Transcriptomic analysis of differential host gene expression upon uptake of symbionts: A case study with Symbiodinium and the major bioeroding sponge Cliona varians

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Riesgo, Ana ^a,b   Peterson, Kristin ^c,d   Richardson, Crystal ^c,e   Heist, Tyler ^c   Strehlow, Brian ^c,f   McCauley, Mark ^c,g   Cotman, Carlos ^c   Hill, Malcolm ^c   Hill, April ^c  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF RICHMOND   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF VIRGINIA   (United States)

^f UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^g UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

Genetic integration; Porifera; Symbiosis; Transcriptome; Zooxanthellae

Indexed keywords

TRANSCRIPTOME;

ANIMAL TISSUE; ARTICLE; CLIONA VARIANS; CONTROLLED STUDY; ECOLOGICAL NICHE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HOST PATHOGEN INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; RNA SEQUENCE; SPONGE (PORIFERA); SUPPRESSION SUBTRACTIVE HYBRIDIZATION; SYMBIODINIUM; SYMBIONT; SYMBIOSIS; TRANSCRIPTOMICS; UNITED STATES; ANIMAL; BIOLOGY; DINOFLAGELLATE; GENE EXPRESSION REGULATION; GENETICS; MOLECULAR GENETICS; REPRODUCIBILITY;

CLIONA; PORIFERA; SYMBIODINIUM;

ANIMALS; COMPUTATIONAL BIOLOGY; DINOFLAGELLIDA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MOLECULAR SEQUENCE ANNOTATION; PORIFERA; REPRODUCIBILITY OF RESULTS; SYMBIOSIS; TRANSCRIPTOME;

EID: 84903419804     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-376     Document Type: Article

References (69)

1. Douglas AE. The symbiotic habit 2010, Princeton: Princeton University Press.
2. Medina M, Sachs JL. Symbiont genomics, our new tangled bank. Genomics 2010, 95:129-137. 10.1016/j.ygeno.2009.12.004, 20053372.
3. Muscatine L, Porter JW. Reef corals - mutualistic symbioses adapted to nutrient-poor environments. Bioscience 1977, 27:454-460.
4. Trench RK. Dinoflagellates in non-parasitic symbioses. The biology of dinoflagellates 1987, 530-570. Oxford: Blackwell, Taylor FJR.
5. Veron JEN. Corals in space and time: the biogeography and evolution of the Scleractinia 1995, Ithaca, NY: Cornell University Press.
6. Coffroth M, Santos S. Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 2005, 156:19-34. 10.1016/j.protis.2005.02.004, 16048130.
7. Boschma H. On the feeding reactions and digestion in the coral polyp Astrangia danae, with notes on its symbionts with zooxanthellae. Biol Bull 1925, 49:407-439.
8. Kawaguchi S. On the physiology of reef corals. VII. The zooxanthella of the reef corals is Gymnodinium sp. Dinoflagellata its culture in vitro. Palao Trop Biol Stn Stud 1944, 2:675-679.
9. Stat M, Carter D, Hoegh-Guldberg O. The evolutionary history of Symbiodinium and scleractinian hosts - symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol 2006, 8:23-43.
10. Weisz J, Massaro A, Ramsby B, Hill M. Zooxanthellar symbionts shape host sponge trophic status through translocation of carbon. Biol Bull 2010, 219:189-197.
11. Stambler N. Marine microralgae/cyanobacteria -invertebrate symbiosis, trading energy for strategic material. All flesh is grass: plant-animal interrelationships 2011, 383-414. Seckbach J, Dubinsky Z, 16.
12. Stambler N. Zooxanthellae: The yellow symbionts inside animals. Coral Reefs: An Ecosystem in Transition 2011, 87-106. New York (NY): Springer, Dubinsky Z, Stambler N.
13. Hill MS, Hill AL. The arrested phagosome and magnesium inhibition hypothesis: novel perspectives on Symbiodinium symbioses. Biol Rev 2012, 87:804-821. 10.1111/j.1469-185X.2012.00223.x, 22404964.
14. Colombo-Pallotta MF, Rodríguez-Román A, Iglesias-Prieto R. Calcification in bleached and unbleached Montastrea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 2010, 29:899-907.
15. Oliver TA, Palumbi SR. Do fluctuating temperature environments elevate coral thermal tolerance?. Coral Reefs 2011, 30:429-440.
16. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL. Projecting coral reef futures under global warming and ocean acidification. Science 2011, 333:418-422. 10.1126/science.1204794, 21778392.
17. McClanahan T, Weil E, Cortés J, Baird AH, Ateweberhan M. Consequences of coral bleaching for sessile reef organisms. Ecological studies: Coral bleaching: patterns, processes, causes and consequences 2009, 121-138. Berlin Heidelberg: Springer, van Oppen MJH, Lough JM.
18. Brandt ME, McManus JW. Disease incidence is related to bleaching extent. Ecology 2009, 90:2859-2867. 10.1890/08-0445.1, 19886494.
19. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J. Climate change, human impacts, and the resilience of coral reefs. Science 2003, 301:929-933. 10.1126/science.1085046, 12920289.
20. Wilkinson C. Status of coral reefs of the world: 2008 2008, Townsville, Australia: Global coral reef monitoring network and reef and rainforest research centre.
21. Maynard JAM, Turner PJ, Anthony KRN, Baird AH, Berkelmans R, Eakin CM, Johnson J, Marshall PA, Packer GR, Rea A, Willis BL. ReefTemp: an interactive monitoring system for coral bleaching using high-resolution SST and improved stress predictors. Geophys Res Lett 2008, 35:L0560.
22. Jeong HJ, Du Yoo Y, Kang NS, Lim AS, Seong KA, Lee SY, Lee MJ, Lee KH, Kim HS, Shin W, Nam SW, Yih W, Lee K. Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc Natl Acad Sci U S A 2012, 109:12604-12609. 10.1073/pnas.1204302109, 3412036, 22814379.
23. Takabayashi M, Adams LM, Pochon X, Gates RD. Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawaii and Florida. Coral Reefs 2012, 31:157-167.
24. Rodriguez-Lanetty M, Phillips WS, Weis VM. Transcriptome analysis of a cnidarian - dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 2006, 7:23. 10.1186/1471-2164-7-23, 1408080, 16472376.
25. Rodriguez-Lanetty M, Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM. Temporal and spatial infection dynamics indicate recognition events in the early hours of a dinoflagellate/coral symbiosis. Mar Biol 2006, 149:713-719.
26. Sunagawa S, Wilson EC, Thaler M, Smith ML, Caruso C, Pringle JR, Weis VM, Medina M, Schwarz JA. Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics 2009, 10:258. 10.1186/1471-2164-10-258, 2702317, 19500365.
27. Voolstra CR, Schwarz JA, Schnetzer J, Sunagawa S, Desalvo MK, Szmant AM, Coffroth MA, Medina M. The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Mol Ecol 2009, 18:1823-1833. 10.1111/j.1365-294X.2009.04167.x, 19317843.
28. De Salvo MK, Sunagawa S, Fisher PL, Voolstra CR, Iglesias-Prieto R, Medina M. Coral host transcriptomic states are correlated with Symbiodinium genotypes. Mol Ecol 2010, 19:1174-1186. 10.1111/j.1365-294X.2010.04534.x, 20149089.
29. Peng S, Wang Y, Wang L, Chen WU, Lu C, Fang L, Chen C. Proteomic analysis of symbiosome membranes in cnidaria-dinoflagellate endosymbiosis. Proteomics 2010, 10:1002-1016.
30. Ganot P, Moya A, Magnone V, Allemand D, Furla P, Sabourault C. Adaptations to endosymbiosis in a cnidarian-dinoflagellate association: differential gene expression and specific gene duplications. PLoS Genet 2011, 7:e1002187. 10.1371/journal.pgen.1002187, 3141003, 21811417.
31. Levy O, Kaniewska P, Alon S, Eisenberg E, Karako-Lampert S, Bay LK, Reef R, Rodriguez-Lanetty M, Miller DJ, Hoegh-Guldberg O. Complex diel cycles of gene expression in coral-algal symbiosis. Science 2011, 331:175. 10.1126/science.1196419, 21233378.
32. Wooldridge SA. Is the coral-algae symbiosis really 'mutually beneficial' for the partners?. Bioessays 2010, 32:615-625. 10.1002/bies.200900182, 20517874.
33. Meyer E, Weis VM. Study of cnidarian-algal symbiosis in the " Omics" age. Biol Bull 2012, 223:44-65.
34. Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M, Pringe JR. Cell biology in model systems as the key to understanding corals. Trends Ecol Evol 2008, 23:369-376. 10.1016/j.tree.2008.03.004, 18501991.
35. Schönberg CHL, Loh WKW. Molecular identity of the unique symbiotic dinoflagellates found in the bioeroding demosponge Cliona orientalis. Mar Ecol Prog Ser 2005, 299:157-166.
36. Granados C, Camargo C, Zea S, Sanchez JA. Phylogenetic relationships among zooxanthellae (Symbiodinium) associated to excavating sponges (Cliona spp.) reveal an unexpected lineage in the Caribbean. Mol Phylogenet Evol 2008, 49:554-560. 10.1016/j.ympev.2008.07.023, 18725307.
37. Pochon X, Gates RD. A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol Phylogenet Evol 2010, 56:492-497. 10.1016/j.ympev.2010.03.040, 20371383.
38. Hill M, Allenby A, Ramsby B, Schönberg C, Hill A. Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: evidence of heteroplasmy and putative host-specific symbiont lineages. Mol Phylogenet Evol 2011, 59:81-88. 10.1016/j.ympev.2011.01.006, 21256238.
39. Hill M, Wilcox T. Unusual mode of symbiont repopulation after bleaching in Anthosigmella varians: acquisition of different zooxanthellae strains. Symbiosis 1998, 25:279-289.
40. Hill MS. Spongivory on Caribbean reefs releases corals from competition with sponges. Oecologia 1998, 117:143-150.
41. Hill MS, Hill AL. Porifera (Sponges). Encyclopedia of Inland Waters, Volume 2 2009, 423-432. Oxford: Elsevier, Likens GE.
42. Rivera A, Hammel J, Haen K, Danka ES, Cieniewicz B, Winters IP, Posfai D, Wörheide G, Lavrov DV, Knight SW, Hill MS, Hill AL. RNA interference in marine and freshwater sponges: actin knockdown in Tethya wilhelma and Ephydatia muelleri by ingested dsRNA expressing bacteria. BMC Biotechnol 2011, 11:67. 10.1186/1472-6750-11-67, 3146823, 21679422.
43. Richardson C, Hill M, Runyen-Janecky L, Hill A. Experimental manipulation of sponge: bacterial symbiont community composition with antibiotics: sponge cell aggregates as a unique tool to study animal: microbe symbiosis. FEMS Microbiol Ecol 2012, 81:407-418. 10.1111/j.1574-6941.2012.01365.x, 22432637.
44. Hill MS, Hill AL, Lopez J, Peterson KJ, Pomponi S, Diaz MC, Thacker RW, Adamska M, Boury-Esnault N, Cárdenas P, Chaves-Fonnegra A, Danka E, De Laine B, Formica D, Hajdu E, Lobo-Hajdu G, Klontz S, Morrow CC, Patel J, Picton B, Pisani D, Pohlmann D, Redmond NE, Reed J, Richie S, Riesgo A, Rubin E, Russell Z, Rützler K, Sperling EA, et al. Reconstruction of family-level phylogenetic relationships within Demospongiae (Porifera) using nuclear encoded housekeeping genes. PLoS One 2013, 8:e50437. 10.1371/journal.pone.0050437, 3553142, 23372644.
45. Thacker RW, Hill AL, Hill MS, Redmond NE, Collins AG, Morrow CC, Spicer L, Carmack CA, Zappe ME, Pohlmann D, Hall C, Diaz MC, Bangalore PV. Nearly complete 28S rRNA gene sequences confirm new hypotheses of sponge evolution. Integr Comp Biol 2013, 53:373-387. 10.1093/icb/ict071, 23748742.
46. Hill MS. Symbiotic zooxanthellae enhance boring and growth rates of the tropical sponge Anthosigmella varians forma varians. Mar Biol 1996, 125:649-654.
47. Andersonn AJ, Gledhill D. Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Annu Rev Mar Sci 2013, 5:321-348.
48. Scalera-Liaci L, Sciscioli M, Lepore E, Gaino E. Symbiotic zooxanthellae in Cinachyra tarentina, a non-boring demosponge. Endocyt Cell Res 1999, 13:105-114.
49. De Wit P, Pespeni MH, Ladner JT, Barshis DJ, Seneca F, Jaris H, Overgaard Therkildsen N, Morikawa M, Palumbi SR. The simple fool's guide to population genomics via RNA-Seq: an introduction to high-throughput sequencing data analysis. Mol Ecol Res 2012, 12:1058-1067.
50. Riesgo A, Andrade SCS, Sharma PP, Novo M, Pérez-Porro AR, Vahtera V, González VL, Kawauchi GY, Giribet G. Comparative description of ten transcriptomes of newly sequenced invertebrates and efficiency estimation of genomic sampling in non-model taxa. Front Zool 2012, 9:1-24. 10.1186/1742-9994-9-1, 3312819, 22269662.
51. Pérez-Porro AR, Navarro-Gómez D, Uriz MJ, Giribet G. A NGS approach to the encrusting Mediterranean sponge Crella elegans (Porifera, Demospongiae, Poecilosclerida): transcriptome sequencing, characterization and overview of the gene expression along three life cycle stages. Mol Ecol Resour 2013, 13:494-509. 10.1111/1755-0998.12085, 23437888.
52. Novo M, Riesgo A, Fernández-Guerra A, Giribet G. Pheromone evolution, reproductive genes, and comparative transcriptomics in Mediterranean earthworms (Annelida, Oligochaeta, Hormogastridae). Mol Biol Evol 2013, 30:1614-1629. 10.1093/molbev/mst074, 23596327.
53. Novara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P. HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 2010, 22:3130-3141. 10.1105/tpc.110.077040, 2965548, 20884801.
54. Ewen-Campen B, Shaner N, Panfilio KA, Suzuki Y, Roth S, Extavour CG. The maternal and early embryonic transcriptome of the milkweed bug Oncopeltus fasciatus. BMC Genomics 2011, 12:61. 10.1186/1471-2164-12-61, 3040728, 21266083.
55. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010, 11(10):R106. 10.1186/gb-2010-11-10-r106, 3218662, 20979621.
56. Supek F, Bošnjak M, Škunca N, Šmuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 2011, 6:e21800. 10.1371/journal.pone.0021800, 3138752, 21789182.
57. Julian D, Statile JL, Wohlgemuth SE, Arp AJ. Enzymatic hydrogen sulfide production in marine invertebrate tissues. Comp Biochem Physiol 2002, 133:105-115.
58. Taylor MW, Radax R, Steger D, Wagner M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 2007, 71:295-347. 10.1128/MMBR.00040-06, 1899876, 17554047.
59. Luo BH, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol 2007, 25:619-647. 10.1146/annurev.immunol.25.022106.141618, 1952532, 17201681.
60. Bond JS, Beynon RJ. The astacin family of metalloendopeptidases. Protein Sci 1995, 4:1247-1261. 10.1002/pro.5560040701, 2143163, 7670368.
61. Ben-Shlomo R. The molecular basis of allorecognition in ascidians. Bioessays 2008, 30:1048-1051. 10.1002/bies.20848, 18937348.
62. Buddemeier RW, Fautin DG. Coral bleaching as an adaptive mechanism - a testable hypothesis. Bioscience 1993, 43:320-326.
63. Cunning R, Baker AC. Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Change 2012, 3:259-262.
64. Yuyama I, Watanabe T, Takei Y. Profiling differential gene expression of symbiotic and aposymbiotic corals using a high coverage gene expression profiling (HiCEP) analysis. Mar Biotechnol 2011, 13:32-40. 10.1007/s10126-010-9265-3, 20333427.
65. Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshwater Res 1999, 50:839-866.
66. Hoegh-Guldberg O, Bruno JF. The impact of climate change on the world's marine ecosystems. Science 2010, 328:1523-1528. 10.1126/science.1189930, 20558709.
67. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinforma 2009, 10:421.
68. Conesa A, Götz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676. 10.1093/bioinformatics/bti610, 16081474.
69. O'Neil ST, Dzurisin JDK, Carmichael RD, Lobo NF, Emrich SJ, Hellmann JJ. Population-level transcriptome sequencing of nonmodel organisms Erynnis propertius and Papilio zelicaon. BMC Genomics 2010, 11:310. 10.1186/1471-2164-11-310, 2887415, 20478048.