崇明东滩湿地土壤硝酸盐异化还原成铵过程及其影响因素
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摘要
以崇明东滩湿地为研究对象,采用同位素示踪结合泥浆实验,研究了从低潮滩向高潮滩变化的土壤硝酸盐异化还原成铵过程(DNRA)及其影响因素.结果表明,土壤硝酸盐异化还原成铵的潜在速率为0.17～0.71 nmol·g~(-1)·h~(-1),表现为低潮滩位较高、高潮滩位较低的空间变化特征.相关性分析表明,酸盐异化还原成铵潜在速率与氧化还原电位、可溶性有机碳、硝酸盐和硫化物呈显著相关性.此外,nrfA基因丰度与硝酸盐异化还原成铵潜在速率呈显著相关性.逐步回归分析发现,可溶有机碳和总有机碳是影响硝酸盐异化还原成铵潜在速率和nrfA基因丰度的关键性环境因子,分别贡献了总变异的78.8%和50.3%.通过估算得出,东滩湿地硝酸盐异化还原成铵过程将硝酸盐转化成铵盐的潜力为2.5～10.4 t·km~(-2)·a~(-1),贡献了长江口每年无机氮输入量的0.68%～2.85%,因此,硝酸盐异化还原成铵过程在控制河口湿地氮赋存方面具有着重要的作用.河口潮汐作用导致的湿地环境特征与有机质和硝酸盐含量的变化影响着硝酸盐异化还原成铵过程,进而对河口湿地生态系统中氮动态产生较大的影响.
In this study, nitrogen isotope tracer combined with slurries incubation experiment was used to investigate spatial distribution and associated biogeochemical controls of dissimilatory nitrate reduction to ammonium in the soils ranging from the low to high intertidal sites in Chongming East wetland. The results indicated that the potential rates of dissimilatory nitrate reduction to ammonium(DNRA) were in the range of 0.17～0.71 nmol·g~(-1)·h~(-1). DNRA rates highly varied across the sampling sites, and were generally higher in low intertidal sites, and lower in high intertidal sites. DNRA rates were significantly related to E_h, DOC, NO~-_3, and sulfate, indicating that they crucial factors controlling DNRA activity. In addition, the nrfA abundance showed a strong influence on DNRA rates. Stepwise regression analysis further suggested that DOC and TOC were main factors regulating DNRA rate and nrfA abundance, contributing 78.8% and 50.3% to the total variations, respectively. The amount of nitrate reduction to ammonium performed by DNRA was approximately 2.5～10.4 t ·km~(-2)·a~(-1), accounting for roughly 0.68%～2.85% of total annual inorganic nitrogen flux transported into the Yangtze Estuary, suggesting that DNRA plays a crucial role in controlling the nitrogen fate in estuarine wetland. Overall, these results indicate that the variations in environmental conditions and organic matter and nitrate availability induced by the tidal fluctuation affect DNRA process, which further plays an important role regulating the nitrogen dynamics in estuarine ecosystems.
In this study, nitrogen isotope tracer combined with slurries incubation experiment was used to investigate spatial distribution and associated biogeochemical controls of dissimilatory nitrate reduction to ammonium in the soils ranging from the low to high intertidal sites in Chongming East wetland. The results indicated that the potential rates of dissimilatory nitrate reduction to ammonium(DNRA) were in the range of 0.17～0.71 nmol·g~(-1)·h~(-1). DNRA rates highly varied across the sampling sites, and were generally higher in low intertidal sites, and lower in high intertidal sites. DNRA rates were significantly related to E_h, DOC, NO~-_3, and sulfate, indicating that they crucial factors controlling DNRA activity. In addition, the nrfA abundance showed a strong influence on DNRA rates. Stepwise regression analysis further suggested that DOC and TOC were main factors regulating DNRA rate and nrfA abundance, contributing 78.8% and 50.3% to the total variations, respectively. The amount of nitrate reduction to ammonium performed by DNRA was approximately 2.5～10.4 t ·km~(-2)·a~(-1), accounting for roughly 0.68%～2.85% of total annual inorganic nitrogen flux transported into the Yangtze Estuary, suggesting that DNRA plays a crucial role in controlling the nitrogen fate in estuarine wetland. Overall, these results indicate that the variations in environmental conditions and organic matter and nitrate availability induced by the tidal fluctuation affect DNRA process, which further plays an important role regulating the nitrogen dynamics in estuarine ecosystems.
引文
An S,Gardner W S.2002.Dissimilatory nitrate reduction to ammonium (DNRA) as a nitrogen link versus denitrification as a sink in a shallow estuary (Laguna Madre/Baffin Bay,Texas)[J].Marine Ecology Progress Series,237:41-50
Cao W Z,Yang J X,Li Y,et al.2016.Dissimilatory nitrate reduction to ammonium conserves N in an anthropogenically impacted sub-tropical mangrove sediments,Southeast China[J].Marine Pollution Bulletin,110:155-161
Christensen P B,Rysgaard S,Sloth N P,et al.2000.Sediment mineralization,nutrient fluxes,denitrification and dissimilatory nitrate reduction to ammonium in an estuarine Fjord with Sea Cage Trout Farms[J].Aquatic Microbial Ecology,21:73-84
Crowe S A,Canfield D E,Sundby B,et al.2012.Anammox,denitrification and fixed-nitrogen removal in sediments from the Lower St.Lawrence Estuary[J].Biogeosciences,9:4309-4321
Dahnke K,Bahlmann E,Emeis K.2008.A nitrate sink in estuaries? An assessment by means of stable nitrate isotopes in the Elbe estuary[J].Limnology Oceanography,53:1504-1511
Deek A,Emeis K,Van Beusekom J.2012.Nitrogen removal in coastal sediments of the German Wadden Sea[J].Biogeochemistry,108:467-483
Deng F Y,Hou LJ,Liu M,et al.2015.Dissimilatory nitrate reduction processes and associated contribution to nitrogen removal in sediments of the Yangtze Estuary[J].Journal of Geophysical Research:Biogeosciences,120(8):1521-1531
Dhakal P,Matocha C J,Huggins F E,et al.2013.Nitrite reactivity with magnetite[J].Environmental Science and Technology,47:6206-6213
Dong L F,Smith C J,Papaspyrou S,et al.2009.Changes in benthic denitrification,nitrate ammonification,and anammox process rates and nitrate and nitrite reductase gene abundances along an estuarine nutrient gradient (the Colne Estuary,United Kingdom)[J].Applied and Environmental Microbiology,75(10):3171-3179
Dong L F,Sobey M N,Smith C,et al.2011.Dissimilatory reduction of nitrate to ammonium (DNRA) not denitrification or anammox dominates benthic nitrate reduction in tropical estuaries[J].Limnology and Oceanography,56:279-291
Gardner W S,Mccarthy M J,An S,et al.2006.Nitrogen ?xation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries[J].Limnology and Oceanography,51:558-568
Giblin A E,Tobias C R,Song B K,et al.2013.The importance of dissimilatory nitrate reduction to ammonium (DNRA) in the nitrogen cycle of coastal ecosystems[J].Oceanography,26(3):124-131
高灯州,曾从盛,章文龙,等.2016.水淹频率增加对闽江口湿地土壤有机碳及其活性组分的影响[J].环境科学学报,36(3):974-980
侯翠翠,宋长春,李英臣,等.2012.不同水分条件沼泽湿地土壤轻组有机碳与微生物活性动态[J].中国环境科学,32(1):113-119
黄佳芳,倪进治,仝川,等.2015.闽江口半咸水沼泽湿地土壤甲烷产生过程及硫酸盐还原对其抑制作用研究[J].环境科学学报,35(3):862-872
Hardison A K,Algar C K,Giblin A E,et al.2015.Influence of organic carbon and nitrate loading on partitioning between dissimilatory nitrate reduction to ammonium (DNRA) and N2 production[J].Geochimica et Cosmochimica Acta,164:146-160
Hou L J,Zheng Y L,Liu M,et al.2013.Anaerobic ammonium oxidation (anammox) bacterial diversity,abundance,and activity in marsh sediments of the Yangtze Estuary[J].Journal of Geophysical Research:Biogeosciences,118:1237-1246
Howarth R,Chan F,Conley D J,et al.2011.Coupled biogeochemical cycles:eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems[J].Frontiers Ecology Environment,9:18-26
Ikenaga M,Guevara R,Dean A L,et al.2010.Changes in community structure of sediment bacteria along the Florida coastal everglades marsh-mangrove-seagrass salinity gradient[J].Microbial Ecology,59(2):284-295
Kreiling R M,Richardson W B,Cavanaugh J C,et al.2011.Summer nitrate uptake and denitrification in an upper Mississippi River backwater lake:the role of rooted aquatic vegetation[J].Biogeochemistry,104:309-324
Laverman A M,Canavan R W,Slomp C P,et al.2007.Potential nitrate removal in a coastal freshwater sediment (Haringvliet Lake,The Netherlands) and response to salinization[J].Water Research,41(14):3061-3068
李家兵,汪旭明,谢蓉蓉,等.2017.闽江口互花米草入侵过程对短叶茳芏沼泽沉积物硝化-反硝化作用的影响[J].环境科学学报,37(3):1065-1073
李小飞,林贤彪,程吕,等.2015.崇明东滩沉积物胞外酶活性与温室气体排放潜力及其影响因素[J].水土保持学报,29(3):202-207
Li X F,Hou L J,Liu M,et al.2015a.Evidence of nitrogen loss from anaerobic ammonium oxidation coupled with ferric iron reduction in an intertidal wetland[J].Environmental Science & Technology 49:11560-11568
Li X F,Hou L J,Liu M,et al.2015b.Primary effects of extracellular enzyme activity and microbial community carbon and nitrogen mineralization in estuarine and tidal wetlands[J].Applied Microbiology and Biotechnology,99(6):2895-2909
Liu J P,Xu K H,Li A C,et al.,2007.Flux and fate of Yangtze River sediment delivered to the East China Sea[J].Geomorphology,85(3/4):208-224
Lovley D R,Phillips E J P.1987.Rapid assay for microbially reducible ferric iron in aquatic sediments[J].Applied and Environmental Microbiology,53:1536-1540
Lunau M,Voss M,Erickson M,et al.2013.Excess nitrate loads to coastal waters reduces nitrate removal efficiency:mechanism and implications for coastal eutrophication[J].Environmental Microbiology,15(5):1492-1504
Morrissey E M,Gillespie J L,Morina J C,et al.2014.Salinity affects microbial activity and soil organic matter content in tidal wetlands[J].Global Change Biology,20:1351-1362
Nizzoli D,Carraro E,Nigro V,et al.2010.Effect of organic enrichment and thermal regime on denitrification and dissimilatory nitrate reduction to ammonium(DNRA) in hypolimnetic sediments of two lowland lakes[J].Water Research,44:2715-2724
Plummer P,Tobias C,Cady D.2015.Nitrogen reduction pathways in estuarine sediments:Influences of organic carbon and sulfide[J].Journal of Geophysical Research:Biogeosciences,120(10):1958-1972
Roberts K L,Velasquez L E,Joye S B.2014.Increased rates of dissimilatory nitrate reduction to ammonium (DNRA) under oxic conditions in a periodically hypoxic estuary[J].Geochimica et Cosmochimica Acta,133:313-324
Robertson E K,Roberts K L,Burdorf L D,et al.2016.Dissimilatory nitrate reduction to ammonium coupled to Fe (II) oxidation in sediments of a periodically hypoxic estuary[J].Limnology and Oceanography,61(1):365-381
Santoro A E.2010.Microbial nitrogen cycling at the saltwater–freshwater interface[J].Hydrogeology Journal,18(1):187-202
She C X,Zhang Z C, Cadillo-Quiroz H,et al.2016.Factors regulating community composition of methanogens and sulfate-reducing bacteria in brackish marsh sediments in the Min River estuary,southeastern China[J].Estuarine Coastal and Shelf Science,181:27-38
Smith C J,Nedwell D B,Dong L F,et al.2007.Diversity and abundance of nitrate reductase genes (narG and napA),nitrite reductase genes (nirS and nrfA),and their transcripts in estuarine sediments[J].Applied and Environmental Microbiology,73:3612-3622
Spohn M,Babka B,Giani L.2013.Changes in soil organic matter quality during sea-influenced marsh soil development at the North Sea coast[J].Catena,107:110-117
陶怡乐,温东辉.2016.细菌硝酸盐异化还原成铵过程及其在河口生态系统中的潜在地位与影响[J].微生物学通报,43(1):172-181
Tang Y S,Wang L,Jia J W,et al.2011.Response of soil microbial respiration of tidal wetlands in the Yangtze River Estuary to different artificial disturbances[J].Ecological Engineering,37:1638-1646
Vance E D,Brookes P C,Jenkinson D S.1987.An extraction method for measuring soil microbial biomass C[J].Soil Biology and Biochemistry,19:703-707
Vieira F C B,Bayer C,Zanatta J A,et al.2007.Carbon management index based on physical fractionation of soil organic matter in an Acrisol under long-term no-till cropping systems[J].Soil & Tillage Research,96:195-204
Wang S Y,Zhu G B,Peng Y Z,et al.2012.Anammox bacterial abundance,activity,and contribution in riparian sediments of the Pear River Estuary[J].Environmental Science and Technology,46:8834-8842
汪旭明,任洪昌,李家兵,等.2015.河口区淡水和微咸水潮汐沼泽湿地沉积物反硝化作用[J].环境科学学报,35(12):3917-3926
王纯,刘兴土,仝川,等.2017.水盐梯度对闽江河口湿地土壤有机碳组分的影响[J].中国环境科学,37(10):3919-3928
徐继荣,王友绍,殷建平,等.2005.珠江口入海河段DIN形态转化与硝化和反硝化作用[J].环境科学学报,25(5):686-692
盂宪民.1999.湿地与全球环境变化[J].地理科学,19(5):385-391
Yin G Y,Hou L J,Liu M,et al.2014.A novel membrane inlet mass spectrometer method to measure 15NH+4 for isotope-enrichment experiments in aquatic ecosystems[J].Environmental Science & Technology,48(16):9555-9562
Zhou M,Butterbach-Bahl K,Vereecken H,et al.2017.A meta-analysis of soil salinization effects on nitrogen pools,cycles and fluxes in coastal ecosystems[J].Global Change Biology,23(3):1338-1352
Cao W Z,Yang J X,Li Y,et al.2016.Dissimilatory nitrate reduction to ammonium conserves N in an anthropogenically impacted sub-tropical mangrove sediments,Southeast China[J].Marine Pollution Bulletin,110:155-161
Christensen P B,Rysgaard S,Sloth N P,et al.2000.Sediment mineralization,nutrient fluxes,denitrification and dissimilatory nitrate reduction to ammonium in an estuarine Fjord with Sea Cage Trout Farms[J].Aquatic Microbial Ecology,21:73-84
Crowe S A,Canfield D E,Sundby B,et al.2012.Anammox,denitrification and fixed-nitrogen removal in sediments from the Lower St.Lawrence Estuary[J].Biogeosciences,9:4309-4321
Dahnke K,Bahlmann E,Emeis K.2008.A nitrate sink in estuaries? An assessment by means of stable nitrate isotopes in the Elbe estuary[J].Limnology Oceanography,53:1504-1511
Deek A,Emeis K,Van Beusekom J.2012.Nitrogen removal in coastal sediments of the German Wadden Sea[J].Biogeochemistry,108:467-483
Deng F Y,Hou LJ,Liu M,et al.2015.Dissimilatory nitrate reduction processes and associated contribution to nitrogen removal in sediments of the Yangtze Estuary[J].Journal of Geophysical Research:Biogeosciences,120(8):1521-1531
Dhakal P,Matocha C J,Huggins F E,et al.2013.Nitrite reactivity with magnetite[J].Environmental Science and Technology,47:6206-6213
Dong L F,Smith C J,Papaspyrou S,et al.2009.Changes in benthic denitrification,nitrate ammonification,and anammox process rates and nitrate and nitrite reductase gene abundances along an estuarine nutrient gradient (the Colne Estuary,United Kingdom)[J].Applied and Environmental Microbiology,75(10):3171-3179
Dong L F,Sobey M N,Smith C,et al.2011.Dissimilatory reduction of nitrate to ammonium (DNRA) not denitrification or anammox dominates benthic nitrate reduction in tropical estuaries[J].Limnology and Oceanography,56:279-291
Gardner W S,Mccarthy M J,An S,et al.2006.Nitrogen ?xation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries[J].Limnology and Oceanography,51:558-568
Giblin A E,Tobias C R,Song B K,et al.2013.The importance of dissimilatory nitrate reduction to ammonium (DNRA) in the nitrogen cycle of coastal ecosystems[J].Oceanography,26(3):124-131
高灯州,曾从盛,章文龙,等.2016.水淹频率增加对闽江口湿地土壤有机碳及其活性组分的影响[J].环境科学学报,36(3):974-980
侯翠翠,宋长春,李英臣,等.2012.不同水分条件沼泽湿地土壤轻组有机碳与微生物活性动态[J].中国环境科学,32(1):113-119
黄佳芳,倪进治,仝川,等.2015.闽江口半咸水沼泽湿地土壤甲烷产生过程及硫酸盐还原对其抑制作用研究[J].环境科学学报,35(3):862-872
Hardison A K,Algar C K,Giblin A E,et al.2015.Influence of organic carbon and nitrate loading on partitioning between dissimilatory nitrate reduction to ammonium (DNRA) and N2 production[J].Geochimica et Cosmochimica Acta,164:146-160
Hou L J,Zheng Y L,Liu M,et al.2013.Anaerobic ammonium oxidation (anammox) bacterial diversity,abundance,and activity in marsh sediments of the Yangtze Estuary[J].Journal of Geophysical Research:Biogeosciences,118:1237-1246
Howarth R,Chan F,Conley D J,et al.2011.Coupled biogeochemical cycles:eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems[J].Frontiers Ecology Environment,9:18-26
Ikenaga M,Guevara R,Dean A L,et al.2010.Changes in community structure of sediment bacteria along the Florida coastal everglades marsh-mangrove-seagrass salinity gradient[J].Microbial Ecology,59(2):284-295
Kreiling R M,Richardson W B,Cavanaugh J C,et al.2011.Summer nitrate uptake and denitrification in an upper Mississippi River backwater lake:the role of rooted aquatic vegetation[J].Biogeochemistry,104:309-324
Laverman A M,Canavan R W,Slomp C P,et al.2007.Potential nitrate removal in a coastal freshwater sediment (Haringvliet Lake,The Netherlands) and response to salinization[J].Water Research,41(14):3061-3068
李家兵,汪旭明,谢蓉蓉,等.2017.闽江口互花米草入侵过程对短叶茳芏沼泽沉积物硝化-反硝化作用的影响[J].环境科学学报,37(3):1065-1073
李小飞,林贤彪,程吕,等.2015.崇明东滩沉积物胞外酶活性与温室气体排放潜力及其影响因素[J].水土保持学报,29(3):202-207
Li X F,Hou L J,Liu M,et al.2015a.Evidence of nitrogen loss from anaerobic ammonium oxidation coupled with ferric iron reduction in an intertidal wetland[J].Environmental Science & Technology 49:11560-11568
Li X F,Hou L J,Liu M,et al.2015b.Primary effects of extracellular enzyme activity and microbial community carbon and nitrogen mineralization in estuarine and tidal wetlands[J].Applied Microbiology and Biotechnology,99(6):2895-2909
Liu J P,Xu K H,Li A C,et al.,2007.Flux and fate of Yangtze River sediment delivered to the East China Sea[J].Geomorphology,85(3/4):208-224
Lovley D R,Phillips E J P.1987.Rapid assay for microbially reducible ferric iron in aquatic sediments[J].Applied and Environmental Microbiology,53:1536-1540
Lunau M,Voss M,Erickson M,et al.2013.Excess nitrate loads to coastal waters reduces nitrate removal efficiency:mechanism and implications for coastal eutrophication[J].Environmental Microbiology,15(5):1492-1504
Morrissey E M,Gillespie J L,Morina J C,et al.2014.Salinity affects microbial activity and soil organic matter content in tidal wetlands[J].Global Change Biology,20:1351-1362
Nizzoli D,Carraro E,Nigro V,et al.2010.Effect of organic enrichment and thermal regime on denitrification and dissimilatory nitrate reduction to ammonium(DNRA) in hypolimnetic sediments of two lowland lakes[J].Water Research,44:2715-2724
Plummer P,Tobias C,Cady D.2015.Nitrogen reduction pathways in estuarine sediments:Influences of organic carbon and sulfide[J].Journal of Geophysical Research:Biogeosciences,120(10):1958-1972
Roberts K L,Velasquez L E,Joye S B.2014.Increased rates of dissimilatory nitrate reduction to ammonium (DNRA) under oxic conditions in a periodically hypoxic estuary[J].Geochimica et Cosmochimica Acta,133:313-324
Robertson E K,Roberts K L,Burdorf L D,et al.2016.Dissimilatory nitrate reduction to ammonium coupled to Fe (II) oxidation in sediments of a periodically hypoxic estuary[J].Limnology and Oceanography,61(1):365-381
Santoro A E.2010.Microbial nitrogen cycling at the saltwater–freshwater interface[J].Hydrogeology Journal,18(1):187-202
She C X,Zhang Z C, Cadillo-Quiroz H,et al.2016.Factors regulating community composition of methanogens and sulfate-reducing bacteria in brackish marsh sediments in the Min River estuary,southeastern China[J].Estuarine Coastal and Shelf Science,181:27-38
Smith C J,Nedwell D B,Dong L F,et al.2007.Diversity and abundance of nitrate reductase genes (narG and napA),nitrite reductase genes (nirS and nrfA),and their transcripts in estuarine sediments[J].Applied and Environmental Microbiology,73:3612-3622
Spohn M,Babka B,Giani L.2013.Changes in soil organic matter quality during sea-influenced marsh soil development at the North Sea coast[J].Catena,107:110-117
陶怡乐,温东辉.2016.细菌硝酸盐异化还原成铵过程及其在河口生态系统中的潜在地位与影响[J].微生物学通报,43(1):172-181
Tang Y S,Wang L,Jia J W,et al.2011.Response of soil microbial respiration of tidal wetlands in the Yangtze River Estuary to different artificial disturbances[J].Ecological Engineering,37:1638-1646
Vance E D,Brookes P C,Jenkinson D S.1987.An extraction method for measuring soil microbial biomass C[J].Soil Biology and Biochemistry,19:703-707
Vieira F C B,Bayer C,Zanatta J A,et al.2007.Carbon management index based on physical fractionation of soil organic matter in an Acrisol under long-term no-till cropping systems[J].Soil & Tillage Research,96:195-204
Wang S Y,Zhu G B,Peng Y Z,et al.2012.Anammox bacterial abundance,activity,and contribution in riparian sediments of the Pear River Estuary[J].Environmental Science and Technology,46:8834-8842
汪旭明,任洪昌,李家兵,等.2015.河口区淡水和微咸水潮汐沼泽湿地沉积物反硝化作用[J].环境科学学报,35(12):3917-3926
王纯,刘兴土,仝川,等.2017.水盐梯度对闽江河口湿地土壤有机碳组分的影响[J].中国环境科学,37(10):3919-3928
徐继荣,王友绍,殷建平,等.2005.珠江口入海河段DIN形态转化与硝化和反硝化作用[J].环境科学学报,25(5):686-692
盂宪民.1999.湿地与全球环境变化[J].地理科学,19(5):385-391
Yin G Y,Hou L J,Liu M,et al.2014.A novel membrane inlet mass spectrometer method to measure 15NH+4 for isotope-enrichment experiments in aquatic ecosystems[J].Environmental Science & Technology,48(16):9555-9562
Zhou M,Butterbach-Bahl K,Vereecken H,et al.2017.A meta-analysis of soil salinization effects on nitrogen pools,cycles and fluxes in coastal ecosystems[J].Global Change Biology,23(3):1338-1352
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