铝对海洋固氮蓝藻Crocosphaera watsonii生长及固氮速率的影响
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摘要
大气沉降向海洋表层输入大量的铝,然而关于铝对海洋浮游植物的影响却少有研究报道。目前,铝对在海洋碳和氮循环中起着重要作用的固氮生物影响的研究还较少。文章以Aquil培养基(无氮硅营养盐)半连续培养单细胞海洋固氮蓝藻Crocosphaera watsonii,利用流式细胞技术和~(15)N同位素示踪法,研究铝(0、0.2、2和20μmol×L~(–1))对Crocosphaera watsonii生长和固氮作用的影响。数据表明,3个铝处理组Crocosphaera watsonii细胞大小、光合色素含量和光系统Ⅱ(PSⅡ)原初光能转化效率(F_v/F_m)都显著降低,生长速率和固氮速率明显受到抑制。结果表明,在营养充足条件下,铝对Crocosphaera watsonii生长和固氮具有抑制性作用。
Although a large amount of aluminum enters the ocean through atmospheric dust deposition every year,the effect of aluminum on marine phytoplankton is seldom examined.Few studies focused on the effects of aluminum on marine nitrogen-fixing cyanobacteria,which play important roles in nitrogen and carbon cycling in the ocean.In this study,a unicellular marine nitrogen-fixing cyanobacterium Crocosphaera watsonii grew in Aquil medium without silicate and nitrogen by semi-continuous cultures.We studied the effect of aluminum(0,0.2,2 and 20 μmol×L~(–1)) on the growth rate and nitrogen fixation rate of Crocosphaera watsonii by using flow cytometry and ~(15)N isotope tracer method.Results showed that aluminum inhibited the growth and nitrogen fixation of Crocosphaera watsonii.Results also showed that cell size,cellular pigments and photochemical efficiency of photosystem II(Fv/Fm) of Crocosphaera watsonii treated with aluminum were significantly decreased.These results demonstrate that aluminum has an inhibitory effect on the growth and nitrogen fixation of Crocosphaera watsonii under the condition of sufficient phosphate and trace nutrients.
Although a large amount of aluminum enters the ocean through atmospheric dust deposition every year,the effect of aluminum on marine phytoplankton is seldom examined.Few studies focused on the effects of aluminum on marine nitrogen-fixing cyanobacteria,which play important roles in nitrogen and carbon cycling in the ocean.In this study,a unicellular marine nitrogen-fixing cyanobacterium Crocosphaera watsonii grew in Aquil medium without silicate and nitrogen by semi-continuous cultures.We studied the effect of aluminum(0,0.2,2 and 20 μmol×L~(–1)) on the growth rate and nitrogen fixation rate of Crocosphaera watsonii by using flow cytometry and ~(15)N isotope tracer method.Results showed that aluminum inhibited the growth and nitrogen fixation of Crocosphaera watsonii.Results also showed that cell size,cellular pigments and photochemical efficiency of photosystem II(Fv/Fm) of Crocosphaera watsonii treated with aluminum were significantly decreased.These results demonstrate that aluminum has an inhibitory effect on the growth and nitrogen fixation of Crocosphaera watsonii under the condition of sufficient phosphate and trace nutrients.
引文
李建宏,曾昭琪,1997.Co、Ni、Cu、Zn离子对蓝藻藻胆体光谱影响研究[J].南京大学学报(自然科学),33(4):639-643.LIJIANHONG,TSENG CHAOTSI,1997.Effects of Co,Ni,Cu,Zn ions on spectra of phycobiliprotein-vesicle[J].Journal of Nanjing University(Natural Sciences),33(4):159-163(in Chinese).
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母波,韩善华,张英慧,等,2007.汞对植物生理生化的影响[J].中国微生态学杂志,19(6):582-583.
史荣君,李志红,周林滨,等,2016.溶解态铝对海洋浮游植物群落结构及聚球藻生长的影响[J].南方水产科学,12(1):1-8.SHI RONGJUN,LI ZHIHONG,ZHOU LINBIN,et al.2016.Influence of dissolved aluminum on marine phytoplankton community structure and growth of Synechococcus sp[J].South China Fisheries Science,12(1):1-8(in Chinese).
BAUMANN H A,MORRISON L,STENGEL D B,2009.Metal accumulation and toxicity measured by PAM-chlorophyll fluorescence in seven species of marine macroalgae[J].Ecotoxicology and Environmental Safety,72(4):1063-1075.
BROWN M T,BRULAND K W,2009.Dissolved and particulate aluminum in the Columbia River and coastal waters of Oregon and Washington:behavior in near-field and far-field plumes[J].Estuarine,Coastal and Shelf Science,84(2):171-185.
DE JONG J T M,BOYéM,GELADO-CABALLERO M D,et al,2007.Inputs of iron,manganese and aluminium to surface waters of the Northeast Atlantic Ocean and the European continental shelf[J].Marine Chemistry,107(2):120-142.
EXLEY C,TOLLERVEY A,GRAY G,et al,1993.Silicon,aluminium and the biological availability of phosphorus in algae[J].Proceedings of the Royal Society B:Biological Sciences,253(1336):93-99.
GARCIA N S,FU FEIXUE,HUTCHINS D A,2013.Colimitation of the unicellular photosynthetic diazotroph Crocosphaera watsonii by phosphorus,light,and carbon dioxide[J].Limnology and Oceanography,58(4):1501-1512.
GARCIA N S,FU FEIXUE,SEDWICK P N,et al,2015.Iron deficiency increases growth and nitrogen-fixation rates of phosphorus-deficient marine cyanobacteria[J].The ISMEJournal,9:238-245.
GEHLEN M,HEINZE C,MAIER-REIMER E,et al,2003.Coupled Al-Si geochemistry in an ocean general circulation model:A tool for the validation of oceanic dust deposition fields?[J].Global Biogeochemical Cycles,17(1):1028.
GENSEMER R W,PLAYLE R C,1999.The bioavailability and toxicity of aluminum in aquatic environments[J].Critical Reviews in Environmental Science and Technology,29(4):315-450.
GILLMORE M L,GOLDING L A,ANGEL B M,et al,2016Toxicity of dissolved and precipitated aluminium to marine diatoms[J].Aquatic Toxicology,174:82-91.
GLAZER A N,1982.Phycobilisomes:structure and dynamics[J].Annual Review of Microbiology,36(1):173-198.
GOLDING L A,ANGEL B M,BATLEY G E,et al,2015.Derivation of a water quality guideline for aluminium in marine waters[J].Environmental Toxicology and Chemistry,34(1):141-151.
JACQ V,RIDAME C,L'HELGUEN S,et al,2014.Response of the unicellular diazotrophic cyanobacterium Crocosphaera watsonii to iron limitation[J].PLo S One,9(1):e86749.
KüPPER H,?ETLíK I,SPILLER M,et al,2002.Heavy metal-induced inhibition of photosynthesis:targets of in vivo heavy metal chlorophyll formation[J].Journal of Phycology,38(3):429-441.
KARL D,MICHAELS A,BERGMAN B,et al,2002.Dinitrogen fixation in the world's oceans[J].Biogeochemistry,57(1):47-98.
LEE CHEN YUH-LING,CHEN HOUNG-YUNG,LIN YEN-HUEI,et al,2014.The relative contributions of unicellular and filamentous diazotrophs to N2 fixation in the South China Sea and the upstream Kuroshio[J].Deep-Sea Research Part I:Oceanographic Research Papers,85:56-71.
LU RONGZHAO,YU YANLI,1985.Effects of proteinase Kon the energy transfer between phycobiliproteins in phycobilisomes[J].Photosynthesis Research,7(1):91-96.
MEASURES C I,VINK S,2000.On the use of dissolved aluminum in surface waters to estimate dust deposition to the ocean[J].Global Biogeochemical Cycles,14(1):317-327.
MENZEL D W,HULBURT E M,TYTHER J H,1963.The effects of enriching Sargasso Sea water on the production and species composition of the phytoplankton[J].Deep Sea Research and Oceanographic Abstracts,10(3):209-219.
MOHR W,GROΒKOPF T,WALLACE D W R,et al,2010a Methodological underestimation of oceanic nitrogen fixation rates[J].PLo S One,5(9):e12583.
MOHR W,INTERMAGGIO M P,LAROCHE J,2010b.Diel rhythm of nitrogen and carbon metabolism in the unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501[J]Environmental Microbiology,12(2):412-421.
MOISANDER P H,BEINART R A,HEWSON I,et al,2010Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain[J].Science,327(5972):1512-1514.
MONTOYA J P,VOSS M,K?HLER P,et al,1996.A simple high-precision,high-sensitivity tracer assay for N2 fixation[J]Applied and Environmental Microbiology,62(3):986-993.
NALEWAJKO C,PAUL B,1985.Effects of manipulations of aluminum concentrations and p H on phosphate uptake and photosynthesis of planktonic communities in two precambrian shield lakes[J].Canadian Journal of Fisheries and Aquatic Sciences,42(12):1946-1953.
PARKHILL J P,MAILLET G,CULLEN J J,2001.Fluorescencebased maximal quantum yield for PSⅡas a diagnostic of nutrient stress[J].Journal of Phycology,37(4):517-529.
PETTERSSON A,BLOMQVIST P,1992.Bioassay for phosphate demand in phytoplankton from acidified lakes:lake Njupfatet an example of phosphate deficiency induced by liming[J].Hydrobiologia,246(2):99-110.
SA?AN M T,BALCIO?LU I A,2006.A case study on algal response to raw and treated effluents from an aluminum plating plant and a pharmaceutical plant[J].Ecotoxicology and Environmental Safety,64(2):234-243.
SA?AN M T,OZTAY F,BOLKENT S,2007.Exposure of Dunaliella tertiolecta to lead and aluminum:Toxicity and effects on ultrastructure[J].Biological Trace Element Research,120(1/3):264-272.
SAMUELSSON G,?QUIST G,1977.A method for studying photosynthetic capacities of unicellular algae based on in vivo chlorophyll fluorescence[J].Physiologia Plantarum40(4):315-319.
SANTANA-CASIANO J M,GONZáLEZ-DáVILA M,LAGLERAL M,et al,1997.The influence of zinc,aluminum and cadmium on the uptake kinetics of iron by algae[J].Marine Chemistry,59(1/2):95-111.
SHI RONGJUN,LI GANG,ZHOU LINBIN,et al,2015.The increasing aluminum content affects the growth,cellular chlorophyll a and oxidation stress of cyanobacteria Synechococcus sp.WH7803[J].Oceanological and Hydrobiological Studies,44(3):343-351.
SOHM J A,WEBB E A,CAPONE D G,2011.Emerging patterns of marine nitrogen fixation[J].Nature Reviews Microbiology,9(7):499-508.
STOFFYN M,1979.Biological control of dissolved aluminum in seawater:experimental evidence[J].Science,203(4381):651-653.
SUNDA W G,HARDISON D R,2010.Evolutionary tradeoffs among nutrient acquisition,cell size,and grazing defense in marine phytoplankton promote ecosystem stability[J].Marine Ecology Progress Series,401:63-76.
SUNDA W G,PRICE N M,MOREL F M M,2005.Trace metal ion buffers and their use in culture studies[M]//ANDERSENR A.Algal Culturing Techniques.Amsterdam:Academy Press/Elsevier:35-63.
TAYLOR S R,1964.Trace element abundances and the chondritic earth model[J].Geochimica et Cosmochimica Acta,28(12):1989-1998.
TZUR A,MOORE J K,JORGENSEN P,et al,2011.Optimizing optical flow cytometry for cell volume-based sorting and analysis[J].PLo S One,6(1):e16053.
VRIELING E,POORT L,BEELEN T,et al,1999.Growth and silica content of the diatoms Thalassiosira weissflogii and Navicula salinarum at different salinities and enrichments with aluminium[J].European Journal of Phycology,34(3):307-316.
XIE JUN,BAI XIAOCUI,LAVOIE M,et al,2015.Analysis of the proteome of the marine diatom Phaeodactylum tricornutum exposed to aluminum providing insights into aluminum toxicity mechanisms[J].Environmental Science&Technology,49(18):11182-11190.
ZEHR J P,2011.Nitrogen fixation by marine cyanobacteria[J].Trends in Microbiology,19(4):162-173.
ZHOU LINBIN,TAN YEHUI,HUANG LIANGMING,et al,2016.Enhanced utilization of organic phosphorus in a marine diatom Thalassiosira weissflogii:A possible mechanism for aluminum effect under P limitation[J].Journal of Experimental Marine Biology and Ecology,478:77-85.
刘洁,常学秀,黄丽娟,等,2005.Ni元素对铜绿微囊藻的生长、光谱特性及藻胆蛋白含量的影响[J].云南大学学报(自然科学版),27(4):365-368.LIU JIE,CHANG XUEXIU,HUANG LIJUAN,et al,2005.Effects of Ni on the growth,absorption spectrum and phycobiliprotein content of Microcystis aeruginosa[J].Journal of Yunnan University,27(4):365-368(in Chinese).
母波,韩善华,张英慧,等,2007.汞对植物生理生化的影响[J].中国微生态学杂志,19(6):582-583.
史荣君,李志红,周林滨,等,2016.溶解态铝对海洋浮游植物群落结构及聚球藻生长的影响[J].南方水产科学,12(1):1-8.SHI RONGJUN,LI ZHIHONG,ZHOU LINBIN,et al.2016.Influence of dissolved aluminum on marine phytoplankton community structure and growth of Synechococcus sp[J].South China Fisheries Science,12(1):1-8(in Chinese).
BAUMANN H A,MORRISON L,STENGEL D B,2009.Metal accumulation and toxicity measured by PAM-chlorophyll fluorescence in seven species of marine macroalgae[J].Ecotoxicology and Environmental Safety,72(4):1063-1075.
BROWN M T,BRULAND K W,2009.Dissolved and particulate aluminum in the Columbia River and coastal waters of Oregon and Washington:behavior in near-field and far-field plumes[J].Estuarine,Coastal and Shelf Science,84(2):171-185.
DE JONG J T M,BOYéM,GELADO-CABALLERO M D,et al,2007.Inputs of iron,manganese and aluminium to surface waters of the Northeast Atlantic Ocean and the European continental shelf[J].Marine Chemistry,107(2):120-142.
EXLEY C,TOLLERVEY A,GRAY G,et al,1993.Silicon,aluminium and the biological availability of phosphorus in algae[J].Proceedings of the Royal Society B:Biological Sciences,253(1336):93-99.
GARCIA N S,FU FEIXUE,HUTCHINS D A,2013.Colimitation of the unicellular photosynthetic diazotroph Crocosphaera watsonii by phosphorus,light,and carbon dioxide[J].Limnology and Oceanography,58(4):1501-1512.
GARCIA N S,FU FEIXUE,SEDWICK P N,et al,2015.Iron deficiency increases growth and nitrogen-fixation rates of phosphorus-deficient marine cyanobacteria[J].The ISMEJournal,9:238-245.
GEHLEN M,HEINZE C,MAIER-REIMER E,et al,2003.Coupled Al-Si geochemistry in an ocean general circulation model:A tool for the validation of oceanic dust deposition fields?[J].Global Biogeochemical Cycles,17(1):1028.
GENSEMER R W,PLAYLE R C,1999.The bioavailability and toxicity of aluminum in aquatic environments[J].Critical Reviews in Environmental Science and Technology,29(4):315-450.
GILLMORE M L,GOLDING L A,ANGEL B M,et al,2016Toxicity of dissolved and precipitated aluminium to marine diatoms[J].Aquatic Toxicology,174:82-91.
GLAZER A N,1982.Phycobilisomes:structure and dynamics[J].Annual Review of Microbiology,36(1):173-198.
GOLDING L A,ANGEL B M,BATLEY G E,et al,2015.Derivation of a water quality guideline for aluminium in marine waters[J].Environmental Toxicology and Chemistry,34(1):141-151.
JACQ V,RIDAME C,L'HELGUEN S,et al,2014.Response of the unicellular diazotrophic cyanobacterium Crocosphaera watsonii to iron limitation[J].PLo S One,9(1):e86749.
KüPPER H,?ETLíK I,SPILLER M,et al,2002.Heavy metal-induced inhibition of photosynthesis:targets of in vivo heavy metal chlorophyll formation[J].Journal of Phycology,38(3):429-441.
KARL D,MICHAELS A,BERGMAN B,et al,2002.Dinitrogen fixation in the world's oceans[J].Biogeochemistry,57(1):47-98.
LEE CHEN YUH-LING,CHEN HOUNG-YUNG,LIN YEN-HUEI,et al,2014.The relative contributions of unicellular and filamentous diazotrophs to N2 fixation in the South China Sea and the upstream Kuroshio[J].Deep-Sea Research Part I:Oceanographic Research Papers,85:56-71.
LU RONGZHAO,YU YANLI,1985.Effects of proteinase Kon the energy transfer between phycobiliproteins in phycobilisomes[J].Photosynthesis Research,7(1):91-96.
MEASURES C I,VINK S,2000.On the use of dissolved aluminum in surface waters to estimate dust deposition to the ocean[J].Global Biogeochemical Cycles,14(1):317-327.
MENZEL D W,HULBURT E M,TYTHER J H,1963.The effects of enriching Sargasso Sea water on the production and species composition of the phytoplankton[J].Deep Sea Research and Oceanographic Abstracts,10(3):209-219.
MOHR W,GROΒKOPF T,WALLACE D W R,et al,2010a Methodological underestimation of oceanic nitrogen fixation rates[J].PLo S One,5(9):e12583.
MOHR W,INTERMAGGIO M P,LAROCHE J,2010b.Diel rhythm of nitrogen and carbon metabolism in the unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501[J]Environmental Microbiology,12(2):412-421.
MOISANDER P H,BEINART R A,HEWSON I,et al,2010Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain[J].Science,327(5972):1512-1514.
MONTOYA J P,VOSS M,K?HLER P,et al,1996.A simple high-precision,high-sensitivity tracer assay for N2 fixation[J]Applied and Environmental Microbiology,62(3):986-993.
NALEWAJKO C,PAUL B,1985.Effects of manipulations of aluminum concentrations and p H on phosphate uptake and photosynthesis of planktonic communities in two precambrian shield lakes[J].Canadian Journal of Fisheries and Aquatic Sciences,42(12):1946-1953.
PARKHILL J P,MAILLET G,CULLEN J J,2001.Fluorescencebased maximal quantum yield for PSⅡas a diagnostic of nutrient stress[J].Journal of Phycology,37(4):517-529.
PETTERSSON A,BLOMQVIST P,1992.Bioassay for phosphate demand in phytoplankton from acidified lakes:lake Njupfatet an example of phosphate deficiency induced by liming[J].Hydrobiologia,246(2):99-110.
SA?AN M T,BALCIO?LU I A,2006.A case study on algal response to raw and treated effluents from an aluminum plating plant and a pharmaceutical plant[J].Ecotoxicology and Environmental Safety,64(2):234-243.
SA?AN M T,OZTAY F,BOLKENT S,2007.Exposure of Dunaliella tertiolecta to lead and aluminum:Toxicity and effects on ultrastructure[J].Biological Trace Element Research,120(1/3):264-272.
SAMUELSSON G,?QUIST G,1977.A method for studying photosynthetic capacities of unicellular algae based on in vivo chlorophyll fluorescence[J].Physiologia Plantarum40(4):315-319.
SANTANA-CASIANO J M,GONZáLEZ-DáVILA M,LAGLERAL M,et al,1997.The influence of zinc,aluminum and cadmium on the uptake kinetics of iron by algae[J].Marine Chemistry,59(1/2):95-111.
SHI RONGJUN,LI GANG,ZHOU LINBIN,et al,2015.The increasing aluminum content affects the growth,cellular chlorophyll a and oxidation stress of cyanobacteria Synechococcus sp.WH7803[J].Oceanological and Hydrobiological Studies,44(3):343-351.
SOHM J A,WEBB E A,CAPONE D G,2011.Emerging patterns of marine nitrogen fixation[J].Nature Reviews Microbiology,9(7):499-508.
STOFFYN M,1979.Biological control of dissolved aluminum in seawater:experimental evidence[J].Science,203(4381):651-653.
SUNDA W G,HARDISON D R,2010.Evolutionary tradeoffs among nutrient acquisition,cell size,and grazing defense in marine phytoplankton promote ecosystem stability[J].Marine Ecology Progress Series,401:63-76.
SUNDA W G,PRICE N M,MOREL F M M,2005.Trace metal ion buffers and their use in culture studies[M]//ANDERSENR A.Algal Culturing Techniques.Amsterdam:Academy Press/Elsevier:35-63.
TAYLOR S R,1964.Trace element abundances and the chondritic earth model[J].Geochimica et Cosmochimica Acta,28(12):1989-1998.
TZUR A,MOORE J K,JORGENSEN P,et al,2011.Optimizing optical flow cytometry for cell volume-based sorting and analysis[J].PLo S One,6(1):e16053.
VRIELING E,POORT L,BEELEN T,et al,1999.Growth and silica content of the diatoms Thalassiosira weissflogii and Navicula salinarum at different salinities and enrichments with aluminium[J].European Journal of Phycology,34(3):307-316.
XIE JUN,BAI XIAOCUI,LAVOIE M,et al,2015.Analysis of the proteome of the marine diatom Phaeodactylum tricornutum exposed to aluminum providing insights into aluminum toxicity mechanisms[J].Environmental Science&Technology,49(18):11182-11190.
ZEHR J P,2011.Nitrogen fixation by marine cyanobacteria[J].Trends in Microbiology,19(4):162-173.
ZHOU LINBIN,TAN YEHUI,HUANG LIANGMING,et al,2016.Enhanced utilization of organic phosphorus in a marine diatom Thalassiosira weissflogii:A possible mechanism for aluminum effect under P limitation[J].Journal of Experimental Marine Biology and Ecology,478:77-85.