Macroalgal Extracts Induce Bacterial Assemblage Shifts and Sublethal Tissue Stress in Caribbean Corals

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Morrow, Kathleen M ^a   Ritson Williams, Raphael ^b   Ross, Cliff ^c   Liles, Mark R ^a   Paul, Valerie J ^b  

^a AUBURN UNIVERSITY   (United States)

^b SMITHSONIAN MARINE STATION   (United States)

^c UNIVERSITY OF NORTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAL EXTRACT; CATALASE; GLUTATHIONE TRANSFERASE; RNA 16S; SUPEROXIDE DISMUTASE;

ACTINOBACTERIA; ALPHAPROTEOBACTERIA; AMPLICON; ARTICLE; CELL STRESS; CONTROLLED STUDY; CORAL; CORAL REEF; CYANOBACTERIUM; DENATURING GRADIENT GEL ELECTROPHORESIS; ENVIRONMENTAL IMPACT; ENZYME ASSAY; FIRMICUTES; GAMMAPROTEOBACTERIA; MACROALGA; MICROBIAL COMMUNITY; MUCUS; NONHUMAN; OXIDATIVE STRESS; POPULATION ABUNDANCE; SPECIES DIFFERENCE; UNITED STATES;

ANIMALS; ANTHOZOA; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; CARIBBEAN REGION; CATALASE; CORAL REEFS; SEAWEED; STRESS, PHYSIOLOGICAL; SUPEROXIDE DISMUTASE;

ALGAE; ANTHOZOA; BACTERIA (MICROORGANISMS); LOBOPHORA VARIEGATA; MONTASTRAEA FAVEOLATA; PORITES ASTREOIDES;

EID: 84866421156     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044859     Document Type: Article

References (73)

1. Kvennefors ECE, Sampayo E, Ridgway T, Barnes AC, Hoegh-Guldberg O, (2010) Bacterial communities of two ubiquitous Great Barrier Reef corals reveals both site- and species-specificity of common bacterial associates. PLoS ONE 5: e10401.
2. Rohwer F, Seguritan V, Azam F, Knowlton N, (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243: 1-10.
3. Sunagawa S, Woodley C, Medina M, (2010) Threatened corals provide underexplored microbial habitats. PLoS ONE 5: e9554.
4. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I, (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Micro 5: 355-362.
5. Sharp KH, Distel D, Paul VJ, (2012) Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME J 6: 790-801.
6. Ainsworth T, Hoegh-Guldberg O, (2009) Bacterial communities closely associated with coral tissues vary under experimental and natural reef conditions and thermal stress. Aquat Biol 4: 289-296.
7. Morrow KM, Moss AG, Chadwick NE, Liles MR (in press) Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl Enviro Microbiol.
8. Banin E, Israely T, Fine M, Loya Y, Rosenberg E, (2001) Role of endosymbiotic zooxanthellae and coral mucus in the adhesion of the coral-bleaching pathogen Vibrio shiloi to its host. FEMS Microbiol Lett 199: 33-37.
9. Ritchie K, (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322: 1-14.
10. Fong P, Paul VJ (2011) Coral Reef Algae. In: Dubinsky Z, Stambler N, editors. Coral Reefs: An Ecosystem in Transition. Dordrecht: Springer Netherlands. 241-272.
11. Chadwick NE, Morrow KM (2011) Competition Among Sessile Organisms on Coral Reefs. In: Dubinsky Z, Stambler N, editors. Coral Reefs: An Ecosystem in Transition. Dordrecht: Springer Netherlands. 341-371.
12. McCook L, Jompa J, Diaz-Pulido G, (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19: 400-417.
13. Birrell C, McCook L, Willis B, Harrington L, (2008) Chemical effects of macroalgae on larval settlement of the broadcast spawning coral Acropora millepora. Mar Ecol Prog Ser 362: 129-137.
14. Paul V, Kuffner I, Walters L, Ritson-Williams R, Beach K, et al. (2011) Chemically mediated interactions between macroalgae Dictyota spp. and multiple life-history stages of the coral Porites astreoides. Mar Ecol Prog Ser 426: 161-170.
15. Rasher DB, Hay ME, (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proc Natl Acad Sci USA 107: 9683-9688.
16. Rasher DB, Hay ME, (2010) Seaweed allelopathy degrades the resilience and function of coral reefs. Commun Integr Biol 3: 564-566.
17. Rasher DB, Stout EP, Engel S, Kubanek J, Hay ME, (2011) Macroalgal terpenes function as allelopathic agents against reef corals. Proc Natl Acad Sci USA 108: 17726-17731.
18. Downs CA, Fauth JE, Robinson CE, Curry R, Lanzendorf B, et al. (2005) Cellular diagnostics and coral health: declining coral health in the Florida Keys. Mar Poll Bull 51: 558-569.
19. Downs CA, Ostrander GK, Rougee L, Rongo T, Knutson S, et al. (2012) The use of cellular diagnostics for identifying sub-lethal stress in reef corals. Ecotoxicol 21: 768-782.
20. Morgan MB, Vogelien DL, Snell TW, (2001) Assessing coral stress responses using molecular biomarkers of gene transcription. Environ Toxicol Chem 20: 537-543.
21. Downs CAC, Richmond RHR, Mendiola WJW, Rougée LL, Ostrander GKG, (2006) Cellular physiological effects of the MV Kyowa violet fuel-oil spill on the hard coral, Porites lobata. Environ Toxicol Chem 25: 3171-3180.
22. Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, et al. (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 33: 533-543.
23. Haas AF, Naumann MS, Struck U, Mayr C, el-Zibdah M, et al. (2010) Organic matter release by coral reef associated benthic algae in the Northern Red Sea. J Exper Mar Biol Ecol 389: 53-60.
24. Dinsdale EA, Rohwer F, (2008) Dissecting microbial employment. Nat Biotechnol 26: 997-998.
25. Steinberg P, deNys R, Kjelleberg S, (2002) Mini Review: Chemical cues for surface colonization. J Chem Ecol 28: 1935-1950.
26. Lane A, Kubanek J (2008) Secondary metabolite defenses against pathogens and biofoulers. In: Amsler CD, editor. Algal chemical ecology. Springer-Verlag Berlin Heidelberg 229-243.
27. Smith J, Shaw M, Edwards RA, Obura D, Pantos O, et al. (2006) Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecol Lett 9: 835-845.
28. Barott K, Smith J, Dinsdale E, Hatay M, Sandin S, et al. (2009) Hyperspectral and physiological analyses of coral-algal interactions. PLoS ONE 4: e8043.
29. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, et al. (1999) Emerging marine diseases-climate links and anthropogenic factors. Science 285: 1505-1510.
30. Barott KL, Rodriguez-Brito B, Janouškovec J, Marhaver KL, Smith JE, et al. (2011) Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ Microbiol 13: 1192-1204.
31. Engel S, Jensen P, Fenical W, (2002) Mini Review: Chemical ecology of marine microbial defense. J Chem Ecol 28: 1971-1985.
32. Puglisi M, Tong Tan L, Jensen P, Fenical W, (2004) Capisterones A and B from the tropical green alga Penicillus capitatus: unexpected anti-fungal defenses targeting the marine pathogen Lindra thallasiae. Tetrahedron 60: 7035-7039.
33. Paul VJ, Puglisi MP, Ritson-Williams R, (2006) Marine chemical ecology. Nat Prod Rep 23: 153-180.
34. Jiang R-W, Lane AL, Mylacraine L, Hardcastle KI, Fairchild CR, et al. (2008) Structures and absolute configurations of sulfate-conjugated triterpenoids including an antifungal chemical defense of the green macroalga Tydemania expeditionis. J Nat Prod 71: 1616-1619.
35. Engel S, Puglisi MP, Jensen PR, Fenical W, (2006) Antimicrobial activities of extracts from tropical Atlantic marine plants against marine pathogens and saprophytes. Mar Biol 149: 991-1002.
36. Maximilien R, De Nys R, Holmström C, Gram L, Givskov M, et al. (1998) Chemical mediation of bacterial surface colonisation by secondary metabolites from the red alga Delisea pulchra. Aquat Microb Biol 15: 233-246.
37. Rasmussen TB, Manefield M, Andersen JB, Eberl L, Anthoni U, et al. (2000) How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology+ 146: 3237-3244.
38. Lane A, Nyadong L, Galhena A, Shearer T, Stout E, et al. (2009) Desorption electrospray ionization mass spectrometry reveals surface-mediated antifungal chemical defense of a tropical seaweed. Proc Natl Acad Sci USA 106(18): 7314-7319.
39. Nylund G, Cervin G, Persson F, Hermansson M, Steinberg P, et al. (2008) Seaweed defence against bacteria: a poly-brominated 2-heptanone from the red alga Bonnemaisonia hamifera inhibits bacterial colonisation. Mar Ecol Prog Ser 369: 39-50.
40. Morrow KM, Paul VJ, Liles MR, Chadwick NE, (2011) Allelochemicals produced by Caribbean macroalgae and cyanobacteria have species-specific effects on reef coral microorganisms. Coral Reefs 30: 309-320.
41. Goecke F, Labes A, Wiese J, Imhoff J, (2010) Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409: 267-299.
42. Paul V, Van Alstyne K, (1992) Activation of chemical defenses in the tropicalgreen-algae Halimeda spp. J Exper Mar Biol Ecol 160: 191-203.
43. Puglisi MP, Engel S, Jensen PR, Fenical W, (2007) Antimicrobial activities of extracts from Indo-Pacific marine plants against marine pathogens and saprophytes. Mar Biol 150: 531-540.
44. Pawlik JR, Steindler L, Henkel TP, Beer S, Ilan M, (2007) Chemical warfare on coral reefs: Sponge metabolites differentially affect coral symbiosis in situ. Limnol Oceanogr 52: 907-911.
45. Wu G, Wilen RW, Robertson AJ, Gusta LV, (1999) Isolation, chromosomal localization, and differential expression of mitochondrial manganese superoxide dismutase and chloroplastic copper/zinc superoxide dismutase genes in wheat. Plant Physiol 120: 513-520.
46. Halliwell B, (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141: 312-322.
47. Rougée LL, Downs CAC, Richmond RHR, Ostrander GKG, (2006) Alteration of normal cellular profiles in the Scleractinian coral (Pocillopora damicornis) following laboratory exposure to fuel oil. Environ Toxicol Chem 25: 3181-3187.
48. Leaver MJ, George SG, (1998) A piscine glutathione S-transferase which efficiently conjugates the end-products of lipid peroxidation. Mar Enviro Res 46: 71-74.
49. Ihaka R, Gentleman R, (1996) R: A Language for Data Analysis and Graphics. J Comput Graph Stat 5: 299-314.
50. Muyzer G, de Waal EC, Uitterlinden AG, (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700.
51. Ferris MJ, Muyzer G, Ward DM, (1996) Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Appl Environ Microbiol 62: 340-346.
52. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ, (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71: 7724-7736.
53. Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, et al. (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4: e1000255.
54. Millar B, Xu J, (2002) Risk assessment models and contamination management: implications for broad-range ribosomal DNA PCR as a diagnostic tool in medical bacteriology. J Clin Microbiol 40: 1575-1580.
55. McCune B, Grace J (2002) Nonmetric multidimensional scaling. In: McCune B, Grace J, editors. Analysis of Ecological Communities. IMjM Software Design, Gleneden Beach, Oregon. 125-142.
56. Puglisi MP, Engel S, Jensen PR, Fenical W, (2007) Antimicrobial activities of extracts from Indo-Pacific marine plants against marine pathogens and saprophytes. Mar Biol 150: 531-540.
57. Vairappan CS, Anangdan SP, Tan KL, Matsunaga S, (2009) Role of secondary metabolites as defense chemicals against ice-ice disease bacteria in biofouler at carrageenophyte farms. J Appl Phycol 22: 305-311.
58. Garzón-Ferreira J, Gil-Agudelo D, Barrios L, (2001) Stony coral diseases observed in southwestern Caribbean reefs. Hydrobiol 460: 65-69.
59. Lafferty K, Porter J, Ford S, (2004) Are diseases increasing in the ocean? Annu Rev Ecol Evol Syst 35: 31-54.
60. Edmunds P, (2002) Long-term dynamics of coral reefs in St. John, US Virgin Islands. Coral Reefs 21: 357-367.
61. Cronin G, Hay ME, (1996) Within-plant variation in seaweed palatability and chemical defenses: optimal defense theory versus the growth-differentiation balance hypothesis. Oecologia 105: 361-368.
62. Schmitt T, Hay M, Lindquist N, (1995) Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology 76: 107-123.
63. Littler D, Littler M (2003) South Pacific reef plants: a divers' guide to the plant life of the South Pacific coral reefs. Washington, D.C.: Offshore Graphics Inc. 172-173.
64. Nugues MM, Bak RPM, (2006) Differential competitive abilities between Caribbean coral species and a brown alga: a year of experiments and a long-term perspective. Mar Ecol Prog Ser 315: 75-86.
65. Nugues MM, Bak RPM, (2008) Long-term dynamics of the brown macroalga Lobophora variegata on deep reefs in Curacao. Coral Reefs 27: 389-393.
66. Jompa J, McCook L, (2002) Effects of competition and herbivory on interactions between a hard coral and a brown alga. J Exper Mar Biol Ecol 271: 25-39.
67. Jompa J, McCook L, (2002) The effects of nutrients and herbivory on competition between a hard coral (Porites cylindrica) and a brown alga (Lobophora variegata). Limnol Oceanogr 47: 527-534.
68. Dobretsov S, Teplitski M, Bayer M, Gunasekera S, Proksch P, et al. (2011) Inhibition of marine biofouling by bacterial quorum sensing inhibitors. Biofouling 27: 893-905.
69. Targett N, Arnold T, (1998) Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J Phycol 34: 195-205.
70. Amsler CD, Fairhead VA, (2005) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43: 1-91.
71. Kubanek J, Jensen P, Keifer P, Sullards M, Collins D, et al. (2003) Seaweed resistance to microbial attack: a targeted chemical defense against marine fungi. Proc Natl Acad Sci USA 100: 6916.
72. Norström A, Nyström M, Lokrantz J, Folke C, (2009) Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Mar Ecol Prog Ser 376: 295-306.
73. McManus JW, Polsenberg JF, (2004) Coral-algal phase shifts on coral reefs: Ecological and environmental aspects. Prog Oceanogr 60: 263-279.