Black reefs: Iron-induced phase shifts on coral reefs

ISME Journal

Volumn 6, Issue 3, 2012, Pages 638-649

  Kelly, Linda Wegley ^a   Barott, Katie L ^a   Dinsdale, Elizabeth ^a   Friedlander, Alan M ^b   Nosrat, Bahador ^a   Obura, David ^c   Sala, Enric ^d   Sandin, Stuart A ^e   Smith, Jennifer E ^e   Vermeij, Mark J A ^f,g   Williams, Gareth J ^e   Willner, Dana ^h   Rohwer, Forest ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c CORDIO East Africa ^*  (Kenya)

^d NATIONAL GEOGRAPHIC SOCIETY   (United States)

^e CENTER FOR MARINE BIODIVERSITY AND CONSERVATION   (United States)

^f CARMABI FOUNDATION   (Netherlands)

^g UNIVERSITY OF AMSTERDAM   (Netherlands)

^h UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

coral reef; iron; metagenomics; microbes; phase shift; shipwreck

Indexed keywords

IRON; SEA WATER; VIRULENCE FACTOR;

ALGA; ATMOSPHERIC DEPOSITION; BENTHOS; CALCIUM CARBONATE; CARBONATE PLATFORM; CLOUD WATER; CORAL REEF; CYANOBACTERIUM; GENOMICS; IRON; MACROALGA; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; PATHOGEN; PHASE TRANSITION; RUNOFF; SEDIMENTARY STRUCTURE; TURBIDITY; VIRULENCE; VIRUS; WATER COLUMN;

ANIMAL; ANTHOZOA; ARCHAEON; ARTICLE; BACTERIUM; CHEMISTRY; CORAL REEF; GENE LIBRARY; GENETICS; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; METAGENOMICS; PACIFIC OCEAN; RED ALGA; SEAWEED; SHIP;

ANIMALS; ANTHOZOA; ARCHAEA; BACTERIA; CORAL REEFS; GENOMIC LIBRARY; GEOGRAPHY; IRON; METAGENOMICS; PACIFIC OCEAN; RHODOPHYTA; SEAWATER; SEAWEED; SHIPS; VIRULENCE FACTORS;

LINE ISLANDS; PACIFIC OCEAN; PACIFIC OCEAN (CENTRAL);

ALGAE; ANTHOZOA; CYANOBACTERIA;

EID: 84857108684     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2011.114     Document Type: Article

References (41)

1. Abram NJ, Gagan MK, McCulloch MT, Chappell J, Hantoro WS. (2003). Coral reef death during the 1997 Indian Ocean dipole linked to Indonesian wildfires. Science 301: 952-955. (Pubitemid 36994804)
2. Abram NJ, Gagan MK, McCulloch MT, Chappell J, Hantoro WS. (2004). The sudden death of a coral reef-Response. Science 303: 1293-1294.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. (1990). Basic local alignment search tool. J Mol Biol 215: 403-410.
4. Amin SA, Green DH, Hart MC, Kupper FC, Sunda WG, Carrano CJ. (2009). Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism. Proc Natl Acad Sci USA 106: 17071-17076.
5. Anderson RM. (1998). Analytical theory of epidemics. In: Krause RM (ed). Emerging Infections. Academic Press: New York, NY, pp 23-50.
6. Barott KL, Caselle JE, Dinsdale EA, Friedlander AM, Maragos JE, Obura D et al. (2010). The lagoon at Caroline/Millennium Atoll, Republic of Kiribati: Natural history of a nearly pristine ecosystem. PLoS One 5: E10950.
7. Behrenfeld MJ, Westberry TK, Boss ES, O'Malley RT, Siegel DA, Wiggert JD et al. (2009). Satellite-detected fluorescence reveals global physiology of ocean phytoplankton. Biogeosciences 6: 779-794.
8. Bruland KW, Donat JR, Hutchins DA. (1991). Interactive influences of bioactive trace-metals on biological production in oceanic waters. Limnol Oceanogr 36: 1555-1577.
9. Charles C, Sandin S. (2009). Line Islands. In: Gillespie RG, Clague DA (eds). The Encyclopedia of Islands. University of California Press: Berkley, CA, pp 553-558.
10. Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y et al. (2005). VFDB: A reference database for bacterial virulence factors. Nucleic Acids Res 33 (Database issue): D325-D328. (Pubitemid 40207888)
11. Clarke KR, Somerfield PJ, Gorley RN. (2008). Testing of null hypotheses in exploratory community analyses: Similarity profiles and biota-environment linkage. J Exp Marine Biol Ecol 366: 56-69.
12. Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM et al. (2008a). Functional metagenomic profiling of nine biomes. Nature 452: 629-632; erratum in: Nature 2008; 455: 830. (Pubitemid 351483360)
13. Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, Wegley L et al. (2008b). Microbial ecology of four coral atolls in the northern Line Islands. PLoS One 3: E1584.
14. Done TJ. (1992). Phase-shifts in coral-reef communities and their ecological significance. Hydrobiologia 247: 121-132. (Pubitemid 24407391)
15. Entsch B, Sim RG, Hatcher BG. (1983). Indications from photosynthetic components that iron is a limiting nutrient in primary producers on coral reefs. Marine Biol 73: 17-30.
16. Gentleman R, Ihaka R. (1996). The R language. In: Billard L, Fisher NI (eds). Proceedings of 28th Symposium on the Interface of Computing Science and Statistics (Graph-Image-Vision). Sydney, NSW, Australia: Interface Found. North America, pp 326-330.
17. Granger J, Price NM. (1999). The importance of siderophores in iron nutrition of heterotrophic marine bacteria. Limnol Oceanogr 44: 541-555. (Pubitemid 29233648)
18. 2 availability. Mari Ecol Progress Series 409: 27-39.
19. Haas AF, Naumann MS, Struck U, Mayr C, el-Zibdah M, Wild C. (2010b). Organic matter release by coral reef associated benthic algae in the Northern Red Sea. J Exp Marine Biol Ecol 389: 53-60.
20. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ et al. (1999). Review: Marine ecology-emerging marine diseases-climate links and anthropogenic factors. Science 285: 1505-1510. (Pubitemid 29420569)
21. Hatcher BG. (1984). A maritime accident provides evidence for alternate stable states in benthic communities on coral reefs. Coral Reefs 3: 199-204.
22. Johnson KS, Gordon RM, Coale KH. (1997). What controls dissolved iron concentrations in the world ocean? Marine Chem 57: 137-161. (Pubitemid 27369724)
23. Knowlton N. (1992). Thresholds and multiple stable states in coral rref community dynamics. Am Zool 32: 674-682.
24. Knowlton N, Jackson JBC. (2008). Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol 6: 215-220.
25. Maragos JE, Williams GJ. (2011). Pacific coral reefs: An introduction. In: Hopley D (ed). Encyclopedia of Modern Coral Reefs. Springer: New York, NY, pp 753-776.
26. Martin JH, Coale KH, Johnson KS, Fitzwater SE, Gordon RM, Tanner SJ et al. (1994). Testing the iron hypothesis in ecosystems of the equatorial Pacific-Ocean. Nature 371: 123-129. (Pubitemid 24285060)
27. Martin JH, Fitzwater SE. (1988). Iron-deficiency limits phytoplankton growth in the northeast Pacific Subarctic. Nature 331: 341-343.
28. Meyer F, Paarmann D, D'Souza M, Olson R, Glass E, Kubal M et al. (2008). The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9: 386.
29. Norstrom AV, Nystrom M, Lokrantz J, Folke C. (2009). Alternative states on coral reefs: Beyond coral-macroalgal phase shifts. Mar Ecol Progress Series 376: 295-306.
30. Nystrom M, Graham NAJ, Lokrantz J, Norstrom AV. (2008). Capturing the cornerstones of coral reef resilience: Linking theory to practice. Coral Reefs 27: 795-809.
31. Obernosterer I, Christaki U, Lefevre D, Catala P, Van Wambeke F, Lebaron P. (2008). Rapid bacterial mineralization of organic carbon produced during a phytoplankton bloom induced by natural iron fertilization in the Southern Ocean. Deep Sea Research Part II 55: 777-789.
32. Rasher DB, Hay ME. (2010). Chemically rich seaweeds poison corals when not controlled by herbivores. Proc Natl Acad Sci USA 107: 9683-9688.
33. Rue EL, Bruland KW. (1995). Complexation of Iron(III) by natural organic-ligands in the central north Pacific as determined by a new competitive ligand equilibration adsorptive cathodic stripping voltammetric method. Marine Chem 50: 117-138. (Pubitemid 26463192)
34. Rue EL, Bruland KW. (1997). The role of organic complexation on ambient iron chemistry in the equatorial Pacific Ocean and the response of a mesoscale iron addition experiment. Limnol Oceanogr 42: 901-910. (Pubitemid 28278268)
35. Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM et al. (2008). Baselines and degradation of coral reefs in the northern Line Islands. PLoS One 3: E1548.
36. Schroeder RE, Green AL, DeMartini EE, Kenyon JC. (2008). Long-term effects of a ship-grounding on coral reef fish assemblages at Rose Atoll, American Samoa. Bull Marine Sci 82: 345-364. (Pubitemid 351986163)
37. Smith JE, Shaw M, Edwards RA, Obura D, Pantos O, Sala E et al. (2006). Indirect effects of algae on coral: Algae-mediated, microbe-induced coral mortality. Ecol Lett 9: 835-845. (Pubitemid 43883034)
38. Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F et al. (2009). Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11: 2148-2163.
39. Tortell PD, Maldonado MT, Granger J, Price NM. (1999). Marine bacteria and biogeochemical cycling of iron in the oceans. FEMS Microbiol Ecol 29: 1-11. (Pubitemid 29189167)
40. Vermeij MJA, Smith JE, Smith CM, Thurber RV, Sandin SA. (2009). Survival and settlement success of coral planulae: Independent and synergistic effects of macroalgae and microbes. Oecologia 159: 325-336.
41. Work TM, Aeby GS, Maragos JE. (2008). Phase shift from a coral to a corallimorph-dominated reef associated with a shipwreck on Palmyra Atoll. PLoS One 3: E2989.