珠江口异养细菌时空分布特征及其调控机制
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摘要
河口是海陆相互作用的重要地带,往往呈现出独特的生物地球化学过程,是研究碳循环过程的重要场所。在春季(2015年5月)、夏季(2015年8月)和冬季(2016年1月)分别对珠江口海域异养附生细菌和游离细菌时空分布及其各自高核酸(HNA)、低核酸(LNA)类群的相对贡献进行了调查研究,并对其调控因子进行了相应探讨。结果表明,珠江口异养细菌分布具有明显的时空差异。空间分布上,珠江口异养细菌丰度自河口上游至下游呈递减趋势,主要与上游污水输入以及珠江径流与高盐外海水在河口内的混合有关;在雨季,河口中下游盐度锋面区出现异养细菌丰度和叶绿素a质量浓度的高值区,锋面区使营养物质停留时间增加,促进浮游生物生长。垂直方向上,表层异养细菌丰度略高于底层。时间尺度上,异养细菌总丰度在春季最高(表层均值为2.94±1.23×10~9个×L~(-1),底层为2.81±1.50×10~9个×L~(-1)),夏季次之(表层均值为2.32±0.43×10~9个×L~(-1),底层为1.90±0.50×10~9个×L~(-1)),冬季最低(表层均值为1.06±0.33×10~9个×L~(-1),底层为9.76±3.44×108个×L~(-1))。珠江口海域异养细菌以附生细菌为主,占异养细菌总丰度的16.56%~96.19%,整体分布较稳定,冬季最高(平均78.65%)、夏季(70.32%)与春季相近(68.17%)。附生细菌以代谢活跃的HNA类群为主,游离细菌则主要以LNA类群为主,代谢活性整体相对较低。
Estuaries are important land-sea interaction zones with unique biogeochemical processes and are important places to study the carbon cycle. Little is known on bacterial regulation in carbon cycling in the Pearl River Estuary. To examine the relative contribution of different groups of heterotrophic bacteria(particle-attached bacteria vs free-living bacteria, and high nucleic acid bacteria vs low nucleic acid bacteria), spatial and temporal variation in heterotrophic bacterial abundance was investigated during three contrasting periods(May 2015, August 2015 and January 2016) in the Pearl River Estuary. The total bacterial abundance was the highest in spring(an average of 2.94±1.30×10~9 cells ×L~(-1) at the surface and 2.81±1.50×10~9 cells ×L~(-1) at the bottom), moderate in summer(2.32±0.43×10~9 cells ×L~(-1) at the surface and 1.85±0.50×10~9 cells ×L~(-1) at the bottom), and the lowest in winter(1.06±0.33×10~9 cells ×L~(-1) at the surface and 9.76±3.44×108 cells ×L~(-1) at the bottom). Bacterial abundance at the surface was slightly higher than that at the bottom. Bacterial abundance decreased spatially from the upstream to the downstream of the estuary, suggesting that sewage input contributed to high bacterial abundance in the upstream, and that the downstream decrease resulted from the mixing of river discharge and seawater. The peaks of bacterial abundance and Chl a were observed at the frontal zone in the wet season, since a front increased the residence time of nutrients and plankton, and favored plankton growth. According to the spatial variation trend of bacterial abundance, it could be inferred that the heterotrophic bacteria of the estuary mainly came from upstream inputs. Heterotrophic bacterial communities were dominated by particle-attached bacteria, which accounted for 78.65%, 70.32% and 68.17% of the total bacterial abundance in spring, summer and winter, respectively. The metabolically active bacteria with high nucleic acid dominated in the particle-attached bacteria, while the low nucleic acid group was the dominant component of the free-living bacteria.
Estuaries are important land-sea interaction zones with unique biogeochemical processes and are important places to study the carbon cycle. Little is known on bacterial regulation in carbon cycling in the Pearl River Estuary. To examine the relative contribution of different groups of heterotrophic bacteria(particle-attached bacteria vs free-living bacteria, and high nucleic acid bacteria vs low nucleic acid bacteria), spatial and temporal variation in heterotrophic bacterial abundance was investigated during three contrasting periods(May 2015, August 2015 and January 2016) in the Pearl River Estuary. The total bacterial abundance was the highest in spring(an average of 2.94±1.30×10~9 cells ×L~(-1) at the surface and 2.81±1.50×10~9 cells ×L~(-1) at the bottom), moderate in summer(2.32±0.43×10~9 cells ×L~(-1) at the surface and 1.85±0.50×10~9 cells ×L~(-1) at the bottom), and the lowest in winter(1.06±0.33×10~9 cells ×L~(-1) at the surface and 9.76±3.44×108 cells ×L~(-1) at the bottom). Bacterial abundance at the surface was slightly higher than that at the bottom. Bacterial abundance decreased spatially from the upstream to the downstream of the estuary, suggesting that sewage input contributed to high bacterial abundance in the upstream, and that the downstream decrease resulted from the mixing of river discharge and seawater. The peaks of bacterial abundance and Chl a were observed at the frontal zone in the wet season, since a front increased the residence time of nutrients and plankton, and favored plankton growth. According to the spatial variation trend of bacterial abundance, it could be inferred that the heterotrophic bacteria of the estuary mainly came from upstream inputs. Heterotrophic bacterial communities were dominated by particle-attached bacteria, which accounted for 78.65%, 70.32% and 68.17% of the total bacterial abundance in spring, summer and winter, respectively. The metabolically active bacteria with high nucleic acid dominated in the particle-attached bacteria, while the low nucleic acid group was the dominant component of the free-living bacteria.
引文
张霞,黄小平,施震,等,2012.珠江口异养细菌丰度与环境因子的耦合关系[J].海洋学报,34(6):228-237.ZHANG XIA,HUANG XIAOPING,SHI ZHEN,et al,2012.Coupling of heterotrophic bacteria abundance and environmental variables of the Zhujiang(Pearl)River Estuary[J].Acta Oceanologica Sinica,34(6):228-237(in Chinese with English abstract).
郑天凌,王海黎,洪华生,1994.微生物在碳的海洋生物地球化学循环中的作用[J].生态学杂志,13(4):47-50.ZHENGTIANLIN,WANG HAILI,HONG HUASHENG,1994.Role of microorganisms in biogeochemical cycling of carbon in oceans[J].Chinese Journal of Ecology,13(4):47-50(in Chinese with English abstract).
ACINAS S G,ANTóN J,RODRíGUEZ-VALERA F,1999.Diversity of free-living and attached bacteria in offshore Western Mediterranean waters as depicted by analysis of genes encoding 16S r RNA[J].Applied and Environmental Microbiology,65(2):514-522.
AZAM F,FENCHEL T,FIELD J G,et al,1983.The ecological role of water-column microbes in the sea[J].Marine Ecology Progress Series,10(3):257-263.
CAI WEIJUN,2011.Estuarine and coastal ocean carbon paradox:CO2 sinks or sites of terrestrial carbon incineration?[J].Annual Review of Marine Science,3(3):123-145.
CARON D A,DAVIS P G,MADIN L P,et al,1982.Heterotrophic bacteria and bacterivorous protozoa in oceanic macroaggregates[J].Science,218(4574):795-797.
CHERRIER J,BAUER J E,DRUFFEL E R M,1996.Utilization and turnover of labile dissolved organic matter by bacterial heterotrophs in eastern north Pacific surface waters[J].Marine Ecology Progress Series,139:267-279.
CRUMP B C,BAROSS J A,1996.Particle-attached bacteria and heterotrophic plankton associated with the Columbia River estuarine turbidity maxima[J].Marine Ecology Progress Series,138:265-273.
CRUMP B C,BAROSS J A,SIMENSTAD C A,1998.Dominance of particle-attached bacteria in the Columbia River estuary,USA[J].Aquatic Microbial Ecology,14(1):7-18.
CRUMP B C,ARMBRUST E V,BAROSS J A,1999.Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia river,its estuary,and the adjacent coastal ocean[J].Applied and Environmental Microbiology,65(7):3192-3204.
CRUMP B C,BAROSS J A,2000.Characterization of the bacterially-active particle fraction in the Columbia River estuary[J].Marine Ecology Progress Series,206:13-22.
DAGG M,BENNER R,LOHRENZ S,et al,2004.Transformation of dissolved and particulate materials on continental shelves influenced by large rivers:plume processes[J].Continental Shelf Research,24(7/8):833-858.
DUCKLOW H,2000.Bacterial Production and biomass in the oceans[M]//KIRCHMANN D L.Microbial Ecology of the Oceans.New York:Wiley:85-120.
FUHRMAN J,1992.Bacterioplankton roles in cycling of organic matter:the microbial food web[M]//FALKOWSKIAVRIL P G,WOODHEAD A D,VIVIRITO K.Primary Productivity and Biogeochemical Cycles in the Sea.New York:Plenum Press:361-383.
FUHRMAN J A,AZAM F,1982.Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters:evaluation and field results[J].Marine Biology,66(2):109-120.
FUHRMAN J A,STEELE J A,HEWSON I,et al,2008.Alatitudinal diversity gradient in planktonic marine bacteria[J].Proceedings of the National Academy of Sciences of the United States of America,105(22):7774-7778.
GARNEAU Mè,VINCENT W F,TERRADO R,et al,2009.Importance of particle-associated bacterial heterotrophy in a coastal Arctic ecosystem[J].Journal of Marine Systems,75(1/2):185-197.
GASOL J M,ZWEIFEL U L,PETERS F,et al,1999.Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria[J].Applied and Environmental Microbiology,65(10):4475-4483.
GRASSHOFF K,KREMLING K,EHRHARDT M,1999.Methods of seawater analysis[M].3rd ed.Weinheim:WILEY-VCHVerlag Gmb H:159-226.
HARRISON P J,YIN KEDONG,LEE J H W,et al,2008.Physical-biological coupling in the Pearl River Estuary[J].Continental Shelf Research,28(12):1405-1415.
IRIBERRI J,UNANUE M,BARCINA I,et al,1987.Seasonal variation in population density and heterotrophic activity of attached and free-living bacteria in coastal waters[J].Applied and Environmental Microbiology,53(10):2308-2314.
JELLETT J F,LI W K W,DICKIE P M,et al,1996.Metabolic activity of bacterioplankton communities assessed by flow cytometry and single carbon substrate utilization[J].Marine Ecology Progress Series,136:213-225.
KNAP A,MICHAELS A,CLOSE A,et al,1996.Protocols for the joint global ocean flux study(JGOFS)core measurements[R].JGOFS Report No.19,vi+170pp.Reprint of the IOC Manuals and Guides No.29.Paris:UNESCO.
LAMONTAGNE M G,HOLDEN P A,2003.Comparison of free-living and particle-associated bacterial communities in a coastal Lagoon[J].Microbial Ecology,46(2):228-237.
LAPOUSSIèRE A,MICHEL C,STARR M,et al,2011.Role of free-living and particle-attached bacteria in the recycling and export of organic material in the Hudson Bay system[J].Journal of Marine Systems,88(3):434-445.
LEBARON P,SERVAIS P,BAUDOUX A C,et al,2002.Variations of bacterial-specific activity with cell size and nucleic acid content assessed by flow cytometry[J].Aquatic Microbial Ecology,28(2):131-140.
LIU HONGBIN,DAGG M,CAMPBELL L,et al,2004.Picophytoplankton and bacterioplankton in the Mississippi River plume and its adjacent waters[J].Estuaries,27(1):147-156.
MARIE D,PARTENSKY F,JACQUET S,et al,1997.Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I[J].Applied and Environmental Microbiology,63(1):186-193.
MORàN X A G,DUCKLOW H W,ERICKSON M,2011.Single-cell physiological structure and growth rates of heterotrophic bacteria in a temperate estuary(Waquoit Bay,Massachusetts)[J].Limnology and Oceanography,56(1):37-48.
NI ZHIXIN,HUANG XIAOPING,ZHANG XIA,2015.Picoplankton and virioplankton abundance and community structure in Pearl River Estuary and Daya Bay,South China[J].Journal of Environmental Sciences,32:146-154.
PAKULSKI J D,BENNER R,WHITLEDGE T,et al,2000.Microbial metabolism and nutrient cycling in the Mississippi and Atchafalaya River plumes[J].Estuarine,Coastal and Shelf Science,50(2):173-184.
POMEROY L R,WIEBE W J,DEIBEL D,et al,1991.Bacterial responses to temperature and substrate concentration during the Newfoundland spring bloom[J].Marine Ecology Progress Series,75:143-159.
ROBINSON C,WILLIAMS P J I,2005.Respiration and its measurements in surface marine waters[M]//GIORRGIO P A,WILLIAM P J B.Respiration in Aquatic Ecosystems.3rd ed.New York:Oxford University Press:147-180.
SHIAH F K,DUKLOW H W,1994.Temperature and substrate regulation of bacterial abundance,production and specific growth rate in Chesapeake Bay,USA[J].Marine Ecology Progress Series,103:297-308.
SHIAH F K,GONG G C,CHEN C C,2003.Seasonal and spatial variation of bacterial production in the continental shelf of the East China Sea:possible controlling mechanisms and potential roles in carbon cycling[J].Deep Sea Research PartⅡ:Topical Studies in Oceanography,50(6/7):1295-1309.
SIMON M,GROSSART H P,SCHWEITZER B,et al,2002.Microbial ecology of organic aggregates in aquatic ecosystems[J].Aquatic Microbial Ecology,28(2):175-211.
VREDE K,2005.Nutrient and temperature limitation of bacterioplankton growth in temperate lakes[J].Microbial Ecology,49(2):245-256.
XU JIE,JING HONGMEI,SUN MINGMING,et al,2013.Regulation of bacterial metabolic activity by dissolved organic carbon and viruses[J].Journal of Geophysical Research:Biogeosciences,118(4):1573-1583.
YIN KEDONG,QIAN PEIYUAN,CHEN J C,et al,2000.Dynamics of nutrients and phytoplankton biomass in the Pearl River estuary and adjacent waters of Hong Kong during summer:preliminary evidence for phosphorus and silicon limitation[J].Marine Ecology Progress Series,194:295-305.
YIN KEDONG,QIAN PEIYUAN,WU M C S,et al,2001.Shift from P to N limitation of phytoplankton growth across the Pearl River estuarine plume during summer[J].Marine Ecology Progress Series,221:17-28.
YUAN XIANGCHENG,HE LEI,YIN KEDDONG,et al,2011.Bacterial distribution and nutrient limitation in relation to different water masses in the coastal and northwestern South China Sea in late summer[J].Continental Shelf Research,31(11):1214-1223.
ZHANG RUI,LIU BAOZHONG,LAU S C K,et al,2007.Particle-attached and free-living bacterial communities in a contrasting marine environment:Victoria Harbor,Hong Kong[J].FEMS Microbiology Ecology,61(3):496-508.
ZHANG XIA,SHI ZHEN,LIU QINGXIA,et al,2013.Spatial and temporal variations of picoplankton in three contrasting periods in the Pearl River Estuary,South China[J].Continental Shelf Research,56:1-12.
ZHOU WEIHUA,LONG AIMIN,JIANG TAO,et al,2011.Bacterioplankton dynamics along the gradient from highly eutrophic Pearl River Estuary to oligotrophic northern South China Sea in wet season:implication for anthropogenic inputs[J].Marine Pollution Bulletin,62(4):726-733.
郑天凌,王海黎,洪华生,1994.微生物在碳的海洋生物地球化学循环中的作用[J].生态学杂志,13(4):47-50.ZHENGTIANLIN,WANG HAILI,HONG HUASHENG,1994.Role of microorganisms in biogeochemical cycling of carbon in oceans[J].Chinese Journal of Ecology,13(4):47-50(in Chinese with English abstract).
ACINAS S G,ANTóN J,RODRíGUEZ-VALERA F,1999.Diversity of free-living and attached bacteria in offshore Western Mediterranean waters as depicted by analysis of genes encoding 16S r RNA[J].Applied and Environmental Microbiology,65(2):514-522.
AZAM F,FENCHEL T,FIELD J G,et al,1983.The ecological role of water-column microbes in the sea[J].Marine Ecology Progress Series,10(3):257-263.
CAI WEIJUN,2011.Estuarine and coastal ocean carbon paradox:CO2 sinks or sites of terrestrial carbon incineration?[J].Annual Review of Marine Science,3(3):123-145.
CARON D A,DAVIS P G,MADIN L P,et al,1982.Heterotrophic bacteria and bacterivorous protozoa in oceanic macroaggregates[J].Science,218(4574):795-797.
CHERRIER J,BAUER J E,DRUFFEL E R M,1996.Utilization and turnover of labile dissolved organic matter by bacterial heterotrophs in eastern north Pacific surface waters[J].Marine Ecology Progress Series,139:267-279.
CRUMP B C,BAROSS J A,1996.Particle-attached bacteria and heterotrophic plankton associated with the Columbia River estuarine turbidity maxima[J].Marine Ecology Progress Series,138:265-273.
CRUMP B C,BAROSS J A,SIMENSTAD C A,1998.Dominance of particle-attached bacteria in the Columbia River estuary,USA[J].Aquatic Microbial Ecology,14(1):7-18.
CRUMP B C,ARMBRUST E V,BAROSS J A,1999.Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia river,its estuary,and the adjacent coastal ocean[J].Applied and Environmental Microbiology,65(7):3192-3204.
CRUMP B C,BAROSS J A,2000.Characterization of the bacterially-active particle fraction in the Columbia River estuary[J].Marine Ecology Progress Series,206:13-22.
DAGG M,BENNER R,LOHRENZ S,et al,2004.Transformation of dissolved and particulate materials on continental shelves influenced by large rivers:plume processes[J].Continental Shelf Research,24(7/8):833-858.
DUCKLOW H,2000.Bacterial Production and biomass in the oceans[M]//KIRCHMANN D L.Microbial Ecology of the Oceans.New York:Wiley:85-120.
FUHRMAN J,1992.Bacterioplankton roles in cycling of organic matter:the microbial food web[M]//FALKOWSKIAVRIL P G,WOODHEAD A D,VIVIRITO K.Primary Productivity and Biogeochemical Cycles in the Sea.New York:Plenum Press:361-383.
FUHRMAN J A,AZAM F,1982.Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters:evaluation and field results[J].Marine Biology,66(2):109-120.
FUHRMAN J A,STEELE J A,HEWSON I,et al,2008.Alatitudinal diversity gradient in planktonic marine bacteria[J].Proceedings of the National Academy of Sciences of the United States of America,105(22):7774-7778.
GARNEAU Mè,VINCENT W F,TERRADO R,et al,2009.Importance of particle-associated bacterial heterotrophy in a coastal Arctic ecosystem[J].Journal of Marine Systems,75(1/2):185-197.
GASOL J M,ZWEIFEL U L,PETERS F,et al,1999.Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria[J].Applied and Environmental Microbiology,65(10):4475-4483.
GRASSHOFF K,KREMLING K,EHRHARDT M,1999.Methods of seawater analysis[M].3rd ed.Weinheim:WILEY-VCHVerlag Gmb H:159-226.
HARRISON P J,YIN KEDONG,LEE J H W,et al,2008.Physical-biological coupling in the Pearl River Estuary[J].Continental Shelf Research,28(12):1405-1415.
IRIBERRI J,UNANUE M,BARCINA I,et al,1987.Seasonal variation in population density and heterotrophic activity of attached and free-living bacteria in coastal waters[J].Applied and Environmental Microbiology,53(10):2308-2314.
JELLETT J F,LI W K W,DICKIE P M,et al,1996.Metabolic activity of bacterioplankton communities assessed by flow cytometry and single carbon substrate utilization[J].Marine Ecology Progress Series,136:213-225.
KNAP A,MICHAELS A,CLOSE A,et al,1996.Protocols for the joint global ocean flux study(JGOFS)core measurements[R].JGOFS Report No.19,vi+170pp.Reprint of the IOC Manuals and Guides No.29.Paris:UNESCO.
LAMONTAGNE M G,HOLDEN P A,2003.Comparison of free-living and particle-associated bacterial communities in a coastal Lagoon[J].Microbial Ecology,46(2):228-237.
LAPOUSSIèRE A,MICHEL C,STARR M,et al,2011.Role of free-living and particle-attached bacteria in the recycling and export of organic material in the Hudson Bay system[J].Journal of Marine Systems,88(3):434-445.
LEBARON P,SERVAIS P,BAUDOUX A C,et al,2002.Variations of bacterial-specific activity with cell size and nucleic acid content assessed by flow cytometry[J].Aquatic Microbial Ecology,28(2):131-140.
LIU HONGBIN,DAGG M,CAMPBELL L,et al,2004.Picophytoplankton and bacterioplankton in the Mississippi River plume and its adjacent waters[J].Estuaries,27(1):147-156.
MARIE D,PARTENSKY F,JACQUET S,et al,1997.Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I[J].Applied and Environmental Microbiology,63(1):186-193.
MORàN X A G,DUCKLOW H W,ERICKSON M,2011.Single-cell physiological structure and growth rates of heterotrophic bacteria in a temperate estuary(Waquoit Bay,Massachusetts)[J].Limnology and Oceanography,56(1):37-48.
NI ZHIXIN,HUANG XIAOPING,ZHANG XIA,2015.Picoplankton and virioplankton abundance and community structure in Pearl River Estuary and Daya Bay,South China[J].Journal of Environmental Sciences,32:146-154.
PAKULSKI J D,BENNER R,WHITLEDGE T,et al,2000.Microbial metabolism and nutrient cycling in the Mississippi and Atchafalaya River plumes[J].Estuarine,Coastal and Shelf Science,50(2):173-184.
POMEROY L R,WIEBE W J,DEIBEL D,et al,1991.Bacterial responses to temperature and substrate concentration during the Newfoundland spring bloom[J].Marine Ecology Progress Series,75:143-159.
ROBINSON C,WILLIAMS P J I,2005.Respiration and its measurements in surface marine waters[M]//GIORRGIO P A,WILLIAM P J B.Respiration in Aquatic Ecosystems.3rd ed.New York:Oxford University Press:147-180.
SHIAH F K,DUKLOW H W,1994.Temperature and substrate regulation of bacterial abundance,production and specific growth rate in Chesapeake Bay,USA[J].Marine Ecology Progress Series,103:297-308.
SHIAH F K,GONG G C,CHEN C C,2003.Seasonal and spatial variation of bacterial production in the continental shelf of the East China Sea:possible controlling mechanisms and potential roles in carbon cycling[J].Deep Sea Research PartⅡ:Topical Studies in Oceanography,50(6/7):1295-1309.
SIMON M,GROSSART H P,SCHWEITZER B,et al,2002.Microbial ecology of organic aggregates in aquatic ecosystems[J].Aquatic Microbial Ecology,28(2):175-211.
VREDE K,2005.Nutrient and temperature limitation of bacterioplankton growth in temperate lakes[J].Microbial Ecology,49(2):245-256.
XU JIE,JING HONGMEI,SUN MINGMING,et al,2013.Regulation of bacterial metabolic activity by dissolved organic carbon and viruses[J].Journal of Geophysical Research:Biogeosciences,118(4):1573-1583.
YIN KEDONG,QIAN PEIYUAN,CHEN J C,et al,2000.Dynamics of nutrients and phytoplankton biomass in the Pearl River estuary and adjacent waters of Hong Kong during summer:preliminary evidence for phosphorus and silicon limitation[J].Marine Ecology Progress Series,194:295-305.
YIN KEDONG,QIAN PEIYUAN,WU M C S,et al,2001.Shift from P to N limitation of phytoplankton growth across the Pearl River estuarine plume during summer[J].Marine Ecology Progress Series,221:17-28.
YUAN XIANGCHENG,HE LEI,YIN KEDDONG,et al,2011.Bacterial distribution and nutrient limitation in relation to different water masses in the coastal and northwestern South China Sea in late summer[J].Continental Shelf Research,31(11):1214-1223.
ZHANG RUI,LIU BAOZHONG,LAU S C K,et al,2007.Particle-attached and free-living bacterial communities in a contrasting marine environment:Victoria Harbor,Hong Kong[J].FEMS Microbiology Ecology,61(3):496-508.
ZHANG XIA,SHI ZHEN,LIU QINGXIA,et al,2013.Spatial and temporal variations of picoplankton in three contrasting periods in the Pearl River Estuary,South China[J].Continental Shelf Research,56:1-12.
ZHOU WEIHUA,LONG AIMIN,JIANG TAO,et al,2011.Bacterioplankton dynamics along the gradient from highly eutrophic Pearl River Estuary to oligotrophic northern South China Sea in wet season:implication for anthropogenic inputs[J].Marine Pollution Bulletin,62(4):726-733.