circ. Res. 89: 1065–1072

    Not in our library10.1161/hh2301.100981

  10. 10.

    Barneah O. Benayahu Y. Weis V. M., 2006 Comparative proteomics of symbiotic and aposymbiotic juvenile soft corals. Mar. Biotechnol. (NY) 8: 11–16

    Not in our library10.1007/s10126-004-5120-8

  11. 11.

    Barshis D. J. Ladner J. T. Oliver T. A. Seneca F. O. Traylor-Knowles N., 2013 Genomic basis for coral resilience to climate change. Proc. Natl. Acad. Sci. USA 110: 1387–1392

    Not in our library10.1073/pnas.1210224110

  12. 12.
  13. 13.

    Bertucci A. Moya A. Tambutté S. Allemand D. Supuran C. T., 2013 Carbonic anhydrases in anthozoan corals—A review. Bioorg. Med. Chem. 21: 1437–1450

    Not in our library10.1016/j.bmc.2012.10.024

  14. 14.

    Burkly L. C. Michaelson J. S. Hahm K. Jakubowski A. Zheng T. S., 2007 TWEAKing tissue remodeling by a multifunctional cytokine: role of TWEAK/Fn14 pathway in health and disease. Cytokine 40: 1–16

    Not in our library10.1016/j.cyto.2007.09.007

  15. 15.

    Burriesci, M. S., 2011 Developing Aiptasia pallida as a tractable model system for cnidarian-dinoflagellate symbiosis: transferred metabolites and designing tools for analysis of ultra-high-throughput-sequencing data. Ph.D. Dissertation, Stanford University, Stanford California.

    Not in our library

  16. 16.

    Burriesci M. S. Raab T. K. Pringle J. R., 2012 Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J. Exp. Biol. 215: 3467–3477

    Not in our library10.1242/jeb.070946

  17. 17.
  18. 18.

    Cates N. McLaughlin J. J. A., 1976 Differences of ammonia metabolism in symbiotic and aposymbiotic Condylactus and Cassiopea spp. J. Exp. Mar. Biol. Ecol. 21: 1–5

    Not in our library

  19. 19.

    Chu H.-T. Hsiao W. W. L. Chen J.-C. Yeh T.-J. Tsai M.-H., 2013 EBARDenovo: Highly accurate de novo assembly of RNA-Seq with efficient chimera-detection. Bioinformatics 29: 1004–1010

    Not in our library10.1093/bioinformatics/btt092

  20. 20.

    Conesa A. Götz S. García-Gómez J. Terol J. Talón M., 2005 Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674

    Not in our library10.1093/bioinformatics/bti610

  21. 21.

    Crossland C. Barnes D. Borowitzka M., 1980 Diurnal lipid and mucus production in the staghorn coral Acropora acuminata. Mar. Biol. 60: 81–90

    Not in our library

  22. 22.

    D’Aoust B. White R. Wells J. Olsen D., 1976 Coral-algal associations: capacity for producing and sustaining elevated oxygen tensions in situ. Undersea Biomed. Res. 3: 35–40

    Not in our library

  23. 23.

    Davidson S. K. Koropatnick T. A. Kossmehl R. Sycuro L. McFall-Ngai M. J., 2004 NO means “yes” in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell. Microbiol. 6: 1139–1151

    Not in our library10.1111/j.1462-5822.2004.00429.x

  24. 24.

    Davy S. K. Allemand D. Weis V. M., 2012 Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76: 229–261

    Not in our library10.1128/mmbr.05014-11

  25. 25.

    De’ath G. Fabricius K. E. Sweatman H. Puotinen M., 2012 The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc. Natl. Acad. Sci. USA 109: 17995–17999

    Not in our library10.1073/pnas.1208909109

  26. 26.

    Dennis G. Sherman B. T. Hosack D. A. Yang J. Gao W., 2003 DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4: 3

    Not in our library

  27. 27.

    Detournay O. Schnitzler C. E. Poole A. Weis V. M., 2012 Regulation of cnidarian–dinoflagellate mutualisms: evidence that activation of a host TGFβ innate immune pathway promotes tolerance of the symbiont. Dev. Comp. Immunol. 38: 525–537

    Not in our library10.1016/j.dci.2012.08.008

  28. 28.

    Downs C. A. Fauth J. E. Halas J. C. Dustan P. Bemiss J., 2002 Oxidative stress and seasonal coral bleaching. Free Radic. Biol. Med. 33: 533–543

    Not in our library10.1016/s0891-5849(02)00907-3

  29. 29.

    Dudler N. Yellowlees D. Miller D. J., 1987 Localization of two L-glutamate dehydrogenases in the coral Acropora latistella. Arch. Biochem. Biophys. 254: 368–371

    Not in our library10.1016/0003-9861(87)90112-3

  30. 30.

    Dunn S. R. Weis V. M., 2009 Apoptosis as a post-phagocytic winnowing mechanism in a coral-dinoflagellate mutualism. Environ. Microbiol. 11: 268–276

    Not in our library10.1111/j.1462-2920.2008.01774.x

  31. 31.

    Dunn S. R. Bythell J. C. Le Tissier M. D. A. Burnett W. J. Thomason J. C., 2002 Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J. Exp. Mar. Biol. Ecol. 272: 29–53

    Not in our library

  32. 32.

    Dunn S. R. Thomason J. C. Le Tissier M. D. A. Bythell J. C., 2004 Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell Death Differ. 11: 1213–1222

    Not in our library10.1038/sj.cdd.4401484

  33. 33.

    Dunn S. R. Phillips W. S. Green D. R. Weis V. M., 2007 Knockdown of actin and caspase gene expression by RNA interference in the symbiotic anemone Aiptasia pallida. Biol. Bull. 212: 250–258

    Not in our library10.2307/25066607

  34. 34.

    Dykens J. A. Shick J. M., 1982 Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297: 579–580

    Not in our library

  35. 35.

    Edgar R. C., 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792–1797

    Not in our library10.1093/nar/gkh340

  36. 36.

    Edgar R. C., 2010 Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461

    Not in our library10.1093/bioinformatics/btq461

  37. 37.

    Fitt W. K., 2000 Cellular growth of host and symbiont in a cnidarian-zooxanthellar symbiosis. Biol. Bull. 198: 110–120

    Not in our library10.2307/1542809

  38. 38.

    Frolov A. Zielinski S. E. Crowley J. R. Dudley-Rucker N. Schaffer J. E., 2003 NPC1 and NPC2 regulate cellular cholesterol homeostasis through generation of low density lipoprotein cholesterol-derived oxysterols. J. Biol. Chem. 278: 25517–25525

    Not in our library10.1074/jbc.m302588200

  39. 39.

    Furla P. Allemand D. Shick J. M. Ferrier-Pagès C. Richier S., 2005 The symbiotic anthozoan: a physiological chimera between alga and animal. Integr. Comp. Biol. 45: 595–604

    Not in our library10.1093/icb/45.4.595

  40. 40.

    Ganot P. Moya A. Magnone V. Allemand D. Furla P., 2011 Adaptations to endosymbiosis in a cnidarian-dinoflagellate association: differential gene expression and specific gene duplications. PLoS Genet. 7: e1002187

    Not in our library10.1371/journal.pgen.1002187

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