一株虾池来源的螺旋拟柱孢藻藻株的分离鉴定及重金属离子Cu~(2+)、Cd~(2+)和Pb~(2+)对其生长的影响
|
摘要
【目的】探讨凡纳滨对虾养殖水体中入侵蓝藻拟柱孢藻的生长生理特性。【方法】从汕头澄海人工对虾养殖池分离纯化藻株,通过形态及其16SrRNA基因鉴定,之后在CT与BG11两种蓝藻通用培养基的基础上优化最佳培养条件,最后分析了不同浓度的3种重金属离子即Cu~(2+)(0–0.8 mg/L)、Cd~(2+)(0–4 mg/L)和Pb~(2+)(0–80 mg/L)对藻株生长的影响。【结果】澄海虾池来源的分离纯化藻株形态呈卷曲螺旋型,16S rRNA基因序列与多株其他来源的拟柱孢藻相似度均达98%以上。实验室培养,藻株最佳生长状态的培养条件是在BG11培养基的基础上调整氮浓度及氮磷比分别为N 62 mg/L,N︰P=9︰1,在此条件下,藻丝生物量可达(0.632±0.170)×107/L,藻丝比平均生长速率最高为(0.063±0.001)/d。本分离藻株活体对重金属Cu~(2+)、Cd~(2+)和Pb~(2+)具有一定的耐受性,其耐受浓度范围分别为0–0.2、0–0.5和1–40 mg/L,其中,Cu~(2+)和Cd~(2+)对藻的生长具有抑制作用,而且此抑制作用随着金属离子剂量的增加及作用时间的延长更加显著,Cu~(2+)和Cd~(2+)对藻体的半数抑制浓度(96 h EC50)分别为0.125和0.551 mg/L;而浓度范围为0–80 mg/L的Pb~(2+)对藻体的生长则表现为低剂量(≤40 mg/L)呈促进,高剂量(≥80 mg/L)则抑制。【结论】从凡纳滨对虾养殖池中分离鉴定出一株形态呈螺旋型的拟柱孢藻,命名为螺旋拟柱孢藻(Cylindrospermopsis raciborskii helix),本藻株活体能够在一定浓度的Cu~(2+)、Cd~(2+)和Pb~(2+)中生长,为螺旋拟柱孢藻活藻生物吸附重金属离子而改善虾池水体环境提供了可能性。
[Objective] We examined the physiological characteristics of invasive cyanobacterium Cylindrospermopsis raciborskii helix isolated from Litopenaeus vannamei culture ponds. [Methods] The algal strain was isolated and purified from shrimp ponds in Chenghai, Shantou, and identified by morphology and 16 S rRNA sequence analysis. Then, with the general culture media of CT and BG11, we optimized the culture conditions. Finally, we analyzed the effect of heavy metals Cu~(2+)(0–0.8 mg/L), Cd~(2+)(0–4 mg/L) and Pb~(2+)(0–80 mg/L)on the growth of the isolated strain. [Results] The identity of 16 S rRNA sequence of the isolated strain was higher than 98% with that of typical strains of Cylindrospermopsis raciborskii from GenBank. Under laboratory culture conditions, the optimal culture medium for the growth of the isolated strain was the modified BG11(N 62 mg/L,N:P=9:1), the exponential biomass and growth rate were up to(0.632±0.170)×107/L,(0.063±0.001)/d, respectively.The isolated strain tolerated heavy metals Cu~(2+), Cd~(2+) and Pb~(2+), and the tolerance concentrations was Pb~(2+)1–40 mg/L, Cd~(2+) 0–0.5 mg/L, Cu~(2+) 0–0.2 mg/L. Furthermore, Cu~(2+) and Cd~(2+) inhibited the growth of the isolated strain, and the inhibition increased with enhancing of heavy metal concentration and contact time, the 96 h EC50 of Cu~(2+) and Cd~(2+) were 0.125 and 0.551 mg/L for the strain, respectively, but Pb~(2+)(0–80 mg/L) had a dual effect on its growth, which promoted growth at low concentration(≤40 mg/L) and inhibited growth at high concentration(≥80 mg/L). [Conclusion] A strain of Cylindrospermopsis raciborskii isolated from L. vannamei culture ponds has the potential of adsorbing heavy metal ions in shrimp ponds.
[Objective] We examined the physiological characteristics of invasive cyanobacterium Cylindrospermopsis raciborskii helix isolated from Litopenaeus vannamei culture ponds. [Methods] The algal strain was isolated and purified from shrimp ponds in Chenghai, Shantou, and identified by morphology and 16 S rRNA sequence analysis. Then, with the general culture media of CT and BG11, we optimized the culture conditions. Finally, we analyzed the effect of heavy metals Cu~(2+)(0–0.8 mg/L), Cd~(2+)(0–4 mg/L) and Pb~(2+)(0–80 mg/L)on the growth of the isolated strain. [Results] The identity of 16 S rRNA sequence of the isolated strain was higher than 98% with that of typical strains of Cylindrospermopsis raciborskii from GenBank. Under laboratory culture conditions, the optimal culture medium for the growth of the isolated strain was the modified BG11(N 62 mg/L,N:P=9:1), the exponential biomass and growth rate were up to(0.632±0.170)×107/L,(0.063±0.001)/d, respectively.The isolated strain tolerated heavy metals Cu~(2+), Cd~(2+) and Pb~(2+), and the tolerance concentrations was Pb~(2+)1–40 mg/L, Cd~(2+) 0–0.5 mg/L, Cu~(2+) 0–0.2 mg/L. Furthermore, Cu~(2+) and Cd~(2+) inhibited the growth of the isolated strain, and the inhibition increased with enhancing of heavy metal concentration and contact time, the 96 h EC50 of Cu~(2+) and Cd~(2+) were 0.125 and 0.551 mg/L for the strain, respectively, but Pb~(2+)(0–80 mg/L) had a dual effect on its growth, which promoted growth at low concentration(≤40 mg/L) and inhibited growth at high concentration(≥80 mg/L). [Conclusion] A strain of Cylindrospermopsis raciborskii isolated from L. vannamei culture ponds has the potential of adsorbing heavy metal ions in shrimp ponds.
引文
[1]Kovács AW,Présing M,V?r?s L.Thermal-dependent growth characteristics for Cylindrospermopsis raciborskii(Cyanoprokaryota)at different light availabilities:methodological considerations.Aquatic Ecology,2016,50(4):623-638.
[2]Dittmann E,Fewer DP,Neilan BA.Cyanobacterial toxins:biosynthetic routes and evolutionary roots.FEMSMicrobiology Reviews,2013,37(1):23-43.
[3]Vehovszkyá,Kovács AW,Farkas A,Gy?ri J,SzabóH,Vasas G.Pharmacological studies confirm neurotoxic metabolite(s)produced by the bloom-forming Cylindrospermopsis raciborskii in Hungary.Environmental Toxicology,2013,30(5):501-512.
[4]William WJ,Sarah S.Distribution and abundance of Cylindrospermopsis raciborskii in Indiana lakes and reservoirs.Bloomington,Indiana:Indiana University,School of Public and Environmental Affairs,2005.
[5]Fastner J,Heinze R,Humpage AR,Mischke U,Eaglesham GK,Chorus I.Cylindrospermopsin occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii(Cyanobacteria)isolates.Toxicon,2003,42(3):313-321.
[6]Lei LM,Peng L,Huang XH,Han BP.Occurrence and dominance of Cylindrospermopsis raciborskii and dissolved cylindrospermopsin in urban reservoirs used for drinking water supply,South China.Environmental Monitoring and Assessment,2014,186(5):3079-3090.
[7]Svir?ev Z,Obradovi?V,Codd GA,Marjanovi?P,Spoof L,Drobac D,Tokodi N,Petkovi?A,Nenin T,Simeunovi?J,Va?i?T,Meriluoto J.Massive fish mortality and Cylindrospermopsis raciborskii bloom in Aleksandrovac Lake.Ecotoxicology,2016,25(7):1353-1363.
[8]Zanchett G,Oliveira-Filho EC.Cyanobacteria and cyanotoxins:from impacts on aquatic ecosystems and human health to anticarcinogenic effects.Toxins(Basel),2013,5(10):1896-1917.
[9]Moreira C,Fathalli A,Vasconcelos V,Antunes A.Phylogeny and biogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii.Archives of Microbiology,2015,197(1):47-52.
[10]Wood SA,Pochon X,Luttringer-Plu L,Vant BN,Hamilton DP.Recent invader or indicator of environmental change?Aphylogenetic and ecological study of Cylindrospermopsis raciborskii in New Zealand.Harmful Algae,2014,39:64-74.
[11]Burford MA,Beardall J,Willis A,Orr PT,Magalhaes VF,Rangel LM,Azevedo SMFOE,Neilan BA.Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii.Harmful Algae,2016,54:44-53.
[12]Babanazarova OV,Sidelev SI,Fastner J.Northern expansion of Cylindrospermopsis raciborskii(Nostocales,Cyanoprokaryota)observed in shallow highly eutrophic lake Nero(Russia).International Journal on Algae,2014,17(2):131-141.
[13]Pierangelini M,Sinha R,Willis A,Burford MA,Orr PT,Beardall J,Neilan BA.Constitutive cylindrospermopsin pool size in Cylindrospermopsis raciborskii under different light and CO2 partial pressure conditions.Applied and Environmental Microbiology,2015,81(9):3069-3076.
[14]Yang YM,Jiang YG,Li XC,Li H,Chen YX,Xie JL,Cai FF,Li RH.Variations of growth and toxin yield in Cylindrospermopsis raciborskii under different phosphorus concentrations.Toxins,2016,9(1):E13.
[15]Zhang WY,Lou I,Ung WK,Kong YJ,Mok KM.Application of PCR and real-time PCR for monitoring cyanobacteria,Microcystis spp.and Cylindrospermopsis raciborskii in Macau freshwater reservoir.Frontiers of Earth Science,2014,8(2):291-301.
[16]Noyma NP,Silva TP,Chiarini-Garcia H,Amado AM,Roland F,Melo RCN.Potential effects of UV radiation on photosynthetic structures of the bloom-forming cyanobacterium Cylindrospermopsis raciborskii CYRF-01.Frontiers in Microbiology,2015,6:1202.
[17]Beamud G,Vico P,Haakonsson S,de La Escalera GM,Piccini C,Brena BM,Pirez M,Bonilla S.Influence of UV-Bradiation on the fitness and toxin expression of the cyanobacterium Cylindrospermopsis raciborskii.Hydrobiologia,2016,763(1):161-172.
[18]?or?evi?NB,Mati?SLJ,Simi?SB,Stani?SM,Mihailovi?VB,Stankovi?NM,Stankovi?VD,?iri?AR.Impact of the toxicity of Cylindrospermopsis raciborskii(Woloszynska)Seenayya&Subba Raju on laboratory rats in vivo.Environmental Science and Pollution Research,2017,24(16):14259-14272.
[19]Dai JJ,Peng L,Yu T,Lei LM.The effects of phosphorus and nitrogen on the growth of Cylindrospermopsis raciborskii N8 isolated from the Zhenhai Reservoir.Acta Hydrobiologica Sinica,2015,39(3):533-539.(in Chinese)戴景峻,彭亮,于婷,雷腊梅.镇海水库拟柱孢藻的分离鉴定和氮磷对其生长的影响.水生生物学报,2015,39(3):533-539.
[20]Zha GC,Mai XW,Zhou CQ,He JG.Study on the planktonic algae community in low salinity culture ponds of Litopenaeus vannamei.Marine Fisheries Research,2006,27(1):1-7.(in Chinese)查广才,麦雄伟,周昌清,何建国.凡纳滨对虾低盐度养殖池浮游藻类群落研究.海洋水产研究,2006,27(1):1-7.
[21]Nie LH,Li XS,Lin ZS,Liu YQ,Yu J,Zha GC.Biosorption of heavy metals by Cylindrospermopsis raciborskii.Journal of Hydroecology,2017,38(1):41-45.(in Chinese)聂利华,李训仕,林壮森,刘亚群,余俊,查广才.拟柱胞藻对水体重金属的生物富集作用研究.水生态学杂志,2017,38(1):41-45.
[22]Vollmer W,Joris B,Charlier P,Foster S.Bacterial peptidoglycan(murein)hydrolases.FEMS Microbiology Reviews,2008,32(2):259-286.
[23]于婷.温度、光照及氮源对拟柱孢藻生长和藻丝形态的影响.暨南大学硕士学位论文,2014.
[24]Nie LH,Li XS,Liu YQ,Zhu XB,Yu J,Zha GC.Study on the effects of temperature,light intensity,salinity and pH on growth characteristics of freshwater cyanobacteria Cylindrospermopsis raciborskii.Ecological Science,2016,35(4):102-108.(in Chinese)聂利华,李训仕,刘亚群,朱兴彪,余俊,查广才.温度、光照、盐度与pH对淡水蓝藻拟柱胞藻生长的影响.生态科学,2016,35(4):102-108.
[25]Yi TT,Zhi CY,Li PL,Yang YJ,Shuai CY.Effect of Pb2+on the growth of freshwater diatom Nitzschia palea.Jiangsu Agricultural Sciences,2016,44(1):340-343.(in Chinese)易婷婷,支崇远,李培林,杨雨嘉,帅春燕.Pb2+对淡水硅藻谷皮菱形藻(Nitzschia palea)生长的影响.江苏农业科学,2016,44(1):340-343.
[26]Komárek J,Kling H.Variation in six planktonic cyanophyte genera in Lake Victoria(East Africa).Algological Studies,1991,61:21-45.
[27]Saker ML,Neilan BA.Varied diazotrophies,morphologies,and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii(Nostocales,Cyanophyceae)from northern Australia.Applied and Environmental Microbiology,2001,67(4):1839-1845.
[28]Li HM,Pei HY,Sun JM,Jin Y,Xu HZ.Progress and prospect in the study of Cylindrospermopsis raciborskii and its toxins.Journal of Lake Sciences,2017,29(4):775-795.(in Chinese)李红敏,裴海燕,孙炯明,金岩,徐杭州.拟柱孢藻(Cylindrospermopsis raciborskii)及其毒素的研究进展与展望.湖泊科学,2017,29(4):775-795.
[29]Wilson KM,Schembri MA,Baker PD,Saint CP.Molecular characterization of the toxic cyanobacterium Cylindrospermopsis raciborskii and design of a species-specific PCR.Applied and Environmental Microbiology,2000,66(1):332-338.
[30]Zha GC,Zhou CQ,Huang JR,He JG,Mai XW.Studies on the structure and biodiversity of the microplankton community in Litopenaeus vannamai desalination culture ponds.Acta Ecologica Sinica,2004,24(8):1748-1755.(in Chinese)查广才,周昌清,黄建荣,何建国,麦雄伟.凡纳对虾淡化养殖虾池微型浮游生物群落及多样性.生态学报,2004,24(8):1748-1755.
[31]Zha GC.Investigation on the ecological factor in Cylindrospermopsis raciborskii bloom in low salty prawn ponds.Ecological Science,2009,28(4):293-298.(in Chinese)查广才.虾池拟柱胞藻爆发的生态因子调查.生态科学,2009,28(4):293-298.
[32]Willis A,Chuang AW,Woodhouse JN,Neilan BA,Burford MA.Intraspecific variation in growth,morphology and toxin quotas for the cyanobacterium,Cylindrospermopsis raciborskii.Toxicon,2016,119:307-310.
[33]Bittencourt-Oliveira MDC,Moura ADN,Hereman TC,Dantas EW.Increase in straight and coiled Cylindrospermopsis raciborskii(cyanobacteria)populations under conditions of thermal de-stratification in a shallow tropical reservoir.Journal of Water Resource and Protection,2011,3(4):245-252.
[34]Zhao L,Lei LM,Peng L,Han BP.Seasonal dynamic and driving factors of Cylindrospermopsis raciborskii in Zhenhai Reservoir,Guangdong Province.Journal of Lake Sciences,2017,29(1):193-199.(in Chinese)赵莉,雷腊梅,彭亮,韩博平.广东省镇海水库拟柱孢藻(Cylindrospermopsis raciborskii)的季节动态及驱动因子分析.湖泊科学,2017,29(1):193-199.
[35]Chislock MF,Sharp KL,Wilson AE.Cylindrospermopsis raciborskii dominates under very low and high nitrogen-tophosphorus ratios.Water Research,2014,49:207-214.
[36]Dolman AM,Rücker J,Pick FR,Fastner J,Rohrlack T,Mischke U,Wiedner C.Cyanobacteria and cyanotoxins:the Influence of nitrogen versus phosphorus.PLoS One,2012,7(6):e38757.
[37]Yu T,Dai JJ,Lei LM,Peng L.Effects of temperature,irradiance and nitrate on the growth of Cylindrospermopsis raciborskii N8.Journal of Lake Sciences,2014,26(3):441-446.(in Chinese)于婷,戴景峻,雷腊梅,彭亮.温度、光照强度及硝酸盐对拟柱孢藻(Cylindrospermopsis raciborskii N8)生长的影响.湖泊科学,2014,26(3):441-446.
[38]李昊翔.螺旋藻对重金属的耐受性和吸附研究.浙江大学硕士学位论文,2005.
[39]Tonietto AE,Oliveira NL,Lombardi AT,Polpo A.Copper and cadmium complexation by Cylindrospermopsis raciborskii exudate.Water Science&Technology,2016,73(10):2544-2551.
[40]Tonietto AE,Lombardi AT,Vieira AAH,Parrish CC,Choueri RB.Cylindrospermopsis raciborskii(cyanobacteria)exudates:chemical characterization and complexation capacity for Cu,Zn,Cd and Pb.Water Research,2014,49:381-390.
[41]Shan HH,Gao CX.The effects of Cu2+on the growth of spirulina.Environmental Science and Management,2009,34(7):97-99.(in Chinese)单环环,高春晓.铜离子对螺旋藻生长的影响.环境科学与管理,2009,34(7):97-99.
[42]Ran XF,Liu R,Bai F,Shi JQ,Wu ZX.The response on the growth and photosystem II of Microcystis aeruginosa to cadmium,a heavy metal.Acta Hydrobiologica Sinica,2015,39(3):627-632.(in Chinese)冉小飞,刘瑞,白芳,施军琼,吴忠兴.微囊藻生长及光合系统Ⅱ对重金属镉的响应.水生生物学报,2015,39(3):627-632.
[43]Zhang ZN,Cui JS.Effects of Pb2+stress on chlorophy IIfluorescence intensity and ultrastructure of Chlorella pyrenoidosa.Science Technology and Engineering,2015,15(10):131-135.(in Chinese)张展宁,崔建升.Pb2+胁迫对蛋白核小球藻叶绿素荧光强度及亚显微结构的影响.科学技术与工程,2015,15(10):131-135.
[44]Li YY,Zhao N,Li SC,Shao MF,Yu ZY,Qin S.Pb2+impacts on growth of two Spirulina strains.Journal of Biology,2013,30(4):37-41.(in Chinese)李勇勇,赵楠,李善策,邵明飞,郁章玉,秦松.重金属铅离子(Pb2+)对两株螺旋藻生长影响的研究.生物学杂志,2013,30(4):37-41.
[45]Zhi TT,Cheng LH,Xu XH,Zhang L,Chen HL.Advances on heavy metals removal from aqueous solution by algae.Progress in Chemistry,2011,23(8):1782-1794.(in Chinese)支田田,程丽华,徐新华,张林,陈欢林.藻类去除水体中重金属的机理及应用.化学进展,2011,23(8):1782-1794.
[2]Dittmann E,Fewer DP,Neilan BA.Cyanobacterial toxins:biosynthetic routes and evolutionary roots.FEMSMicrobiology Reviews,2013,37(1):23-43.
[3]Vehovszkyá,Kovács AW,Farkas A,Gy?ri J,SzabóH,Vasas G.Pharmacological studies confirm neurotoxic metabolite(s)produced by the bloom-forming Cylindrospermopsis raciborskii in Hungary.Environmental Toxicology,2013,30(5):501-512.
[4]William WJ,Sarah S.Distribution and abundance of Cylindrospermopsis raciborskii in Indiana lakes and reservoirs.Bloomington,Indiana:Indiana University,School of Public and Environmental Affairs,2005.
[5]Fastner J,Heinze R,Humpage AR,Mischke U,Eaglesham GK,Chorus I.Cylindrospermopsin occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii(Cyanobacteria)isolates.Toxicon,2003,42(3):313-321.
[6]Lei LM,Peng L,Huang XH,Han BP.Occurrence and dominance of Cylindrospermopsis raciborskii and dissolved cylindrospermopsin in urban reservoirs used for drinking water supply,South China.Environmental Monitoring and Assessment,2014,186(5):3079-3090.
[7]Svir?ev Z,Obradovi?V,Codd GA,Marjanovi?P,Spoof L,Drobac D,Tokodi N,Petkovi?A,Nenin T,Simeunovi?J,Va?i?T,Meriluoto J.Massive fish mortality and Cylindrospermopsis raciborskii bloom in Aleksandrovac Lake.Ecotoxicology,2016,25(7):1353-1363.
[8]Zanchett G,Oliveira-Filho EC.Cyanobacteria and cyanotoxins:from impacts on aquatic ecosystems and human health to anticarcinogenic effects.Toxins(Basel),2013,5(10):1896-1917.
[9]Moreira C,Fathalli A,Vasconcelos V,Antunes A.Phylogeny and biogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii.Archives of Microbiology,2015,197(1):47-52.
[10]Wood SA,Pochon X,Luttringer-Plu L,Vant BN,Hamilton DP.Recent invader or indicator of environmental change?Aphylogenetic and ecological study of Cylindrospermopsis raciborskii in New Zealand.Harmful Algae,2014,39:64-74.
[11]Burford MA,Beardall J,Willis A,Orr PT,Magalhaes VF,Rangel LM,Azevedo SMFOE,Neilan BA.Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii.Harmful Algae,2016,54:44-53.
[12]Babanazarova OV,Sidelev SI,Fastner J.Northern expansion of Cylindrospermopsis raciborskii(Nostocales,Cyanoprokaryota)observed in shallow highly eutrophic lake Nero(Russia).International Journal on Algae,2014,17(2):131-141.
[13]Pierangelini M,Sinha R,Willis A,Burford MA,Orr PT,Beardall J,Neilan BA.Constitutive cylindrospermopsin pool size in Cylindrospermopsis raciborskii under different light and CO2 partial pressure conditions.Applied and Environmental Microbiology,2015,81(9):3069-3076.
[14]Yang YM,Jiang YG,Li XC,Li H,Chen YX,Xie JL,Cai FF,Li RH.Variations of growth and toxin yield in Cylindrospermopsis raciborskii under different phosphorus concentrations.Toxins,2016,9(1):E13.
[15]Zhang WY,Lou I,Ung WK,Kong YJ,Mok KM.Application of PCR and real-time PCR for monitoring cyanobacteria,Microcystis spp.and Cylindrospermopsis raciborskii in Macau freshwater reservoir.Frontiers of Earth Science,2014,8(2):291-301.
[16]Noyma NP,Silva TP,Chiarini-Garcia H,Amado AM,Roland F,Melo RCN.Potential effects of UV radiation on photosynthetic structures of the bloom-forming cyanobacterium Cylindrospermopsis raciborskii CYRF-01.Frontiers in Microbiology,2015,6:1202.
[17]Beamud G,Vico P,Haakonsson S,de La Escalera GM,Piccini C,Brena BM,Pirez M,Bonilla S.Influence of UV-Bradiation on the fitness and toxin expression of the cyanobacterium Cylindrospermopsis raciborskii.Hydrobiologia,2016,763(1):161-172.
[18]?or?evi?NB,Mati?SLJ,Simi?SB,Stani?SM,Mihailovi?VB,Stankovi?NM,Stankovi?VD,?iri?AR.Impact of the toxicity of Cylindrospermopsis raciborskii(Woloszynska)Seenayya&Subba Raju on laboratory rats in vivo.Environmental Science and Pollution Research,2017,24(16):14259-14272.
[19]Dai JJ,Peng L,Yu T,Lei LM.The effects of phosphorus and nitrogen on the growth of Cylindrospermopsis raciborskii N8 isolated from the Zhenhai Reservoir.Acta Hydrobiologica Sinica,2015,39(3):533-539.(in Chinese)戴景峻,彭亮,于婷,雷腊梅.镇海水库拟柱孢藻的分离鉴定和氮磷对其生长的影响.水生生物学报,2015,39(3):533-539.
[20]Zha GC,Mai XW,Zhou CQ,He JG.Study on the planktonic algae community in low salinity culture ponds of Litopenaeus vannamei.Marine Fisheries Research,2006,27(1):1-7.(in Chinese)查广才,麦雄伟,周昌清,何建国.凡纳滨对虾低盐度养殖池浮游藻类群落研究.海洋水产研究,2006,27(1):1-7.
[21]Nie LH,Li XS,Lin ZS,Liu YQ,Yu J,Zha GC.Biosorption of heavy metals by Cylindrospermopsis raciborskii.Journal of Hydroecology,2017,38(1):41-45.(in Chinese)聂利华,李训仕,林壮森,刘亚群,余俊,查广才.拟柱胞藻对水体重金属的生物富集作用研究.水生态学杂志,2017,38(1):41-45.
[22]Vollmer W,Joris B,Charlier P,Foster S.Bacterial peptidoglycan(murein)hydrolases.FEMS Microbiology Reviews,2008,32(2):259-286.
[23]于婷.温度、光照及氮源对拟柱孢藻生长和藻丝形态的影响.暨南大学硕士学位论文,2014.
[24]Nie LH,Li XS,Liu YQ,Zhu XB,Yu J,Zha GC.Study on the effects of temperature,light intensity,salinity and pH on growth characteristics of freshwater cyanobacteria Cylindrospermopsis raciborskii.Ecological Science,2016,35(4):102-108.(in Chinese)聂利华,李训仕,刘亚群,朱兴彪,余俊,查广才.温度、光照、盐度与pH对淡水蓝藻拟柱胞藻生长的影响.生态科学,2016,35(4):102-108.
[25]Yi TT,Zhi CY,Li PL,Yang YJ,Shuai CY.Effect of Pb2+on the growth of freshwater diatom Nitzschia palea.Jiangsu Agricultural Sciences,2016,44(1):340-343.(in Chinese)易婷婷,支崇远,李培林,杨雨嘉,帅春燕.Pb2+对淡水硅藻谷皮菱形藻(Nitzschia palea)生长的影响.江苏农业科学,2016,44(1):340-343.
[26]Komárek J,Kling H.Variation in six planktonic cyanophyte genera in Lake Victoria(East Africa).Algological Studies,1991,61:21-45.
[27]Saker ML,Neilan BA.Varied diazotrophies,morphologies,and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii(Nostocales,Cyanophyceae)from northern Australia.Applied and Environmental Microbiology,2001,67(4):1839-1845.
[28]Li HM,Pei HY,Sun JM,Jin Y,Xu HZ.Progress and prospect in the study of Cylindrospermopsis raciborskii and its toxins.Journal of Lake Sciences,2017,29(4):775-795.(in Chinese)李红敏,裴海燕,孙炯明,金岩,徐杭州.拟柱孢藻(Cylindrospermopsis raciborskii)及其毒素的研究进展与展望.湖泊科学,2017,29(4):775-795.
[29]Wilson KM,Schembri MA,Baker PD,Saint CP.Molecular characterization of the toxic cyanobacterium Cylindrospermopsis raciborskii and design of a species-specific PCR.Applied and Environmental Microbiology,2000,66(1):332-338.
[30]Zha GC,Zhou CQ,Huang JR,He JG,Mai XW.Studies on the structure and biodiversity of the microplankton community in Litopenaeus vannamai desalination culture ponds.Acta Ecologica Sinica,2004,24(8):1748-1755.(in Chinese)查广才,周昌清,黄建荣,何建国,麦雄伟.凡纳对虾淡化养殖虾池微型浮游生物群落及多样性.生态学报,2004,24(8):1748-1755.
[31]Zha GC.Investigation on the ecological factor in Cylindrospermopsis raciborskii bloom in low salty prawn ponds.Ecological Science,2009,28(4):293-298.(in Chinese)查广才.虾池拟柱胞藻爆发的生态因子调查.生态科学,2009,28(4):293-298.
[32]Willis A,Chuang AW,Woodhouse JN,Neilan BA,Burford MA.Intraspecific variation in growth,morphology and toxin quotas for the cyanobacterium,Cylindrospermopsis raciborskii.Toxicon,2016,119:307-310.
[33]Bittencourt-Oliveira MDC,Moura ADN,Hereman TC,Dantas EW.Increase in straight and coiled Cylindrospermopsis raciborskii(cyanobacteria)populations under conditions of thermal de-stratification in a shallow tropical reservoir.Journal of Water Resource and Protection,2011,3(4):245-252.
[34]Zhao L,Lei LM,Peng L,Han BP.Seasonal dynamic and driving factors of Cylindrospermopsis raciborskii in Zhenhai Reservoir,Guangdong Province.Journal of Lake Sciences,2017,29(1):193-199.(in Chinese)赵莉,雷腊梅,彭亮,韩博平.广东省镇海水库拟柱孢藻(Cylindrospermopsis raciborskii)的季节动态及驱动因子分析.湖泊科学,2017,29(1):193-199.
[35]Chislock MF,Sharp KL,Wilson AE.Cylindrospermopsis raciborskii dominates under very low and high nitrogen-tophosphorus ratios.Water Research,2014,49:207-214.
[36]Dolman AM,Rücker J,Pick FR,Fastner J,Rohrlack T,Mischke U,Wiedner C.Cyanobacteria and cyanotoxins:the Influence of nitrogen versus phosphorus.PLoS One,2012,7(6):e38757.
[37]Yu T,Dai JJ,Lei LM,Peng L.Effects of temperature,irradiance and nitrate on the growth of Cylindrospermopsis raciborskii N8.Journal of Lake Sciences,2014,26(3):441-446.(in Chinese)于婷,戴景峻,雷腊梅,彭亮.温度、光照强度及硝酸盐对拟柱孢藻(Cylindrospermopsis raciborskii N8)生长的影响.湖泊科学,2014,26(3):441-446.
[38]李昊翔.螺旋藻对重金属的耐受性和吸附研究.浙江大学硕士学位论文,2005.
[39]Tonietto AE,Oliveira NL,Lombardi AT,Polpo A.Copper and cadmium complexation by Cylindrospermopsis raciborskii exudate.Water Science&Technology,2016,73(10):2544-2551.
[40]Tonietto AE,Lombardi AT,Vieira AAH,Parrish CC,Choueri RB.Cylindrospermopsis raciborskii(cyanobacteria)exudates:chemical characterization and complexation capacity for Cu,Zn,Cd and Pb.Water Research,2014,49:381-390.
[41]Shan HH,Gao CX.The effects of Cu2+on the growth of spirulina.Environmental Science and Management,2009,34(7):97-99.(in Chinese)单环环,高春晓.铜离子对螺旋藻生长的影响.环境科学与管理,2009,34(7):97-99.
[42]Ran XF,Liu R,Bai F,Shi JQ,Wu ZX.The response on the growth and photosystem II of Microcystis aeruginosa to cadmium,a heavy metal.Acta Hydrobiologica Sinica,2015,39(3):627-632.(in Chinese)冉小飞,刘瑞,白芳,施军琼,吴忠兴.微囊藻生长及光合系统Ⅱ对重金属镉的响应.水生生物学报,2015,39(3):627-632.
[43]Zhang ZN,Cui JS.Effects of Pb2+stress on chlorophy IIfluorescence intensity and ultrastructure of Chlorella pyrenoidosa.Science Technology and Engineering,2015,15(10):131-135.(in Chinese)张展宁,崔建升.Pb2+胁迫对蛋白核小球藻叶绿素荧光强度及亚显微结构的影响.科学技术与工程,2015,15(10):131-135.
[44]Li YY,Zhao N,Li SC,Shao MF,Yu ZY,Qin S.Pb2+impacts on growth of two Spirulina strains.Journal of Biology,2013,30(4):37-41.(in Chinese)李勇勇,赵楠,李善策,邵明飞,郁章玉,秦松.重金属铅离子(Pb2+)对两株螺旋藻生长影响的研究.生物学杂志,2013,30(4):37-41.
[45]Zhi TT,Cheng LH,Xu XH,Zhang L,Chen HL.Advances on heavy metals removal from aqueous solution by algae.Progress in Chemistry,2011,23(8):1782-1794.(in Chinese)支田田,程丽华,徐新华,张林,陈欢林.藻类去除水体中重金属的机理及应用.化学进展,2011,23(8):1782-1794.