Volume 6, Issue 6, December 2017, Page: 98-109
Response of the Coral Associated Nitrogen Fixing Bacteria Toward Elevated Water Temperature
Leomir Diaz, Institute of Biology, University of the Philippines, Diliman Quezon City, Philippines
Received: Oct. 9, 2017;       Accepted: Nov. 3, 2017;       Published: Nov. 29, 2017
DOI: 10.11648/j.wros.20170606.14      View  1489      Downloads  55
Abstract
Coral reefs are among the most biologically diverse and economically important ecosystem on the planet. Despite the importance, reef habitat is being under threat from human exploitation, and its most serious stressor is increasing seawater temperature, an aftermath of global warming phenomenon. The increasing seawater temperature causes bleaching, diseases and insufficiency of nutrients of corals. Despite being surrounded by ocean waters were nutrient are in short supply, the reef ecosystem is a significant source of new nitrogen. Biological nitrogen fixation is a significant internal source of marine organism. The growth of all organism lies on the availability of mineral nutrients particularly of nitrogen (N2). Approximately 80% of atmosphere is made of nitrogen, however, N2 can only be available for use by organism unless it undergoes a process of nitrogen fixation. In this aspect, related literature on biological nitrogen fixation seems sparse especially on the effects of increasing seawater temperature, a well-known contributing factor of coral bleaching. In this study, an investigation was conducted on nitrogen fixing bacterial communities associated in the coral Acropora digitifera, exploring its responses towards elevated water temperature. The study shows that exposure to high temperature causes a drastic change in the community of nitrogen fixing bacteria which are abundant in coral mucus. These changes, is correlated with the shift in the metabolic function in coral holobiont, thus, affecting both health and resiliency of corals. Overall, the finding highlights the impact of elevated seawater temperature on the nitrogen fixing bacterial composition and its diversity as well as its effects of this on host metabolism.
Keywords
Nitrogen Fixing Bacteria, Coral Mucus, Elevated Water Temperature, Coral Health
To cite this article
Leomir Diaz, Response of the Coral Associated Nitrogen Fixing Bacteria Toward Elevated Water Temperature, Journal of Water Resources and Ocean Science. Vol. 6, No. 6, 2017, pp. 98-109. doi: 10.11648/j.wros.20170606.14
Copyright
Copyright © 2017 Authors retain the copyright of this article.
This article is an open access article distributed under the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Reference
[1]
Abed R, Al-Thukair A, Beer D. "Bacterial Diversity of Cyanobacterial mat degrading petroleum compounds at elevated salinities and temperatures". FEMS; Microbiol. Ecol. 2006. vol. 57: 290-301.
[2]
Auman AJ, Speake CC, “Lidstrom ME. nifH sequences and nitrogen fixation in type I and type II methanotrophs,” Appl. Environ. Microbiol, 2001. vol 67:4009–4016.
[3]
Barott, K. L., and F. L. Rohwer. "Unseen players shape benthic competition on coral reefs". Trends Microbio 2012. vol 20:621–628.
[4]
Bauer K, Díez B, Lugomela C, Seppala S, Borg A. J, and Bergman B. “Variability in benthic diazotrophy and cyanobacterial diversity in a tropical intertidal lagoon,” FEMS Microbiol Ecol, 2008. vol 63:2, 205–221.
[5]
Benson A, Muscatine L, "Wax in coral mucus—energy transfer from corals to reef fishes". Limnol Oceanogr, 1974, vol 19: 810–814.
[6]
Canfield D, Glazer N, Falkowski P. "The evolution and future of earth's nitrogen cycle". Science 2010, vol 330:192-196.
[7]
Capone, D. G., and E. J. Carpenter. "Nitrogen fixation in the marine environment". Science 1982: vol 217:1140–1142.
[8]
Charpy L, Alliod R, Rodier M, and Golubic S, "Benthic nitrogen fixation in the SW New Caledonia lagoon, Aqua. Micro. Ecol," 2007, 47:1, 73–81.
[9]
Charpy L, Palinska KA, Casareto B et al., “Dinitrogen-fixing cyanobacteria in microbial mats of two shallow coral reef ecosystems,” Microbial Ecol 2010. vol 59:1, 174–186.
[10]
Chimetto LA, Brocchi M, Thompson CC, Martins RCR, Ramos HR and Thompson FL. "Vibrios dominate as culturable nitrogen-fixing bacteria of the Brazilian coral Mussismilia hispida." Syst Appl Microbiol 2008. vol 31: 312-319.
[11]
Chimetto LA, Brocchi M, Gondo M, Thompson CC, Gomez-Gil B, Thompson FL,. "Genomic diversity of vibrios associated with the Brazilian coral Mussismilia hispida and its sympatric zoanthids (Palythoa caribaeorum, Palythoa variabilis and Zoanthus solanderi)". J Appl Microbiol 2009. vol 106; 1818–1826.
[12]
Coffroth MA. Mucous sheet formation on poritid corals—an evaluation of coral mucus as a nutrient source on reefs. Mar Biol 1990. vol 105:39–49.
[13]
Coles S, Strathman R. Observations on coral mucus flocs and their potential trophic significance. Limnol Oceanogr 1973. vol 18:673–678.
[14]
Davey M, Holmes J, and Johnstone R. "High rates of nitrogen fixation (acetylene reduction) on coral skeleton following bleaching mortality". Coral reefs 2008. vol 27: 227-236. DOI10.1007/s00338-007-0316-9
[15]
Dedysh, S. N., Ricke, P., Liesack, W. "NifH and NifD phylogenies: an evolutionary basis for understanding nitrogen fixation capabilities of methanotrophic bacteria". Microbiology 2004. vol 150: 1301-1313.
[16]
Dekas A, Poretsky R, Orphan V. "Deep sea archae fix and share nitrogen in methyle consuming microbial consortia". Science 2009, vol 326: 422-426.
[17]
Diez B, Alio CP, Marsh T, and Massanai R. "Application of Denaturing Gradient Gel Electrophoresis (DGGE) To study the diversity of marine picoeukaryotic assembleges and comparison of DGGE with other molecular techniques". Appl. Environ. Microbiol 2001. 67(7): 2942-295.
[18]
Distel D., Morrill, W. MacLaren-Toussaint, N., Franks, D., Waterbury, J. "Teredinibacter turnerae gen. nov., sp. nov., a dinitrogen-fixing, cellulolytic, endosymbiotic gammaproteobacterium isolated from the gills of wood-bring molluscs". International Journal of Systematic and Evolutionary Microbiology 2002. vol 52: 2261-2269.
[19]
Dobretsov, S., and P.-Y. Qien. "The role of epibiotic bacteria from the surface of the soft coral Dendronephthya sp. in the inhibition of larval settlement". J. Exp. Mar. Biol. Ecol. 2004. vol 299:35–50.
[20]
Ferguson R. L., Buckley E. N. and Palumbo A. V. "Response of marine bacterioplankton to differential filtration and confinement". Appl. Environ. Microbiol 1984. vol 47, 49–55.
[21]
Fitt, WK et al., "Response of two species of Indo pacific corals, Porites cylindrica and Stylophora pistillata to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching". J Exp. Mar Biol. Ecol. 2009. vol 373; 102-110.
[22]
Fred EB, Baldwin IL, McCoy E. Root nodule bacteria and leguminous plants, vol 5. Parallel Press, Madison, WI. 1992.
[23]
Frieler, K., M. Meinshausen, A. Golly, M. Mengel, K. Lebek, S. D. Donner, et al. "Limiting global warming to 2 degrees C is unlikely to save most coral reefs". Nat. Clim. Change 2013. vol. 3:165–170.
[24]
Garrard, S., R. Hunter, A. Frommel, A. Lane, J. Phillips, R. Cooper, et al. "Biological impacts of ocean acidification: a postgraduate perspective on research priorities". Mar. Biol. 2012. vol 160:1789–1805.
[25]
Gruber N. The Dynamic of marine nitrogen cycle and atmospheric CO2. T. Oguz and M. Follows, eds. Carbon Climate Interactions, Kluwer, Dordretch 2004. pp 97-148.
[26]
Hagstrom A, Larsson U, Horstedt P, and Normark S. "Frequency of dividing cells. a new approach to the determination of bacterial growth rates in aquatic environments". Appl. Environ. Microbiol. 1979. vol 37:805-812.
[27]
Harnik, P. G., H. K. Lotze, S. C. Anderson, Z. V. Finkel, S. Finnegan, D. R. Lindberg, et al. "Extinctions in ancient and modern seas". Trends Ecol. Evol. 2012. vol 27:608–617.
[28]
Hennecke H, et al. "Concurrent evolution of nitrogenase genes and 16S rRNA in Rhizobium species and other nitrogen fixing bacteria". Arch. Microbiol. 1985. vol 142:342–348.
[29]
Horn M, Wagner M. "Bacterial endosymbionts of free-living amoebae". J Eukaryot Microbiol. 2004. vol 51:509–514.
[30]
Hoegh-Guldberg, O., P. Mumby, A. Hooten, R. Steneck, P. Greenfield, E. Gomez, et al. "Coral reefs under rapid climate change and ocean acidification". Science 2007. vol 318:1737–1742.
[31]
Hoegh-Guldberg, O. "Coral reef ecosystems and anthropogenic climate change". Reg. Environ. Change. 2011. vol 11:215–227.
[32]
Holants J, Leroux O. Leliaert F, Decleyre H. De Cleck Oliver, Willems A. "Who is there? Exploration of Endophytic bacteria within the Siphonous Green seaweed Bryopsis (Bryopsidales, Chlorophyta)". Plos One 2011. 6(10); e26458.
[33]
Huber JA, Welch DBM, Morrison GH, Huse SM, Neal PR, Butterfield DA, Sogin ML. "Microbial population structures in the deep marine biosphere". Science 2007. vol. 318:98-100.
[34]
Hughes, T. P., Graham. NaJ, J. B. C. Jackson, P. J. Mumby, and R. S. Steneck. "Rising to the challenge of sustaining coral reef resilience". Trends Ecol. Evol. 2010. vol 25:633–642.
[35]
Karl D, A. Michaels B, Bergmam D, et al. "Dinitrogen Fixation in the world's Ocean". Biogeochemistry 2002. vol 57:47-98.
[36]
Kellogg CA, Lisle JT, and Galkiewicz JP. "Culture independent characterization of bacterial communities associated with the cold water coral Lophelia pertusa in the northeastern Gulf of Mexico". Appl. Environ. Microbiol. 2009. vol 75; 2294-2303.
[37]
Kimes NE, Van Nostrand JD, Weil E, Zhou J, Morris PJ. "Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies". Environ Microbiol 2010. vol 12: 541–556.
[38]
Kikuchi Y. "Endosymbiotic bacteria in insects: Their diversity and culturability". Microbes Environ. 2009. vol 24:195–204.
[39]
Kleypas, J. A., and K. K. Yates. "Coral reefs and ocean acidification". Oceanography 2009. vol 22:108–117.
[40]
Kneip C, Lockhart P, Vosz C, and Maeir G. "Nitrogen fixation in eukaryotes- new models for symbiosis". BMC Evol. Biol. 2007, pp 7:55.
[41]
Koren O, Rosenberg E. "Bacteria associated with mucus and tissue of the coral Oculina patagonica in summer and winter". Appl. Environ. Microbiol 2006. vol 72(8):5254-5259.
[42]
Krediet, C. J., K. B. Ritchie, V. J. Paul, and M. Teplitski. "Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases". Proc. Biol. Sci. 2013, 280:20122328.
[43]
Lia CRS, Teixeira RS, Peixoto JC, Cury W, Jun S, Vivian H, Pellizari JT, Alexandre SR: "Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica" ISME J 2010, vol 4: 989-1001.
[44]
Lesser MP, Mazel CH, Gorbunav MY, Falkowski PG. "Discovery of symbiotic nitrogen fixing cyanobacteria in corals". Science, 2004, vol 305; 997-1000
[45]
Lema, K. A., B. L. Willis, and D. G. Bourne. "Amplicon pyrosequencing reveals spatial and temporal consistency in diazotroph assemblages of the Acropora millepora microbiome". Environ. Microbiol 2014. Early View. doi:10.1111/ 1462-2920.12366.
[46]
Lema AK, Willis BL, Bourne DG. "Corals form characteristic associations with symbiotic nitrogen fixing bacteria". Appl. Environ. Microbiol 2012. vol 78(9); 3136-3144
[47]
Ladner JT, Palumbi SR, "Extensive sympatry, cryptic diversity and introgression throughout the geographic distribution of two coral species complexes". Mol. Ecol 2012. Vol 21, pp 2224–2238.
[48]
Larkum, A. W. D. "High rates of nitrogen fixation on coral skeletons after predation by the crown of thorns starfish Acanthaster planci". Mar. Biol 1988. vol 97: pp 503–506.
[49]
Larkum, A. W. D., I. R. Kennedy, and W. J. Muller. "Nitrogen fixation on a coral reef". Mar. Biol 1988. Vol 98: pp 143–155.
[50]
López-Bueno A, Tamames J, Velázquez D, Moya A, Quesada A, Alcamí. A. "High diversity of the viral community from an Antarctic Lake". Science 2009, 326:858-861.
[51]
Lodwig EM, et al. "Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis". Nature 2003. vol 422: 722–726.
[52]
Malik KA, and Claus D. "Xanthobacter flavus, a new species of nitrogen fixing hydrogen bacteria". Int. J Systm Bacteriol 1979. vol 29(4); 283-287.
[53]
Margulies M, Egholm M, Altman WE, et al: "Genome sequencing in microfabricated high- density picolitre reactors". Nature 2005, 437:376-380.
[54]
Martensson L, Diez B, Wartiainen I, Zheng W et al., "Diazotrophic diversity, nifH gene expression and nitrogenase activity in a rice paddy field in Fujian China". Springer, Plant Soi 2009l. DOI 10.1007/s11104-009-9970-8
[55]
Marsden J, Meeuwig J. “Preferences of planktotrophic larvae of the tropical serpulid Spirobranchus giganteus (Pallas) for exudates of corals from a Barbados reef”. J Exp Mar Biol Ecol 1990. vol 137:97–104.
[56]
Martensson L, Diez B, Wartiainen I, Zheng W et al., (2009). Diazotrophic diversity, nifH gene expression and nitrogenase activity in a rice paddy field in Fujian China. Springer, Plant Soil. DOI 10.1007/s11104-009-9970-8
[57]
Mehta M, Butterfield D, Baross J, "Phylogenetic diversity of nitrogenase (nifH) genes in deep sea and hydrothermal vent environment of the juan de fuca ridge". Appl. Environ. Microbiol. 2003, pp 69: 960-970.
[58]
Meron, D., E. Atias, L. I. Kruh, H. Elifantz, D. Minz, M. Fine, et al. "The impact of reduced pH on the microbial community of the coral Acropora eurystoma". ISME J 2011. Vol 5:51–60.
[59]
Middlebrook R, Hoegh-Guldberg O, Leggat W. "The effect of thermal history on the susceptibility of reef building corals to thermal stress". J Exp Biol 2008. Vo l 211:1050-1056.
[60]
Muyzer G and Smalla K. "Application of denaturing gradient gel eletrophoresis (DGGE) and temperature gradient gel eletrophoresis (TGGE) in microbial ecology". Acad. Pub. 1998. vol 73: 127-141.
[61]
Olson ND, Ainsworth TD, Gates RD, Takabayashi M. "Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates". J Exp Mar Biol Ecol 2009. Vol 371: 140–146.
[62]
O’Neil, J. M., and D. G. Capone. "Nitrogen cycling in coral reef environments". pp. 949–989 in D. G. Capone, D. A. Bronk, M. R. Mulholland and E. J. Carpenter, eds. Nitrogen in the marine environment, 2nd ed. Academic Press, San Diego. 2008.
[63]
Patton W. "Distribution and ecology of animals associ- ated with branching corals (Acropora spec.) from the Great Barrier Reef, Australia". Bull Mar Sci 1994. vol 55:193–211
[64]
Pandolfi, J. M., S. R. Connolly, D. J. Marshall, and A. L. Cohen. "Projecting coral reef futures under global warming and ocean acidification". Science 2011. vol 333:418–422.
[65]
Radecker N, Pogoreutz C, Voolstra C, Wiedenmann J, and Wild C. "Nitrogen cycling in corals: the key to understanding holobiont functioning". Trends in Microbiology August 2015, Vol. 23, No. 8.
[66]
Raeid M. M Abed., Golubic S, Garcia-Pichel F, Camoin G. F, and Sprachta S. “Characterization of microbialite-forming cyanobacteria in a tropical lagoon: Tikehau Atoll, Tuamotu, French Polynesia,” J of Phyco 2003, vol 39:5, 862–873.
[67]
Rees, A. P. "Pressures on the marine environment and the changing climate of ocean biogeochemistry. Philos. Trans". A Math. Phys. Eng. Sci. 2012. vol 370:5613–5635.
[68]
Ritchie KB, Smith GW. "Preferential carbon utilization by surface bacterial communities from water mass, normal, and white-band diseased Acropora cervicornis". Molecular Marine Biology and Biotechnology 1995. vol 4: 345–352.
[69]
Ritchie KB, Smith GW. "Carbon-source utilization of coral-associated marine hetero- trophs". J Mar Biotechnol 1995a. pp 3:107–109.
[70]
Ritchie KB, Smith GW. "Coral health and diseases". Springer: New York/Berlin" 2004.
[71]
Salihoglu, B., S. Neuer, S. Painting, R. Murtugudde, E. E. Hofmann, J. H. Steele, et al. "Bridging marine ecosystem and biogeochemistry research: lessons and recommendations from comparative studies". J. Mar. Syst. 2012. vol 109–110:161–175.
[72]
Schloss PD. Westcott SL, Ryabin T, Hall JR, Hartman M. Hollister EB. Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG. Van Horn DJ, Weber CF. "Introducing mothur: open-source, platform-independent, community supported software for describing and comparing microbial communities". Appl. Environ. Microbiol 2009. Vol 75:7535-7541.
[73]
Schloss PD. "Evaluating different approaches that test whether microbial communities have the same structure". The ISME J 2008. vol 2: 265-275.
[74]
Schloss PD, Handelsman J. "Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness". Appl Environ Microbiol 2005. vol 71: 1501–1506.
[75]
Shannon CE & Weaver W. "The Mathematical Theory of Communication". University of Illinois Press, Champaign, IL. Simpson EH. Measurement of Diversity. Nature 1994. pp 163:688.
[76]
Stachowicz JJ, Hay ME. "Mutualism and coral persistence: the role of herbivore resistance to algal chemical defense". Ecology 1999. vol 80:2085–2101.
[77]
Shinzato C et al. "Using the Acropora digitifera genome to understand coral response to environmental change". Nature 2011. vol 476: 320-323.
[78]
Simpson, C. J., J. L. Cary, and R. J. Masini. "Destruction of corals and other reef animals by coral spawn slicks on Ningaloo Reef, Western Australia". Coral Reefs 1993. vol 12:185–191.
[79]
Ueda T, Suga Y, Yahiro N, Matsuguchi T,. "Genetic diversity of N2-fixing bacteria associated with rice roots by molecular evolutionary analysis of nifD library". Can. J. Microbiol. 1995. vol 41:235-240.
[80]
Ulisse Cardini, Vanessa N. Bednarz, Rachel A. Foster & Christian Wild. "Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change". Eco. Evol. 2014. vol 4(9); 1706-1727.
[81]
Williams WM, Viner AB, Broughton WJ,. “Nitrogen fixation (acetylene reduction) associated with the living coral Acropora variabilis.” Mar Biol. 1987. vol 94: 531-535.
[82]
Wilkinson, C. R., D. M. Williams, P. W. Sammarco, R. W. Hogg, and L. A. Trott. "Rates of nitrogen-fixation on coral reefs across the continental-shelf of the central Great Barrier Reef". Mar. Biol. 1984. vol 80:255–262.
[83]
Winnepenninckx, B., Backeljau, T. and De Wachter, R. "Extraction of high molecular weight DNA from molluscs". TIG 1993. pp 9: 407.
[84]
Yang JD, Worley E, Wang MY et al. "Natural variation for nutrient use and remobilization efficiencies in switchgrass". Bio Energy Res. 2009. vol 2:257-266.
[85]
Yang CS et al. Endozoicomonas montiporae sp. nov. isolated from the encrusting pore coral Montipora aequituberculata. Int. J. Syst. Evol. Microbiol, 2010. vol 60; 1158-1162.
[86]
Zehr JP, Jenkins BD, Short SM, Steward GF. Nitrogenase gene diversity and microbial community structure: across-system comparison". Environ. Microbiol. 2003. vol 5:539–554.
[87]
Zehr JP, McReynolds LA. "Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii." Appl. Environ. Microbiol. 1989. vol 55:2522–2526.
[88]
Oliver TA, Palumbi SR. "Do fluctuating temperature environments elevate coral thermal tolerance?" Coral reef 2011. vol 30;429-440.
Browse journals by subject