Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates

Ecology and Evolution

Volumn 3, Issue 8, 2013, Pages 2393-2400

  Ceh, Janja ^a,b   Kilburn, Matt R ^c   Cliff, John B ^c   Raina, Jean Baptiste ^b,d   Van Keulen, Mike ^a   Bourne, David G ^b  

^a MURDOCH UNIVERSITY   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d JAMES COOK UNIVERSITY   (Australia)

Author keywords

Bacteria; Coral larvae; NanoSIMS; Nitrogen

Indexed keywords

ALGAE; ALTEROMONAS; ALTEROMONAS SP.; ANIMALIA; ANTHOZOA; BACTERIA (MICROORGANISMS); POCILLOPORA DAMICORNIS; SYMBIODINIUM; VIBRIO; VIBRIO ALGINOLYTICUS;

EID: 84887983366     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.642     Document Type: Article

References (29)

1. Altschul, S. F., T. L. Madden, A. A. Schaeffer, J. Zhang, Z. Zhang, and W. Miller. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Apprill, A., H. Q. Marlow, M. Q. Martindale, and M. S. Rappe. 2009. The onset of microbial associations in the coral Pocillopora meandrina. ISME J. 3:685-699.
3. Beman, J. M., K. J. Roberts, L. Wegley, F. Rowher, and C. A. Francis. 2007. Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Appl. Environ. Microbiol. 73:5642-5647.
4. Ceh, J., M. van Keulen, and D. G. Bourne. 2013. Intergenerational transfer of specific bacteria in corals and possible implications for offspring fitness. Microb. Ecol. 65:227-231.
5. Ducklow, H. W., and R. Mitchell. 1979. Bacterial populations and adaptations in the mucus layers of living corals. Limnol. Oceanogr. 24:715-725.
6. Fiore, C. L., J. K. Jarett, N. D. Olson, and M. P. Lesser. 2010. Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol. 18:455-463.
7. Foster, R. A., M. M. M. Kuypers, Vagner T., R.W. Paerl, N. Musat, and J. P. Zehr. 2011. Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses. ISME J. 5:1484-1493.
8. Guerinot, M. L., and D. G. Patriquin. 1981. The association of N2-fixing bacteria with sea urchins. Mar. Biol. 62:197-207.
9. Kimes, N. E., J. D. Van Nostrand, E. Weil, J. Zhou, and P. J. Morris. 2010. Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies. Environ. Microbiol. 12:541-556.
10. Kneip, C., P. Lockhart, C. Voß, and U. G. Maier. 2007. Nitrogen fixation in eukaryotes - new models for symbiosis. BMC Evol. Biol. 7:55.
11. Lechene, C. P., Y. Luyten, G. McMahon, and D. L. Distel. 2007. Quantitative imaging of nitrogen fixation by individual bacteria within animal cells. Science 317:1510-1511.
12. Lesser, M. P., C. H. Mazel, M. Y. Gorbunov, and P. G. Falkowski. 2004. Discovery of symbiotic nitrogenfixing cyanobacteria in corals. Science 305:997-1000.
13. Lesser, M. P., L. I. Falcon, A. Rodriguez-Roman, O. Hoegh-Guldberg, and R. Iglesias-Prieto. 2007. Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar. Ecol. Prog. Ser. 346:143-152.
14. Marchesi, J. R., T. Sato, A. J. Weightman, T. A. Martin, and W. G. Wade. 1998. Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl. Environ. Microbiol. 64:795-799.
15. Meikle, P., G. N. Richards, and D. Yellowlees. 1988. Structural investigations on the mucus from six species of coral. Mar. Biol. 99:187-193.
16. Mohamed, N. M., K. Saito, Y. Tal, and R. T. Hill. 2010. Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J. 4:38-48.
17. Olson, N. D., T. D. Ainsworth, R. D. Gates, and M. Takabayashi. 2009. Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates. J. Exp. Mar. Biol. Ecol. 371:140-146.
18. Pernice, M., A. Meibom, A. Van Den Heuvel, C. Kopp, I. Domarrt-Coulon, O. Hoegh-Guldberg, et al. 2012. A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. ISME J. 6:1314-1324.
19. Rohwer, F., V. Segritan, F. Azam, and N. Knowlton. 2002. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243:1-10.
20. Rosenberg, E., O. Koren, L. Reshef, R. Efrony, and I. Zilber-Rosenberg. 2007. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5:355-362.
21. Ryan, P. D., D. A. T. Harper, and J. S. Whalley. 1995. Palstat:user's manual and case histories: statistics for palaeontologists and palaeobiologists. Springer, Berlin.
22. Sharp, K. H., K. B. Ritchie, P. J. Schupp, R. Ritson-Williams, and V. J. Paul. 2010. Bacterial acquisition in juveniles of several broadcast spawning coral species. PLoS One 5:e10898.
23. Sharp, K. H., D. L. Distel, and V. J. Paul. 2011. Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME J. 4:790-801.
24. Sheppard, C. R. C., S. K. Davy, and G. M. Pilling. 2009. The biology of coral reefs. Oxford Univ. Press, New York, NY.
25. Sjoblad, R. D., and R. Mitchell. 1979. Chemotactic responses of Vibrio alginolyticus to algal extracellular products. Can. J. Microbiol. 25:964-967.
26. Taylor, M. W., R. Radax, S. Steger, and M. Wagner. 2007. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71:295-347.
27. Thompson, F. L., B. Gomez-Gil, A. T. Ribeiro Vasconcelos, and T. Sawabe. 2007. Multilocus sequence analysis reveals that vibrio harveyi and V. campbellii are distinct species. Appl. Environ. Microbiol. 73:4279-4285.
28. Wegley, L., M. Breitbart, R. A. Edwards, and F. Rohwer. 2007. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ. Microbiol. 9:2707-2719.
29. Yellowlees, D., T. A. W. Rees, and W. Leggat. 2008. Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell Environ. 31:679-694.