Do the shuffle: Changes in Symbiodinium consortia throughout juvenile coral development

PLoS ONE

Volumn 12, Issue 2, 2017, Pages

  Reich, Hannah G ^a   Robertson, Deborah L ^a   Goodbody Gringley, Gretchen ^b  

^a CLARK UNIVERSITY   (United States)

^b BERMUDA INSTITUTE OF OCEAN SCIENCES   (Bermuda)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; CORAL; GENE AMPLIFICATION; JUVENILE; NONHUMAN; PLANULA; SYMBIODINIUM; SYMBIONT; ANIMAL; ANTHOZOA; ATLANTIC ISLANDS; BERMUDA; BIODIVERSITY; BIOTA; CARIBBEAN; CLASSIFICATION; CORAL REEF; DINOFLAGELLATE; ENVIRONMENT; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; ANTHOZOA; ATLANTIC ISLANDS; BERMUDA; BIODIVERSITY; BIOTA; CARIBBEAN REGION; CORAL REEFS; DINOFLAGELLIDA; ENVIRONMENT; SYMBIOSIS;

EID: 85012077565     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0171768     Document Type: Article

References (71)

1. De'ath G, Fabricius KE, Sweatman H, Puotinen M. The 27-year decline of coral cover on the Great Barrier Reef and its causes. PNAS. 2012; 109(44): 17995-9. doi: 10.1073/pnas.1208909109 PMID: 23027961
2. Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR. Long-term region-wide declines in Caribbean corals. Science. 2003; 301(5635): 958-60. doi: 10.1126/science.1086050 PMID: 12869698
3. Jackson J, Donovan M, Cramer K, Lam V. Status and trends of Caribbean coral reefs: Global Coral Reef Monitoring Network. 2014: 1970-2012. Gland, Switzerland: Global Coral Reef Monitoring Network, IUCN; 2014.
4. Aronson RB, Precht WF. Landscape patterns of reef coral diversity: A test of the intermediate disturbance hypothesis. J Exp Mar Biol Ecol. 1995; 192(1): 1-14.
5. Goodbody-Gringley G, Woollacott RM, Giribet G. Population structure and connectivity in the Atlantic scleractinian coral Montastraea cavernosa (Linnaeus, 1767). Mar Ecol. 2012; 33(1): 32-48.
6. Serrano X, Baums IB, O'Reilly K, Smith T, Jones R, Shearer T, et al. Geographic differences in vertical connectivity in the Caribbean coral Montastraea cavernosa despite high levels of horizontal connectivity at shallow depths. Mol Ecol. 2014; 23(17): 4226-40. doi: 10.1111/mec.12861 PMID: 25039722
7. Nunes F, Norris RD, Knowlton N. Implications of isolation and low genetic diversity in peripheral populations of an amphi-Atlantic coral. Mol Ecol. 2009; 18(20): 4283-97. doi: 10.1111/j.1365-294X.2009. 04347.x PMID: 19765228
8. Goodbody-Gringley G, Vollmer SV, Woollacott RM, Giribet G. Limited gene flow in the brooding coral Favia fragum (Esper, 1797). Mar Biol. 2010; 157(12): 2591-602.
9. Serrano X, Baums IB, Smith TB, Jones RJ, Shearer TL, Baker AC. Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides. Sci Rep. 2016; 6.
10. Green DH, Edmunds PJ, Carpenter RC. Increasing relative abundance of Porites astreoides on Caribbean reefs mediated by an overall decline in coral cover. Mar Ecol Prog Ser. 2008; 359: 1-10.
11. Vermeij MJ, Bakker J, Hal Nvd, Bak RP. Juvenile coral abundance has decreased by more than 50% in only three decades on a small Caribbean island. Diversity. 2011; 3(3): 296-307.
12. Kenkel CD, Goodbody-Gringley G, Caillaud D, Davies SW, Bartels E, Matz MV. Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol. 2013; 22(16): 4335-48. doi: 10.1111/mec.12391 PMID: 23906315
13. Kenkel CD, Meyer E, Matz MV. Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments. Mol Ecol. 2013; 22(16): 4322-34. doi: 10.1111/mec.12390 PMID: 23899402
14. Bak R, Engel M. Distribution, abundance and survival of juvenile hermatypic corals (Scleractinia) and the importance of life history strategies in the parent coral community. Mar Biol. 1979; 54(4): 341-52.
15. Chornesky EA, Peters EC. Sexual reproduction and colony growth in the scleractinian coral Porites astreoides. Bio Bull. 1987; 172(2): 161-77.
16. Byler KA, Carmi-Veal M, Fine M, Goulet TL. Multiple symbiont acquisition strategies as an adaptive mechanism in the coral Stylophora pistillata. PloS One. 2013; 8(3): E59596. doi: 10.1371/journal.pone. 0059596 PMID: 23555721
17. Edmunds PJ. The effects of temperature on the growth of juvenile scleractinian corals. Mar Biol. 2008; 154(1): 153-62.
18. Edmunds PJ, Bruno JF, Carlon DB. Effects of depth and microhabitat on growth and survivorship of juvenile corals in the Florida Keys. Mar Ecol Prog Ser. 2004; 278: 115-24.
19. Edmunds PJ, Gates RD. Size-dependent differences in the photophysiology of the reef coral Porites astreoides. Bio Bull. 2004; 206(2): 61-4.
20. Kenkel CD, Setta SP, Matz MV. Heritable differences in fitness-related traits among populations of the mustard hill coral, Porites astreoides. Heredity. 2015; 115(6): 509-16. doi: 10.1038/hdy.2015.52 PMID: 26081798
21. Cantin NE, van Oppen MJ, Willis BL, Mieog JC, Negri AP. Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs. 2009; 28: 405-14.
22. Little AF, Oppen MJ, Willis BL. Flexibility in algal symbioses shapes growth in reef corals. Science. 2004; 304(5676): 1492-4. doi: 10.1126/science.1095733 PMID: 15178799
23. Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJH. The roles and interactions of symbiont, host and environment in defining coral fitness. PloS One. 2009; 4(7): E6364. doi: 10.1371/journal.pone.0006364 PMID: 19629182
24. Yamashita H, Suzuki G, Kai S, Hayashibara T, Koike K. Establishment of Coral-Algal Symbiosis Requires Attraction and Selection. PLoS One. 2014; 9(5): E97003. doi: 10.1371/journal.pone.0097003 PMID: 24824794
25. Abrego D, Van Oppen M, Willis BL. Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny. Mol Ecol. 2009; 18(16): 3532-43. doi: 10. 1111/j.1365-294X.2009.04276.x PMID: 19627494
26. Abrego D, Ulstrup KE, Willis BL, van Oppen MJ. Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc Lond [Biol]. 2008; 275(1648): 2273-82.
27. Stambler N. Zooxanthellae: The yellow symbionts inside animals. Coral Reefs: An ecosystem in transition. Dordrecht: Springer Netherlands; 2011. p. 87-106.
28. Pochon X, Gates RD. A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol Phylogenet Evol. 2010; 56(1): 492-7. doi: 10.1016/j.ympev.2010.03.040 PMID: 20371383
29. Abrego D, Willis BL, van Oppen MJ. Impact of light and temperature on the uptake of algal symbionts by coral juveniles. PloS One. 2012; 7(11): E50311. doi: 10.1371/journal.pone.0050311 PMID: 23185603
30. Baker AC. Reef corals bleach to survive change. Nature. 2001; 411(6839): 765-6. doi: 10.1038/35081151 PMID: 11459046
31. Berkelmans R, van Oppen MJH. 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 Lond [Biol]. 2006; 273(1599): 2305-12.
32. Cunning R, Baker AC. Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang. 2013; 3: 259-62.
33. Silverstein RN, Cunning R, Baker AC. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob Chang Biol. 2015; 21(1): 236-49. doi: 10. 1111/gcb.12706 PMID: 25099991
34. Stat M, Gates RD. Clade D Symbiodinium in scleractinian corals: A "nugget" of hope, a selfish opportunist, an ominous sign, or all of the above? J Mar Biol. 2010; 2011: 1-9.
35. Boulotte NM, Dalton SJ, Carroll AG, Harrison PL, Putnam HM, Peplow LM, et al. Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals. ISME J. 2016.
36. Yamashita H, Suzuki G, Hayashibara T, Koike K. Do corals select zooxanthellae by alternative discharge? Mar Biol. 2011; 158(1): 87-100.
37. Jones A, Berkelmans R. Potential costs of acclimatization to a warmer climate: Growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS One. 2010; 5(5): E10437. doi: 10.1371/journal. pone.0010437 PMID: 20454653
38. Stat M, Morris E, Gates RD. Functional diversity in coral-dinoflagellate symbiosis. PNAS. 2008; 105 (27): 9256-61. doi: 10.1073/pnas.0801328105 PMID: 18591663
39. Cunning R, Gillette P, Capo T, Galvez K, Baker A. Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans. Coral Reefs. 2015; 34 (1): 155-60.
40. Venn AA, Wilson MA, Rosenthal HG, Keely BJ, Douglas AE. The impact of coral bleaching on the pigment profile of the symbiotic alga, Symbiodinium. Plant Cell Environ. 2006; 29(12): 2133-42. doi: 10. 1111/j.1365-3040.2006.001587.x PMID: 17081247
41. Reynolds JM, Bruns BU, Fitt WK, Schmidt GW. Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. PNAS. 2008; 105(36): 13674-8. doi: 10.1073/pnas.0805187105 PMID: 18757737
42. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol. 2006; 148 (4): 711-22.
43. Coffroth MA, Santos SR, Goulet TL. Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Mar Ecol Prog Ser. 2001; 222: 85-96.
44. Marlow HQ, Martindale MQ. Embryonic development in two species of scleractinian coral embryos: Symbiodinium localization and mode of gastrulation. Evol Dev. 2007; 9(4): 355-67. doi: 10.1111/j.1525- 142X.2007.00173.x PMID: 17651360
45. Goodbody-Gringley G, Wetzel DL, Gillon D, Pulster E, Miller A, Ritchie KB. Toxicity of Deepwater Horizon source oil and the chemical dispersant, Corexit® 9500, to coral larvae. PloS One. 2013; 8(1): E45574. doi: 10.1371/journal.pone.0045574 PMID: 23326298
46. Johannes RE, Wiebe WJ. Method for determination of coral tissue biomass and composition. Limnol Oceanogr. 1970; 15(5): 822-4.
47. Goodbody-Gringley G. Diel planulation by the brooding coral Favia fragum (Esper, 1797). J Exp Mar Biol Ecol. 2010; 389(1): 70-4.
48. Pochon X, Pawlowski J, Zaninetti L, Rowan R. High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol. 2001; 139 (6): 1069-78.
49. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual. 3rd ed. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2001.
50. Altschul SF, Madden TL, Scha ffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSIBLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997; 25 (17): 3389-402. PMID: 9254694
51. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012; 28(12): 1647-9. doi: 10.1093/bioinformatics/bts199 PMID: 22543367
52. Arif C, Daniels C, Bayer T, Banguera-Hinestroza E, Barbrook A, Howe CJ, et al. Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region. Mol Ecol. 2014; 23(17): 4418-33. doi: 10.1111/mec.12869 PMID: 25052021
53. Zar JH. Biostatistical analysis 4th ed. Upper Saddle River, NJ: Prentice Hall; 1999.
54. Mitchell A, Bergmann PJ. Thermal and moisture habitat preferences do not maximize jumping performance in frogs. Funct Ecol. 2016; 30(5): 733-42.
55. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2014.
56. Banaszak AT, LaJeunesse TC, Trench RK. The synthesis of mycosporine-like amino acids (MAAs) by cultured, symbiotic dinoflagellates. J Exp Mar Biol Ecol. 2000; 249(2): 219-33. PMID: 10841936
57. Banaszak AT, Santos MGB, LaJeunesse TC, Lesser MP. The distribution of mycosporine-like amino acids (MAAs) and the phylogenetic identity of symbiotic dinoflagellates in cnidarian hosts from the Mexican Caribbean. J Exp Mar Biol Ecol. 2006; 337(2): 131-46.
58. Bongaerts P, Frade PR, Hay KB, Englebert N, Latijnhouwers KR, Bak RP, et al. Deep down on a Caribbean reef: Lower mesophotic depths harbor a specialized coral-endosymbiont community. Sci Rep. 2015; 5: 7652. doi: 10.1038/srep07652 PMID: 25564461
59. Goodbody-Gringley G, Marchini C, Chequer AD, Goffredo S. Population structure of Montastraea cavernosa on shallow versus mesophotic reefs in Bermuda. PLoS One. 2015; 10(11): E0142427. doi: 10.1371/journal.pone.0142427 PMID: 26544963
60. Siegel DA, Michaels AF, Sorensen JC, O'Brien MC, Hammer MA. Seasonal variability of light availability and utilization in the Sargasso Sea. J Geophys Res. 1995; 100(C5): 8695-713.
61. Bongaerts P, Carmichael M, Hay KB, Tonk L, Frade PR, Hoegh-Guldberg O. Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species. R Soc.Open Sci. 2015; 2 (2): 140297. doi: 10.1098/rsos.140297 PMID: 26064597
62. Warner ME, LaJeunesse TC, Robison JD, Thur RM. The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: Potential implications for coral bleaching. Limnol Oceanogr. 2006; 51(4): 1887-97.
63. Savage AM, Goodson MS, Visram S, Trapido-Rosenthal H, Wiedenmann J, Douglas AE. Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: Dinoflagellates of the genus Symbiodinium in corals and sea anemones. Mar Ecol Prog Ser. 2002; 244: 17-26.
64. Dodge RE, Logan A, Antonius A. Quantitative reef assessment studies in Bermuda: A comparison of methods and preliminary results. Bull Mar Sci. 1982; 32(3): 745-60.
65. Nitschke MR, Davy SK, Ward S. Horizontal transmission of Symbiodinium cells between adult and juvenile corals is aided by benthic sediment. Coral Reefs. 2016; 35(1)1-10.
66. Baker AC. Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst. 2003; 34: 661-89.
67. Mieog JC, van Oppen MJH, Cantin NE, Stam WT, Olsen JL. 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. 2007; 26(3): 449-57.
68. Holstein DM, Smith TB, Paris CB. Depth-independent reproduction in the reef coral Porites astreoides from shallow to mesophotic zones. PloS One. 2016; 11(1): E0146068. doi: 10.1371/journal.pone. 0146068 PMID: 26789408
69. Padilla-Gamiño JL, Pochon X, Bird C, Concepcion GT, Gates RD. From parent to gamete: Vertical transmission of Symbiodinium (Dinophyceae) ITS2 sequence assemblages in the reef building coral Montipora capitata. PloS One. 2012; 7(6): E38440. doi: 10.1371/journal.pone.0038440 PMID: 22701642
70. Kopp C, Domart-Coulon I, Barthelemy D, Meibom A. Nutritional input from dinoflagellate symbionts in reef-building corals is minimal during planula larval life stage. Sci Adv. 2016; 29(2): 255-75.
71. Lee MJ, Jeong HJ, Jang SH, Lee SY, Kang NS, Lee KH, et al. Most low-abundance "background" Symbiodinium spp. are transitory and have minimal functional significance for symbiotic corals. Microb Ecol. 2016; 71(3): 771-83. doi: 10.1007/s00248-015-0724-2 PMID: 26781946