Abstract
This study examined the response of a coral holobiont to thermal stress when the bacterial community was treated with antibiotics. Colonies of Pocillopora damicornis were exposed to broad and narrow-spectrum antibiotics targeting coral-associated α and γ-Proteobacteria. Corals were gradually heated from the control temperature of 26 to 31 °C, and measurements were made of host, zooxanthellar and microbial condition. Antibiotics artificially reduced the abundance and activity of bacteria, but had minimal effect on zooxanthellae photosynthetic efficiency or host tissue protein content. Heated corals without antibiotics showed significant declines in F V /F M , typical of thermal stress. However, heated corals treated with antibiotics showed severe tissue loss in addition to a decline in F V /F M . This study demonstrated that a disruption to the microbial consortium diminished the resilience of the holobiont. Corals exposed to antibiotics under control temperature did not bleach, suggesting that temperature may be an important factor influencing the activity, diversity and ecological function of the holobiont bacterial community.
Similar content being viewed by others
References
Ainsworth TD, Fines M, Roff G, Hoegh-Gildberg O (2008) Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patigonica. ISME J 2:67–73
Ainsworth TD, Thurber RV, Gates RD (2010) The future of coral reefs: a microbial perspective. Trends Ecol Evol 25:233–240
Amann RI, Ludwig W, Schleifer K-H (1995) Phylogenic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20
Barron MG, McGill CJ, Courtney LA, Marcovich DT (2010) Experimental bleaching of a reef-building coral using a simplified recirculating laboratory exposure system. J Mar Biol Article ID 415167:8
Ben-Haim Y, Rosenberg E (2002) A novel Vibrio sp. pathogen of the coral Pocillopora damicornis. Mar Biol 141:47–55
Ben-Haim Y, Rosenberg E (2004) Temperature-regulated bleaching and tissue lysis of Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, New York, pp 301–324
Ben-Haim Y, Zicherman-Keren M, Rosenberg E (2003) Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Envir Microbiol 69:4236–4242
Berner T, Baghdasarian G, Muscatine L (1993) Repopulation of a sea anemone with symbiotic dinoflagellates: analysis by in vivo fluorescence. J Exp Mar Biol Ecol 170:145–158
Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174
Bourne D, Iida Y, Uthicke S, Smith-Keune C (2008) Changes in coral-associated microbial communities during a bleaching event. ISME J 2:350–363
Brown BE, Le Tissier MDA, Bythell JC (1995) Mechanisms of bleaching deduced from histological studies of reef corals during a natural bleaching event. Mar Biol 122:655–663
Choi KH, Dobbs FC (1999) Comparison of two kinds of Biolog microplates (GN and ECO) in their ability to distinguish among aquatic microbial communities. J Microbiol Methods 36:203–213
D’Croz L, Maté JL (2004) Experimental responses to elevated water temperature in genotypes of the reef coral Pocillopora damicornis from upwelling and non-upwelling environments in Panama. Coral Reefs 23:473–483
Davies PS (1984) The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi. Coral Reefs 2:181–186
Ducklow HW, Mitchell R (1979) Bacterial populations and adaptations in the mucus layers on living corals. Limnol Oceanogr 24:715–725
Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biol Bull 182:324–332
Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Change Biol 2:495–509
Hill R, Larkum A, Frankart C, Kühl M, Ralph PJ (2004) Loss of functional Photosystem II reaction centres in zooxanthellae of corals exposed to bleaching conditions: using fluorescence rise kinetics. Photosynth Res 82:59–72
Hill R, Brown CM, DeZeeuw K, Campbell DA, Ralph PJ (2011) Increased rate of D1 repair in coral symbionts during bleaching is insufficient to counter accelerated photo-inactivation. Limnol Oceanogr 56:139–146
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
Hueerkamp C, Glynn PW, D’Croz L, Maté JL, Colley SB (2001) Bleaching and recovery of five eastern Pacific corals in an El Niño-related temperature experiment. Bull Mar Sci 69:215–236
Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c 1 and c 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanzen 167:191–194
Jokiel PL (2004) Temperature stress and coral bleaching. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, New York, pp 401–425
Jones RJ (1997) Zooxanthellae loss as a bioassay for assessing stress in corals. Mar Ecol Prog Ser 149:163–171
Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant, Cell Environ 21:1219–1230
Koh EG (1997) Do scleractinian corals engage in chemical warfare against microbes? J Chem Ecol 23:379–398
Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72:5254–5259
Kushmaro A, Rosenberg E, Fine M, Ben-Haim Y, Loya Y (1998) Effect of temperature onbleaching of the coral Oculina patagonica by Vibrio shiloi AK-1. Mar Ecol Prog Ser 171:131–137
Kushmaro A, Banin E, Loya Y, Stackebrandt E, Rosenberg E (2001) Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica. Int J Syst Evol Microbiol 51:1383–1388
Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000
Lesser MP, Falcón LI, Rodríguez-Román A, Enríquez S, Hoegh-Guldberg O, Iglesias-Prieto R (2007) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152
Levy O, Dubinsky Z, Achituv Y, Erez J (2006) Diurnal polyp expansion behavior in stony corals may enhance carbon availability for symbionts photosynthesis. J Exp Mar Biol Ecol 333:1–11
Mouchka ME, Hewson I, Harvell CD (2010) Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol 50:662–674
Raina J-B, Tapiolas D, Willis BL, Bourne DG (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol 75:3492–3501
Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073
Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14
Ritchie KB, Smith GW (2004) Microbial communities of coral surface mucopolysaccharide layers. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, New York, pp 259–264
Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10
Rosenberg E (2004) The bacterial disease hypothesis of coral bleaching. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, New York, pp 445–461
Rosenberg E, Ben-Haim Y (2002) Microbial diseases of corals and global warming. Environ Microbiol 4:318–326
Rosenberg E, Kellog CA, Rowher F (2007a) Coral microbiology. Oceanography 20:146–154
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007b) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362
Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 34:407–417
Rypien KL, Ward JR, Azam F (2010) Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12:28–39
Sala MM, Arin L, Balagué V, Felipe J, Guadayol Ò, Vaqué D (2005) Functional diversity of bacterioplankton assemblages in western Antarctic seawaters during late spring. Mar Ecol Prog Ser 292:13–21
Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou GC, Govindjee S (eds) Chlorophyll fluorescence: a signature of photosynthesis. Kluwer, Dordrecht, pp 279–319
Schultz GE, Ducklow H (2000) Changes in bacterioplankton metabolic capabilities along a salinity gradient in the York River estuary, Virginia, USA. Aquat Microb Ecol 22:163–174
Shashar N, Cohen Y, Loya Y, Sar N (1994) Nitrogen fixation (acetylene reduction) in stony corals: evidence for coral–bacteria interactions. Mar Ecol Prog Ser 111:259–264
Stefanowicz A (2006) The Biolog Plates technique as a tool in ecological studies of microbial communities. Polish J Environ Stud 15:669–676
Stimson J, Kinzie RA III (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J Exp Mar Biol Ecol 153:63–74
Sweet MJ, Croquer A, Bythell JC (2011a) Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30:39–52
Sweet MJ, Croquer A, Bythell JC (2011b) Dynamics of bacterial community development in the reef coral Acropora muricata following experimental antibiotic treatment. Coral Reefs 30:1121–1133
Thurber RLV, Barott KL, Hall D, Liu H, Rodriguez-Mueller B, Desnues C, Edwards RA, Haynes M, Angly FE, Wegley L, Rohwer FL (2008) Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. Proc Natl Acad Sci USA 105:18413–18418
Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11:2148–2163
Toren A, Landau L, Kushmaro A, Loya Y, Rosenberg E (1998) Effect of temperature on adhesion of Vibrio strain AK-1 to Oculina patagonica and on coral bleaching. Appl Environ Microbiol 64:1379–1384
Ulstrup KE, Berkelmans R, Ralph PJ, van Oppen MJH (2006) Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: the role of zooxanthellae. Mar Ecol Prog Ser 314:135–148
van Oppen MJH, Leong J, Gates RD (2009) Coral-virus interactions: a double-edged sword? Symbiosis 47:1–8
Wang G-H, Liu J–J, Qi X-N, Jin J, Wang Y, Liu X-B (2008) Effects of fertilization on bacterial community structure and function in a black soil of Dehui region estimated by Biolog and PCR-DGGE methods. Acta Ecologica Sinica 28:220–226
Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012
Whitaker JR, Granum PE (1980) An absolute method for protein determination based on difference in absorbance at 235 and 280 nm. Anal Biochem 109:156–157
Wilson WH, Francis I, Ryan K, Davy SK (2001) Temperature induction of viruses in symbiotic dinoflagellates. Aquat Microb Ecol 25:99–102
Wilson WH, Dale AL, Davy JE, Davy SK (2005) An enemy within? Observations of virus-like particles in reef corals. Coral Reefs 24:145–148
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Kühl.
Electronic supplementary material
Below is the link to the electronic supplementary material.
227_2012_1967_MOESM1_ESM.eps
Photographs showing coral condition representative of each treatment after 120 h. a Control, b + Antibiotics, c Heat-stressed d Heat-stress + Antibiotics (EPS 3.47 mb)
Rights and permissions
About this article
Cite this article
Gilbert, J.A., Hill, R., Doblin, M.A. et al. Microbial consortia increase thermal tolerance of corals. Mar Biol 159, 1763–1771 (2012). https://doi.org/10.1007/s00227-012-1967-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-012-1967-9