Deep-sequencing method for quantifying background abundances of Symbiodinium types: Exploring the rare Symbiodinium biosphere in reef-building corals

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Quigley, Kate M ^a   Davies, Sarah W ^b   Kenkel, Carly D ^b   Willis, Bette L ^a   Matz, Mikhail V ^b   Bay, Line K ^c  

^a JAMES COOK UNIVERSITY   (Australia)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

INTERNAL TRANSCRIBED SPACER 2;

ACROPORA DIGITIFERA; ACROPORA HYACINTHUS; ARTICLE; BIOSPHERE; CONTROLLED STUDY; CORAL; CORAL REEF; DATA ANALYSIS SOFTWARE; ENDOSYMBIONT; GENE LOCUS; GENETIC MARKER; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC ORIGIN; ITS 2 GENE; LIMIT OF DETECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PALAU; POPULATION ABUNDANCE; QUANTITATIVE STUDY; RNA GENE; RNA SEQUENCE; SENSITIVITY AND SPECIFICITY; SPECIES COMPARISON; SPECIES COMPOSITION; SYMBIODINIUM; SYMBIODINIUM MICROADRIATICUM; SYMBIOSIS; ANIMAL; ANTHOZOA; DINOFLAGELLATE; ECOSYSTEM; GENETICS; HAPLOTYPE; HIGH THROUGHPUT SEQUENCING; PHYSIOLOGY; PROCEDURES;

ANIMALS; ANTHOZOA; BASE SEQUENCE; CORAL REEFS; DINOFLAGELLIDA; ECOSYSTEM; HAPLOTYPES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; LIMIT OF DETECTION; PALAU; SYMBIOSIS;

EID: 84899629877     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094297     Document Type: Article

References (97)

1. Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci USA 98: 5419-5425. (Pubitemid 32435657)
2. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol, Evol Syst 34: 661-689. (Pubitemid 38171434)
3. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. Bioscience 34: 705-709.
4. Cantin N, van Oppen M, Willis B, Mieog J, Negri A (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28: 405-414.
5. Muscatine L, Goiran C, Land L, Jaubert J, Cuif J-P, et al. (2005) Stable isotopes (d13C and d15N) of organic matrix from coral skeleton. Proc Natl Acad Sci USA 102: 1525-1530.
6. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci U S A 105: 17442-17446.
7. Anthony KRN, Maynard JA, Diaz-Pulido G, Mumby PJ, Marshall PA, et al. (2011) Ocean acidification and warming will lower coral reef resilience. Global Change Biol 17: 1798-1808.
8. Reynolds JM, Bruns BU, Fitt WK, Schmidt GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci USA 105: 13674-13678.
9. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Aust J Mar Freshw Res 50: 839-866. (Pubitemid 30018479)
10. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, et al. (2003) Climate Change, Human Impacts, and the Resilience of Coral Reefs. Science 301: 929-933. (Pubitemid 36994796)
11. van Oppen MJH, Baker AC, Coffroth MA, Willis BL (2009) Bleaching resistance and the role of algal endosymbionts coral bleaching. In: van Oppen M, Lough J, editors. Berlin/Heidelberg: Springer. pp.83-102.
12. Smith RT, Pinzon JH, LaJeunesse TC (2009) Symbioinium (Dinophyta) diversity and stability in aquarium corals. J Phycol 45: 1030-1036.
13. Baker AC, Romanski AM (2007) Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: Comment on Goulet (2006). Mar Ecol Prog Ser 335: 237-242. (Pubitemid 46797410)
14. Silverstein RN, Correa AMS, Baker AC (2012) Specificity is rarely absolute in coral-algal symbiosis: implications for coral response to climate change. Proc R Soc Biol Sci Ser B 1738: 2609-2618.
15. Mieog J, van Oppen M, Cantin N, Stam W, Olsen J (2007) Real-time PCR reveals a high incidence of Symbiodinium; clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs 26: 449-457. (Pubitemid 350104765)
16. Mieog J, van Oppen M, Berkelmans R, Stam W, Olsen J (2009) Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Mol Ecol Resour 9: 74-82.
17. Lewis CL, Coffroth MA (2004) The Acquisition of Exogenous Algal Symbionts by an Octocoral After Bleaching. Science 304: 1490-1492. (Pubitemid 38720926)
18. Toller WW, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull (Woods Hole) 201: 360-373. (Pubitemid 34057132)
19. LaJeunesse TC, Smith RT, Finney J, Oxenford H (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral 'bleaching' event. Proc R Soc Biol Sci Ser B 276: 4139-4148.
20. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proc R Soc Biol Sci Ser B 273: 2305-2312. (Pubitemid 44387337)
21. Abrego D, Ulstrup KE, Willis BL, van Oppen MJH (2008) Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc Biol Sci Ser B 275: 2273-2282.
22. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304: 1492-1494. (Pubitemid 38720927)
23. Thornhill DJ, Kemp DW, Bruns BU, Fitt WK, Schmidt GW (2008) Correspondence between cold tolerance and temperate biogeography in a western atlantic Symbiodinium (Dinophyta) lineage. J Phycol 44: 1126-1135.
24. Jones A, Berkelmans R (2010) Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS ONE 5.
25. Loram JE, Trapido-Rosenthal HG, Douglas AE (2007) Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Mol Ecol 16: 4849-4857. (Pubitemid 350135210)
26. Frade PR, Englebert N, Faria J, Visser PM, Bak RPM (2008a) Distribution and photobiology of Symbiodinium types in different light environments for three colour morphs of the coral Madracis pharensis: is there more to it than total irradiance? Coral Reefs 27: 913-925.
27. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, et al. (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Clim Change 2: 116-120.
28. LaJeunesse T, Reyes-Bonilla H, Warner M (2007) Spring ''bleaching'' among Pocillopora; in the Sea of Cortez, Eastern Pacific. Coral Reefs 26: 265-270. (Pubitemid 46870816)
29. Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24: 16-20.
30. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006) Multiyear, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148: 711-722. (Pubitemid 43183831)
31. Fabricius KE, Mieog JC, Colin PL, Idip D, H. van Oppen MJ (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol 13: 2445-2458. (Pubitemid 38946432)
32. LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull (Woods Hole) 199: 126-134.
33. van Oppen MJH, Palstra FP, Piquet AM-T, Miller DJ (2001) Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc R Soc Lond, Ser B: Biol Sci 268: 1759-1767. (Pubitemid 32844022)
34. Thornhill DJ, Lajeunesse TC, Santos SR (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 16: 5326-5340. (Pubitemid 350265260)
35. Davy SK, Allemand D, Weis VM (2012) Cell Biology of Cnidarian- Dinoflagellate Symbiosis. Microbiol Mol Biol Rev 76: 229-261.
36. Correa A, McDonald M, Baker A (2009) Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade symbionts in Caribbean corals. Mar Biol 156: 2403-2411.
37. Goffredi SK, Johnson SB, Vrijenhoek RC (2007) Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms. Appl Environ Microbiol 7: 2314-2323. (Pubitemid 46649524)
38. Gates RD, Ainsworth TD (2011) The nature and taxonomic composition of coral symbiomes as drivers of performance limits in scleractinian corals. J Exp Mar Biol Ecol 408: 94-101.
39. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, et al. (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12: 2070-2082.
40. Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9: 2707-2719. (Pubitemid 47547539)
41. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, et al. (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6: 564-576.
42. Gaidos E, Rusch A, Ilardo M (2011) Ribosomal tag pyrosequencing of DNA and RNA from benthic coral reef microbiota: community spatial structure, rare members and nitrogen-cycling guilds. Environ Microbiol 13: 1138-1152.
43. Pedrós-Alió C (2012) The Rare Bacterial Biosphere. Annual Review of Marine Science 4: 449-466.
44. Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19: 5555-5565.
45. Bik HM, Porazinska DL, Creer S, Caporaso JG, Knight R, et al. (2012) Sequencing our way towards understanding global eukaryotic biodiversity. Trends Ecol Evol 27: 233-243.
46. Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts-Symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8: 23-43. (Pubitemid 44311626)
47. Apprill AM, Gates RD (2007) Recognizing diversity in coral symbiotic dinoflagellate communities
48. Stat M, Gates RD (2011) Clade D Symbiodinium in Scleractinian Corals: A ''Nugget'' of Hope, a Selfish Opportunist, an Ominous Sign, or All of the Above? Journal of Marine Biology 2011: 1-9.
49. Song J, Shi L, Li D, Sun Y, Niu Y, et al. (2012) Extensive pyrosequencing reveals frequent intra-genomic variations of internal transcribed spacer regions of nuclear ribosomal DNA. PloS one 7: e43971.
50. Kenkel C, Goodbody-Gringley G, Caillaud D, Davies S, Bartels E, et al. (2013) Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol 22: 4335-4348.
51. de O Santos E, Alves N, Dias GM, Mazotto AM, Vermelho A, et al. (2011) Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire. ISME 5: 1471-1483.
52. Bay LK, Howells EJ, van Oppen MJH (2009) Isolation, characterisation and cross amplification of thirteen microsatellite loci for coral endo-symbiotic dinoflagellates (Symbiodinium clade C). Conserv Genet Resour 1: 199-203.
53. LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiont dinoflagellates in the genus Symbiodinium using the ITS region: in search of a ''species'' level marker. J Phycol 37: 866-880.
54. Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139: 1069-1078. (Pubitemid 34049858)
55. Davies SW, Rahman M, Meyer E, Green EA, Buschizarro E, et al. (2012) Novel polymorphic microsatellite markers for population genetics of the endangered Caribbean star coral, Montastraea faveolata. Marine Biodiversity 2013: 1-6.
56. Ulstrup KE, van Oppen MJH (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12: 3477-3484. (Pubitemid 37496707)
57. Niu B, Fu L, Sun S, Li W (2010) Artificial and natural duplicates in pyrosequencing reads of metagenomic data. BMC Bioinformatics 11.
58. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215.
59. Pruitt KD, Tatusova T, Browh GR, Maglott DR (2012) NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Research 40: D130-D135.
60. Leggat W, Yellowlees D, Medina M (2011) Recent progress in Symbiodinium transcriptomics. J Exp Mar Biol Ecol 408: 120-125.
61. Stat M, Bird CE, Pochon X, Chasqui L, Chauka LJ, et al. (2011) Variation in Symbiodinium ITS2 Sequence Assemblages among Coral Colonies. PLoS ONE 6: e15854.
62. Fox J, Weisberg S (2011) An {R} Companion to Applied Regression, Second Edition. Thousand Oaks, CA: Sage. Available: http://socserv.socsci.mcmaster. ca/jfox/Books/Companion
63. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9: 1657-1659.
64. R Core Team (2012) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available: http:// www.R-project.org
65. Harrell FE (2007) R package Harrell Miscellaneous (Hmisc). 3.2-1 ed: Available: http://biostat.mc.vanderbilt.edu/s/Hmisc
66. Bodenhofer U, Krone M, Klawonn F (2012) Testing noisy numerical data for monotonic association. Inform Sci.
67. Bodenhofer U, Klawonn F (2008) Robust rank correlation coefficients on the basis of fuzzy orderings: initial steps. Mathware Soft Comput 1: 5-20.
68. Paradis E (2010) Pegas: an R package for population genetics with an integratedmodular approach. Bioinformatics 26: 419-420.
69. Metzker ML (2010) Application of Next-Generation Sequencing technologies-the next generation. Nat Rev Genet 11: 31-46.
70. LaJeunesse T, Bhagooli R, Hidaka M, Devantier L, Done T, et al. (2004a) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284: 147-161. (Pubitemid 40134218)
71. LaJeunesse TC, Loh WKW, Woesik Rv, Hoegh-Guldberg O, Schmidt GW, et al. (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr 48: 2046-2054. (Pubitemid 37207606)
72. Tonk L, Bongaerts P, Sampayo EM, Hoegh-Guldberg O (2013) SymbioGBR: a web-based database of Symbiodinium associated with cnidarian hosts on the Great Barrier Reef. BMC Ecol 13: 7.
73. Drew EA (1972) The biology and physiology of alga-invertebrates symbioses. II. The density of symbiotic algal cells in a number of hermatypic hard corals and alcyonarians from various depths. J Exp Mar Biol Ecol 9: 71-75.
74. Kembel SW, Wu M, Eisen JA, Green JL (2012) Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLoS Comp Biol 8: e1002743.
75. Pilloni G, Granitsiotis MS, Engel M, Lueders T (2012) Testing the limits of 454 pyrotag sequencing: reproducibility, quantitative assessment and comparison to T-RFLP fingerprinting of aquifer microbes. PloS one 7: e40467.
76. Egge E, Bittner L, Andersen T, Audic S, de Vargas C, et al. (2013) 454 pyrosequencing to describe microbial eukaryotic community composition, diversity and relative abundance: a test for marine haptophytes. PloS one 8: e74371.
77. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci U S A 92: 2850-2853.
78. LaJeunesse TC (2005) ''Species'' Radiations of Symbiotic Dinoflagellates in the Atlantic and Indo-Pacific Since the Miocene-Pliocene Transition. Mol Biol Evol 22: 570-581.
79. Garren M, Walsh SM, Caccone A, Knowlton N (2006) Patterns of association between Symbiodinium and members of the Montastraea annularis species complex on spatial scales ranging from within colonies to between geographic regions. Coral Reefs 4: 503-512. (Pubitemid 44748964)
80. Stat M, Morris E, Gates RD (2008) Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci U S A 27: 9256-9261.
81. Thornhill D, Fitt W, Schmidt G (2006) Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25: 515-519. (Pubitemid 44748966)
82. LaJeunesse TL (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141: 387-400.
83. LaJeunesse TC, Bonilla HR, Warner ME, Wills M, Schmidt GW, et al. (2008) Specificity and stability in high latitude eastern Pacific coral-algal symbioses. Limnol Oceanogr 53: 719-727. (Pubitemid 351705422)
84. Howells EJ, Willis BL, Bay LK, van Oppen MJH (2013) Spatial and temporal genetic structure of Symbiodinium populations within a common reef-building coral on the Great Barrier Reef. Mol Ecol 22: 3693-3708.
85. Pochon X, Putnam H, Burki F, Gates R (2012) Identifying and characterizing alternative molecular markers for the symbiotic and free-living dinoflagellate genus Symbiodinium. PLoS ONE 7: e29816.
86. LaJeunesse TC, Thornhill DJ (2011) Improved resolution of reef-coral endosymbiont Symbiodinium species diversity, ecology, and evolution through psbA non-coding region Genotyping. PLoS ONE 6: e29013.
87. Lin S (2006) The smallest dinoflagellate genome is yet to be found: a comment on LaJeunesse et al. ''Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among Dinoflagellates''. J Phycol 42: 746-748. (Pubitemid 43807279)
88. Hou Y, Lin S (2009) Distinct Gene Number-Genome Size Relationships for Eukaryotes and Non-Eukaryotes: Gene Content Estimation for Dinoflagellate Genomes. PLoS ONE 4: e6978.
89. Zhang Z, Green BR, Cavalier-Smith T (2000) Phylogeny of Ultra-Rapidly Evolving Dinoflagellate Chloroplast Genes: A Possible Common Origin for Sporozoan and Dinoflagellate Plastids. J Mol Evol 51: 26-40. (Pubitemid 30469699)
90. Stat M, Pochon X, Cowie R, Gates R (2009) Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar Ecol Prog Ser 386: 83-96.
91. Sanders JG, Palumbi SR (2011) Populations of Symbiodinium muscatinei Show Strong Biogeographic Structuring in the Intertidal Anemone Anthopleura elegantissima. Biol Bull (Woods Hole) 220: 199-208.
92. Stat M, Gates RD (2008) Vectored introductions of marine endosymbiotic dinoflagellates into Hawaii. Biol Invasions 10: 579-583. (Pubitemid 351422021)
93. Wolf M, Chen S, Song J, Ankenbrand M, Mü ller T (2013) Compensatory base changes in ITS2 secondary structures correlate with the biological species concept despite intragenomic variability in ITS2 sequences-a proof of concept. PloS one 8: e66726.
94. Wolf M, Achtziger M, Schultz J, Dandekar T, Mü ller T (2005) Homology modeling revealed more than 20,000 rRNA internal transcribed spacer 2 (ITS2) secondary structures. RNA 11: 1616-1623. (Pubitemid 41505535)
95. Lein H-E, Dai C-F, Wallace CC (2004) Secondary structure and phylogenetic utility of the ribosomal internal transcribed spacer 2 (ITS2) in scleractinian corals. Zool Stud 43: 759-771. (Pubitemid 40112761)
96. Kenkel CD, Goodbody-Gringley G, Caillaud D, Davies SW, Bartels E, et al. Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol: in press.
97. Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc R Soc Biol Sci Ser B 1746: 4352-4361.