造礁石珊瑚共附生固氮微生物的固氮活性
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摘要
造礁石珊瑚是珊瑚礁生态系统的主要建造者,其共附生微生物参与的生物固氮过程可以缓解寡营养海域的氮素限制,从而维持珊瑚礁生态系统较高的初级生产力。本研究以位于海南三亚鹿回头和西沙南沙洲两地的造礁石珊瑚为对象,采用乙炔还原法测定了不同季节及不同物种的珊瑚共附生固氮微生物的固氮活性;同时测定了海水营养盐含量,分析了珊瑚固氮活性与环境因子之间的关系。结果表明:三亚鹿回头海域的鹿角杯形珊瑚(Pocillopora damicornis)、澄黄滨珊瑚(Porites lutea)和芽枝鹿角珊瑚(Acropora gemmifera)的固氮活性无季节性差异;但相同季节3种珊瑚的固氮活性具有显著的物种间差异,其中鹿角杯形珊瑚的固氮活性最高(P<0.05),夏季为5.925×10~(-11)mol C_2H_4·g~(-1)·h~(-1),冬季为6.471×10~(-11)mol C_2H_4·g~(-1)·h~(-1);西沙寡营养条件下的澄黄滨珊瑚的固氮活性在夏季为5.401×10~(-11)mol C_2H_4·g~(-1)·h~(-1),显著高于同一季节三亚鹿回头的澄黄滨珊瑚的固氮活性(1.971×10~(-11)mol C_2H_4·g~(-1)·h~(-1))(P<0.01)。研究表明,在营养盐浓度较高的背景下,珊瑚的固氮活性受环境因子和季节变化的影响较小。西沙南沙州海水中溶解性营养盐浓度的升高可能会减弱珊瑚共附生固氮微生物的固氮能力。
Hermatypic corals are the main constructor of coral reef ecosystems. The nitrogen( N)fixation by hermatypic corals associated microbes can relieve N limitation in oligotrophic tropical waters,and consequently sustain high primary productivity of the coral reef ecosystems. In this study,the acetylene reduction assay( ARA) method was applied to detect the N fixation rate of diazotrophs associated with the corals inhabited in Luhuitou Peninsula,Sanya,Hainan and Nanshazhou,Xisha Island. The concentrations of dissolved inorganic nutrients were measured to explore the relationship between N fixation rate and environmental factors. The N fixation rate of all investigated corals in Luhuitou Peninsula showed no significant seasonal change. There were significant differences in the N fixation rates among Pocillopora damicornis,Porites lutea,and Acropora gemmifera. The highest N fixation rate was detected in Pocillopora damicomis( P < 0. 05),being 5.925×10~(-11) mol C_2H_4·g~(-1)·h~(-1) and 6. 471 × 10~(-11) mol C_2H_4·g~(-1)·h~(-1) in summer and winter,respectively. The N fixation rate of Porites lutea( 5. 401 × 10~(-11) mol C_2H_4·g~(-1)·h~(-1))from oligotrophic Xisha was significantly higher than that from Lunhuitou( 1.971×10~(-11) mol C_2H_4·g~(-1)·h~(-1))( P<0.01). Our results revealed no seasonal variation of N fixing rate in coral reef ecosystems with high concentration of nutrients. In addition,the high concentration of soluble nutrients in seawater may reduce the N fixation activity in corals.
Hermatypic corals are the main constructor of coral reef ecosystems. The nitrogen( N)fixation by hermatypic corals associated microbes can relieve N limitation in oligotrophic tropical waters,and consequently sustain high primary productivity of the coral reef ecosystems. In this study,the acetylene reduction assay( ARA) method was applied to detect the N fixation rate of diazotrophs associated with the corals inhabited in Luhuitou Peninsula,Sanya,Hainan and Nanshazhou,Xisha Island. The concentrations of dissolved inorganic nutrients were measured to explore the relationship between N fixation rate and environmental factors. The N fixation rate of all investigated corals in Luhuitou Peninsula showed no significant seasonal change. There were significant differences in the N fixation rates among Pocillopora damicornis,Porites lutea,and Acropora gemmifera. The highest N fixation rate was detected in Pocillopora damicomis( P < 0. 05),being 5.925×10~(-11) mol C_2H_4·g~(-1)·h~(-1) and 6. 471 × 10~(-11) mol C_2H_4·g~(-1)·h~(-1) in summer and winter,respectively. The N fixation rate of Porites lutea( 5. 401 × 10~(-11) mol C_2H_4·g~(-1)·h~(-1))from oligotrophic Xisha was significantly higher than that from Lunhuitou( 1.971×10~(-11) mol C_2H_4·g~(-1)·h~(-1))( P<0.01). Our results revealed no seasonal variation of N fixing rate in coral reef ecosystems with high concentration of nutrients. In addition,the high concentration of soluble nutrients in seawater may reduce the N fixation activity in corals.
引文
陈蕾,张燕英,董俊德,等.2013.三亚湾壮实鹿角珊瑚组织内共附生固氮菌多样性分析.科学通报,58(17):1596-1603.
樊惠.1995.乙炔还原法测定固氮作用的限制因素.微生物学通报,22(4):235-238.
黄小芳,董俊德,张燕英,等.2012.海洋固氮微生物与环境因子关系综述.生态学杂志,31(4):1028-1033.
林峰,陈敏,杨伟锋,等.2013.夏季台湾海峡南部海域上层水体的生物固氮作用.生态学报,33(19):6354-6362.
王丽荣,赵焕庭.2006.珊瑚礁生态系统服务及其价值评估.生态学杂志,25(11):1384-1389.
Bakus GJ.1969.Energetics and feeding in shallow marine waters.International Review of General and Experimental Zoology,4:275-369.
Bednarz VN,Cardini U,Hoytema NV,et al.2015.Seasonal variation in dinitrogen fixation and oxygen fluxes associated with two dominant zooxanthellate soft corals from the northern Red Sea.Marine Ecology Progress Series,519:141-152.
Bythell JC,Wild C.2011.Biology and ecology of coral mucus release.Journal of Experimental Marine Biology and Ecology,408:88-93.
Cardini U,Bednarz VN,Naumann MS,et al.2015.Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions.Proceedings of the Royal Society B:Biological Sciences,282:2015-2257.
Davey M,Holmes G,Johnstone R.2008.High rates of nitrogen fixation(acetylene reduction)on coral skeletons following bleaching mortality.Coral Reefs,27:227-236.
Ferguson RL,Buckley EN,Palumbo AV.1984.Response of marine bacterioplankton to differential filtration and confinement.Applied and Environmental Microbiology,47:49-55.
Flett RJ,Hamilton RD,Campbell NE.1976.Aquatic acetylenereduction techniques:Solutions to several problems.Canadian Journal of Microbiology,22:43-51.
Grover R,Ferrierpagès C,Maguer JF,et al.2014.Nitrogen fixation in the mucus of Red Sea corals.Journal of Experimental Biology,217:3962.
Holmes G,Johnstone RW.2010.The role of coral mortality in nitrogen dynamics on coral reefs.Journal of Experimental Marine Biology and Ecology,387:1-8.
Johannes RE,Alberts J,D'Elia C,et al.1972.The metabolism of some coral reef communities:A team study of nutrient and energy flux at Eniwetok.Bioscience,22:541-543.
Larkum AWD.1988.High rates of nitrogen fixation on coral skeletons after predation by the crown of thorns starfish Acanthaster planci.Marine Biology,97:503-506.
Lema KA,Willis BL,Bourne DG.2012.Corals form characteristic associations with symbiotic nitrogen-fixing bacteria.Applied and Environmental Microbiology,78:3136-44.
Lesser MP,Falcon LI,Rodriguez-Roman A,et al.2007.Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa.Marine Ecology Progress Series,346:143-152.
Lewis JB.2010.Processes of organic production on coral reefs.Biological Reviews,52:305-347.
Lovelock CE,Feller IC,Mckee KL,et al.2004.The effect of nutrient enrichment on growth,photosynthesis and hydraulic conductance of dwarf mangroves in Panam.Functional Ecology,18:25-33.
Odum HT,Odum EP.1955.Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll.Ecological Monographs,25:291-320.
O'Neil JM,Capone DG.1989.Nitrogenase activity in tropical carbonate marine sediments.Marine Ecology Progress Series,56:145-156.
Patriquin D,Knowles R.1972.Nitrogen fixation in rhizosphere of marine angiosperms.Marine Biology,16:49-58.
Pogoreutz C,Radecker N,Cardenas A,et al.2017a.Sugar enrichment provides evidence for a role of nitrogen fixation in coral bleaching.Global Change Biology,23:3838-3848.
Pogoreutz C,Radecker N,Cardenas A,et al.2017b.Nitrogen fixation aligns with nif H abundance and expression in two coral trophic functional groups.Frontiers in Microbiology,8:1187.
Radecker N,Meyer FW,Bednarz VN,et al.2014.Ocean acidification rapidly reduces dinitrogen fixation associated with the hermatypic coral Seriatopora hystrix.Marine Ecology Progress Series,511:297-302.
Ruth R,Pandolfi JM,Lovelock CE.2012.The effect of nutrient enrichment on the growth,nucleic acid concentrations,and elemental stoichiometry of coral reef macroalgae.Ecology and Evolution,2:1985-1995.
Shashar N,Cohen Y,Loya Y,et al.1994a.Nitrogen fixation(acetylene reduction)in stony corals:Evidence for coralbacteria interactions.Marine Ecology Progress Series,17:41-68.
Shashar N,Feldstein T,Cohen Y,et al.1994b.Nitrogen fixation(acetylene reduction)on a coral reef.Coral Reefs,13:171-174.
Smith SV.1984.Phosphorus versus nitrogen limitation in the marine environment.Limnology and Oceanography,29:1149-1160.
Sohm JA,Webb EA,Capone DG.2011.Emerging patterns of marine nitrogen fixation.Nature Reviews Microbiology,9:499-508.
Staal M,Lintelhekkert ST,Harren F,et al.2001.Nitrogenase activity in cyanobacteria measured by the acetylene reduction assay:A comparison between batch incubation and on-line monitoring.Environmental Microbiology,3:343-351.
Szmant AM.2002.Nutrient enrichment on coral reefs:Is it a major cause of coral reef decline.Estuaries,25:743-766.
Webb KL,Dupaul WD,Wiebe W,et al.1975.Enewetak(Eniwetok)Atoll:Aspects of the nitrogen cycle on a coral reef.Limnology and Oceanography,20:198-210.
Wiebe WJ,Johannes RE,Webb KL.1975.Nitrogen fixation in a coral reef community.Science,188:257-259.
Wilkinson CR,Sammarco PW.1983.Effects of fish grazing and damselfish territoriality on coral reef algae.II.nitrogen fixation.Marine Ecology,13:15-19.
Wilkinson CR,Williams DM,Sammarco PW,et al.1984.Rates of nitrogen fixation on coral reefs across the continental shelf of the central Great Barrier Reef.Marine Biology,80:255-262.
Williams WM,Viner AB,Broughton WJ.1987.Nitrogen fixation(acetylene reduction)associated with the living coral Acropora variabilis.Marine Biology,94:531-535.
Wilson ST,B9ttjer D,Church MJ,et al.2012.Comparative assessment of nitrogen fixation methodologies,conducted in the oligotrophic north pacific ocean.Applied and Environmental Microbiology,78:6516-23.
樊惠.1995.乙炔还原法测定固氮作用的限制因素.微生物学通报,22(4):235-238.
黄小芳,董俊德,张燕英,等.2012.海洋固氮微生物与环境因子关系综述.生态学杂志,31(4):1028-1033.
林峰,陈敏,杨伟锋,等.2013.夏季台湾海峡南部海域上层水体的生物固氮作用.生态学报,33(19):6354-6362.
王丽荣,赵焕庭.2006.珊瑚礁生态系统服务及其价值评估.生态学杂志,25(11):1384-1389.
Bakus GJ.1969.Energetics and feeding in shallow marine waters.International Review of General and Experimental Zoology,4:275-369.
Bednarz VN,Cardini U,Hoytema NV,et al.2015.Seasonal variation in dinitrogen fixation and oxygen fluxes associated with two dominant zooxanthellate soft corals from the northern Red Sea.Marine Ecology Progress Series,519:141-152.
Bythell JC,Wild C.2011.Biology and ecology of coral mucus release.Journal of Experimental Marine Biology and Ecology,408:88-93.
Cardini U,Bednarz VN,Naumann MS,et al.2015.Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions.Proceedings of the Royal Society B:Biological Sciences,282:2015-2257.
Davey M,Holmes G,Johnstone R.2008.High rates of nitrogen fixation(acetylene reduction)on coral skeletons following bleaching mortality.Coral Reefs,27:227-236.
Ferguson RL,Buckley EN,Palumbo AV.1984.Response of marine bacterioplankton to differential filtration and confinement.Applied and Environmental Microbiology,47:49-55.
Flett RJ,Hamilton RD,Campbell NE.1976.Aquatic acetylenereduction techniques:Solutions to several problems.Canadian Journal of Microbiology,22:43-51.
Grover R,Ferrierpagès C,Maguer JF,et al.2014.Nitrogen fixation in the mucus of Red Sea corals.Journal of Experimental Biology,217:3962.
Holmes G,Johnstone RW.2010.The role of coral mortality in nitrogen dynamics on coral reefs.Journal of Experimental Marine Biology and Ecology,387:1-8.
Johannes RE,Alberts J,D'Elia C,et al.1972.The metabolism of some coral reef communities:A team study of nutrient and energy flux at Eniwetok.Bioscience,22:541-543.
Larkum AWD.1988.High rates of nitrogen fixation on coral skeletons after predation by the crown of thorns starfish Acanthaster planci.Marine Biology,97:503-506.
Lema KA,Willis BL,Bourne DG.2012.Corals form characteristic associations with symbiotic nitrogen-fixing bacteria.Applied and Environmental Microbiology,78:3136-44.
Lesser MP,Falcon LI,Rodriguez-Roman A,et al.2007.Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa.Marine Ecology Progress Series,346:143-152.
Lewis JB.2010.Processes of organic production on coral reefs.Biological Reviews,52:305-347.
Lovelock CE,Feller IC,Mckee KL,et al.2004.The effect of nutrient enrichment on growth,photosynthesis and hydraulic conductance of dwarf mangroves in Panam.Functional Ecology,18:25-33.
Odum HT,Odum EP.1955.Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll.Ecological Monographs,25:291-320.
O'Neil JM,Capone DG.1989.Nitrogenase activity in tropical carbonate marine sediments.Marine Ecology Progress Series,56:145-156.
Patriquin D,Knowles R.1972.Nitrogen fixation in rhizosphere of marine angiosperms.Marine Biology,16:49-58.
Pogoreutz C,Radecker N,Cardenas A,et al.2017a.Sugar enrichment provides evidence for a role of nitrogen fixation in coral bleaching.Global Change Biology,23:3838-3848.
Pogoreutz C,Radecker N,Cardenas A,et al.2017b.Nitrogen fixation aligns with nif H abundance and expression in two coral trophic functional groups.Frontiers in Microbiology,8:1187.
Radecker N,Meyer FW,Bednarz VN,et al.2014.Ocean acidification rapidly reduces dinitrogen fixation associated with the hermatypic coral Seriatopora hystrix.Marine Ecology Progress Series,511:297-302.
Ruth R,Pandolfi JM,Lovelock CE.2012.The effect of nutrient enrichment on the growth,nucleic acid concentrations,and elemental stoichiometry of coral reef macroalgae.Ecology and Evolution,2:1985-1995.
Shashar N,Cohen Y,Loya Y,et al.1994a.Nitrogen fixation(acetylene reduction)in stony corals:Evidence for coralbacteria interactions.Marine Ecology Progress Series,17:41-68.
Shashar N,Feldstein T,Cohen Y,et al.1994b.Nitrogen fixation(acetylene reduction)on a coral reef.Coral Reefs,13:171-174.
Smith SV.1984.Phosphorus versus nitrogen limitation in the marine environment.Limnology and Oceanography,29:1149-1160.
Sohm JA,Webb EA,Capone DG.2011.Emerging patterns of marine nitrogen fixation.Nature Reviews Microbiology,9:499-508.
Staal M,Lintelhekkert ST,Harren F,et al.2001.Nitrogenase activity in cyanobacteria measured by the acetylene reduction assay:A comparison between batch incubation and on-line monitoring.Environmental Microbiology,3:343-351.
Szmant AM.2002.Nutrient enrichment on coral reefs:Is it a major cause of coral reef decline.Estuaries,25:743-766.
Webb KL,Dupaul WD,Wiebe W,et al.1975.Enewetak(Eniwetok)Atoll:Aspects of the nitrogen cycle on a coral reef.Limnology and Oceanography,20:198-210.
Wiebe WJ,Johannes RE,Webb KL.1975.Nitrogen fixation in a coral reef community.Science,188:257-259.
Wilkinson CR,Sammarco PW.1983.Effects of fish grazing and damselfish territoriality on coral reef algae.II.nitrogen fixation.Marine Ecology,13:15-19.
Wilkinson CR,Williams DM,Sammarco PW,et al.1984.Rates of nitrogen fixation on coral reefs across the continental shelf of the central Great Barrier Reef.Marine Biology,80:255-262.
Williams WM,Viner AB,Broughton WJ.1987.Nitrogen fixation(acetylene reduction)associated with the living coral Acropora variabilis.Marine Biology,94:531-535.
Wilson ST,B9ttjer D,Church MJ,et al.2012.Comparative assessment of nitrogen fixation methodologies,conducted in the oligotrophic north pacific ocean.Applied and Environmental Microbiology,78:6516-23.