Response of ammonia-oxidizing archaea to heavy metal contamination in freshwater sediment
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摘要
It has been well-documented that the distribution of ammonia-oxidizing bacteria(AOB) and archaea(AOA) in soils can be affected by heavy metal contamination, whereas information about the impact of heavy metal on these ammonia-oxidizing microorganisms in freshwater sediment is still lacking. The present study explored the change of sediment ammonia-oxidizing microorganisms in a freshwater reservoir after being accidentally contaminated by industrial discharge containing high levels of metals. Bacterial amoA gene was found to be below the quantitative PCR detection and was not successfully amplified by conventional PCR. The number of archaeal amoA gene in reservoir sediments were 9.62 × 10~2–1.35 × 10~7 copies per gram dry sediment. AOA abundance continuously decreased, and AOA richness, diversity and community structure also considerably varied with time. Therefore, heavy metal pollution could have a profound impact on freshwater sediment AOA community. This work could expand our knowledge of the effect of heavy metal contamination on nitrification in natural ecosystems.
It has been well-documented that the distribution of ammonia-oxidizing bacteria(AOB) and archaea(AOA) in soils can be affected by heavy metal contamination, whereas information about the impact of heavy metal on these ammonia-oxidizing microorganisms in freshwater sediment is still lacking. The present study explored the change of sediment ammonia-oxidizing microorganisms in a freshwater reservoir after being accidentally contaminated by industrial discharge containing high levels of metals. Bacterial amoA gene was found to be below the quantitative PCR detection and was not successfully amplified by conventional PCR. The number of archaeal amoA gene in reservoir sediments were 9.62 × 10~2–1.35 × 10~7 copies per gram dry sediment. AOA abundance continuously decreased, and AOA richness, diversity and community structure also considerably varied with time. Therefore, heavy metal pollution could have a profound impact on freshwater sediment AOA community. This work could expand our knowledge of the effect of heavy metal contamination on nitrification in natural ecosystems.
It has been well-documented that the distribution of ammonia-oxidizing bacteria(AOB) and archaea(AOA) in soils can be affected by heavy metal contamination, whereas information about the impact of heavy metal on these ammonia-oxidizing microorganisms in freshwater sediment is still lacking. The present study explored the change of sediment ammonia-oxidizing microorganisms in a freshwater reservoir after being accidentally contaminated by industrial discharge containing high levels of metals. Bacterial amoA gene was found to be below the quantitative PCR detection and was not successfully amplified by conventional PCR. The number of archaeal amoA gene in reservoir sediments were 9.62 × 10~2–1.35 × 10~7 copies per gram dry sediment. AOA abundance continuously decreased, and AOA richness, diversity and community structure also considerably varied with time. Therefore, heavy metal pollution could have a profound impact on freshwater sediment AOA community. This work could expand our knowledge of the effect of heavy metal contamination on nitrification in natural ecosystems.
引文
Akerblom,S.,Baath,E.,Bringmark,L.,Bringmark,E.,2007.Experimentally induced effects of heavy metal on microbial activity and community structure of forest mor layers.Biol.Fertil.Soils 44,79-91.
Bertagnolli,A.D.,Ulloa,O.,2017.Hydrography shapes community composition and diversity of amoA-containing Thaumarchaeota in the coastal waters off central Chile.Environ.Microbiol.Rep.9,717-728.
Cao,H.L.,Li,M.,Hong,Y.G.,Gu,J.D.,2011.Diversity and abundance of ammonia-oxidizing archaea and bacteria in polluted mangrove sediment.Syst.Appl.Microbiol.34,513-523.
Chen,J.,Bittinger,K.,Charlson,E.S.,Hoffmann,C.,Lewis,J.,Wu,G.D.,et al.,2012.Associating microbiome composition with environmental covariates using generalized UniFrac distances.Bioinformatics 28,2106-2113.
Costa,P.S.,Reis,M.P.,Avila,M.P.,Leite,L.R.,de Araujo,F.M.G.,Salim,A.C.M.,et al.,2015.Metagenome of a microbial community inhabiting a metal-rich tropical stream sediment.PLoS One 10 UNSP e0119465.
Di,H.J.,Cameron,K.C.,Shen,J.P.,Winefield,C.S.,O'Callaghan,M.,Bowatte,S.,et al.,2009.Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils.Nat.Geosci.2,621-624.
Duff,A.M.,Zhang,L.M.,Smith,C.J.,2017.Small-scale variation of ammonia oxidisers within intertidal sediments dominated by ammonia-oxidising bacteria Nitrosomonas sp.amoA genes and transcripts.Sci.Rep.7,13200.
Edgar,R.C.,2013.UPARSE,highly accurate OTU sequences from microbial amplicon reads.Nat.Methods 10,996.
Edgar,R.C.,Haas,B.J.,Clemente,J.C.,Quince,C.,Knight,R.,2011.UCHIME improves sensitivity and speed of chimera detection.Bioinformatics 27,2194-2200.
Erguder,T.H.,Boon,N.,Wittebolle,L.,Marzorati,M.,Verstraete,W.,2009.Environmental actors shaping the ecological niches of ammonia oxidizing archaea.FEMS Microbiol.Rev.33,855-869.
Francis,C.A.,Roberts,K.J.,Beman,J.M.,Santoro,A.E.,Oakley,B.B.,2005.Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean.Proc.Natl.Acad.Sci.U.S.A.102,14683-14688.
Gough,H.L.,Stahl,D.A.,2011.Microbial community structures in anoxic freshwater lake sediment along a metal contamination gradient.ISME J.5,543-558.
Guo,Q.W.,Li,N.N.,Bing,Y.X.,Chen,S.L.,Zhang,Z.K.,Chang,S.,et al.,2018.Denitrifier communities impacted by heavy metal contamination in freshwater sediment.Environ.Pollut.242,426-432.
He,H.,Zhen,Y.,Mi,T.Z.,Lu,X.L.,Yu,Z.G.,2015.Seasonal and spatial distribution of ammonia-oxidizing microorganism communities in surface sediments from the East China Sea.Acta Oceanol.Sin.34,83-92.
He,H.,Zhen,Y.,Mi,T.Z.,Yu,Z.G.,2016.Community composition and abundance of ammonia-oxidizing archaea in sediments from the Changjiang Estuary and its adjacent area in the East China Sea.Geomicrobiol J.33,416-425.
He,H.,Zhen,Y.,Mi,T.Z.,Fu,L.L.,Yu,Z.G.,2018.Ammoniaoxidizing archaea and bacteria differentially contribute to ammonia oxidation in sediments from adjacent waters of Rushan Bay,China.Front.Microbiol.9,116.
Huang,L.Q.,Dong,H.L.,Jiang,H.C.,Wang,S.,Yang,J.,2016a.Relative importance of advective flow versus environmental gradient in shaping aquatic ammonium oxidizers near the Three Gorges Dam of the Yangtze River,China.Environ.Microbiol.Rep.8,667-674.
Huang,R.,Zhao,D.Y.,Zeng,J.,Tian,M.Y.,Shen,F.,Jiang,C.L.,et al.,2016b.Bioturbation of Tubificid worms affects the abundance and community composition of ammonia-oxidizing archaea and bacteria in surface lake sediments.Ann.Microbiol.66,1065-1073.
K?nneke,M.,Bernhard,A.E.,de la Torre,J.R.,Walker,C.B.,Waterbury,J.B.,Stahl,D.A.,2005.Isolation of an autotrophic ammonia-oxidizing marine archaeon.Nature 437,543-546.
Kumar,S.,Stecher,G.,Tamura,K.,2016.MEGA7,Molecular evolutionary genetics analysis version 7.0 for bigger datasets.Mol.Biol.Evol.33,1870-1874.
Letunic,I.,Bork,P.,2016.Interactive tree of life(iTOL)v3,an online tool for the display and annotation of phylogenetic and other trees.Nucleic Acids Res.44,W242-W245.
Li,X.F.,Zhu,Y.G.,Cavagnaro,T.R.,Chen,M.M.,Sun,J.W.,Chen,X.P.,2009.Do ammonia-oxidizing archaea respond to soil Cu contamination similarly as ammonia-oxidizing bacteria?Plant Soil 324,209-217.
Li,M.C.,Wei,G.S.,Shi,W.C.,Sun,Z.T.,Li,H.,Wang,X.Y.,et al.,2018.Distinct distribution patterns of ammonia-oxidizing archaea and bacteria in sediment and water column of the Yellow River estuary.Sci.Rep.8,1584.
Liu,Y.R.,Zheng,Y.M.,Shen,J.P.,Zhang,L.M.,He,J.Z.,2010.Effects of mercury on the activity and community composition of soil ammonia oxidizers.Environ.Sci.Pollut.Res.17,1237-1244.
Liu,Y.,Liu,Y.Z.,Ding,Y.J.,Zheng,J.W.,Zhou,T.,Pan,G.X.,et al.,2014a.Abundance,composition and activity of ammonia oxidizer and denitrifier communities in metal polluted rice paddies from South China.PLoS One 9 UNSP e102000.
Liu,B.,Li,Y.M.,Zhang,J.P.,Zhou,X.H.,Wu,C.D.,2014b.Abundance and diversity of ammonia-oxidizing microorganisms in the sediments of Jinshan Lake.Curr.Microbiol.69,751-757.
Mertens,J.,Broos,K.,Wakelin,S.A.,Kowalchuk,G.A.,Springae,D.,Smolders,E.,2009.Bacteria,not archaea,restore nitrification in a zinc-contaminated soil.ISME J.3,916-923.
Mosier,A.C.,Francis,C.A.,2008.Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary.Environ.Microbiol.10,3002-3016.
Nacke,H.,Schoning,I.,Schindler,M.,Schrumpf,M.,Daniel,R.,Nicol,G.W.,et al.,2017.Links between seawater flooding,soil ammonia oxidiser communities and their response to changes in salinity.FEMS Microbiol.Ecol.93 fix144.
Nunoura,T.,Hirai,M.,Yoshida-Takashima,Y.,Nishizawa,M.,Kawagucci,S.,Yokokawa,T.,et al.,2016.Distribution and niche separation of planktonic microbial communities in the water columns from the surface to the hadal waters of the Japan Trench under the eutrophic ocean.Front.Microbiol.7,1261.
Porat,I.,Vishnivetskaya,T.A.,Mosher,J.J.,Brandt,C.C.,Yang,Z.M.K.,Brooks,S.C.,et al.,2010.Characterization of archaeal community in contaminated and uncontaminated surface stream sediments.Microb.Ecol.60,784-795.
Qin,W.,Heal,K.R.,Ramdasi,R.,Kobelt,J.N.,Martens-Habbena,W.,Bertagnolli,A.D.,et al.,2017.Nitrosopumilus maritimus gen.nov.,sp nov.,Nitrosopumilus cobalaminigenes sp nov.,Nitrosopumilus oxyclinae sp nov.,and Nitrosopumilus ureiphilus sp nov.,four marine ammonia-oxidizing archaea of the phylum Thaumarchaeota.Int.J.Syst.Evol.Microbiol.67,5067-5079.
Rotthauwe,J.H.,Witzel,K.P.,Liesack,W.,1997.The ammonia monooxygenase structural gene amoA as a functional marker,molecular fine-scale analysis of natural ammonia-oxidizing populations.Appl.Environ.Microbiol.63,4704-4712.
Ruyters,S.,Mertens,J.,Springael,D.,Smolders,E.,2010.Stimulated activity of the soil nitrifying community accelerates community adaptation to Zn stress.Soil Biol.Biochem.42,766-772.
Subrahmanyam,G.,Hu,H.W.,Zheng,Y.M.,Archana,G.,He,J.Z.,Liu,Y.R.,2014.Response of ammonia oxidizing microbes to the stresses of arsenic and copper in two acidic alfisols.Appl.Soil Ecol.77,59-67.
Volant,A.,Desoeuvre,A.,Casiot,C.,Lauga,B.,Delpoux,S.,Morin,G.,et al.,2012.Archaeal diversity,temporal variation in the arsenic-rich creek sediments of Carnoules Mine,France.Extremophiles 16,645-657.
Wang,C.,Shan,B.Q.,Zhang,H.,Zhao,Y.,2014a.Limitation of spatial distribution of ammonia-oxidizing microorganisms in the Haihe River,China,by heavy metals.J.Environ.Sci.26,502-511.
Wang,X.Y.,Wang,C.,Bao,L.L.,Xie,S.G.,2014b.Abundance and community structure of ammonia-oxidizing microorganisms in reservoir sediment and adjacent soils.Appl.Microbiol.Biotechnol.98,1883-1892.
Wang,J.H.,Wang,L.J.,Zhu,L.S.,Wang,J.,2018a.Individual and combined effects of enrofloxacin and cadmium on soil microbial biomass and the ammonia-oxidizing functional gene.Sci.Total Environ.624,900-907.
Wang,L.,Wang,J.,Zhu,L.,Wang,J.,2018b.Toxic effects of oxytetracycline and copper,separately or combined,on soil microbial biomasses.Environ.Geochem.Health 40,763-776.
Yang,Y.Y.,Zhang,J.X.,Zhao,Q.,Zhou,Q.H.,Li,N.N.,Wang,Y.L.,et al.,2016.Sediment ammonia-oxidizing microorganisms in two plateau freshwater lakes at different trophic states.Microb.Ecol.71,257-265.
Yin,Y.N.,Song,W.,Gu,J.,Zhang,K.Y.,Qian,X.,Zhang,X.,et al.,2016.Effects of copper on the abundance and diversity of ammonia oxidizers during dairy cattle manure composting.Bioresour.Technol.221,181-187.
Zeng,J.,Zhao,D.Y.,Yu,Z.B.,Huang,R.,Wu,Q.L.L.,2014.Temperature responses of ammonia-oxidizing prokaryotes in freshwater sediment microcosms.PLoS One 9,e100653.
Zhang,M.,Zhu,G.R.,Zhou,M.,Li,H.M.,Lu,Y.W.,Liu,Z.G.,2015.Eutrophication assessment and estimation of water environmental capacity in Lake Xiannv of Jiangxi.Resour.Environ.Yangtze Basin 24,1395-1404.
Zhang,Y.,Chen,L.J.,Sun,R.H.,Dai,T.J.,Tian,J.P.,Zheng,W.,et al.,2016.Population and diversity of ammonia-oxidizing archaea and bacteria in a pollutants'receiving area in Hangzhou Bay.Appl.Microbiol.Biotechnol.100,6035-6045.
Zhang,X.J.,Lin,P.F.,Chen,C.,2017.Emergent water supply in environmental accident of cadmium,thallium and arsenic in Xiannvhu Lake in Xinyu City.China Water Wastewater 33,1-10.
Zhao,K.,Kong,W.D.,Khan,A.,Liu,J.B.,Guo,G.X.,Muhanmmad,S.,et al.,2017.Elevational diversity and distribution of ammonia-oxidizing archaea community in meadow soils on the Tibetan Plateau.Appl.Microbiol.Biotechnol.101,7065-7074.
Zhou,Z.F.,Liu,Y.R.,Sun,G.X.,Zheng,Y.M.,2015.Responses of soil ammonia oxidizers to a short-term severe mercury stress.J.Environ.Sci.38,8-13.
Bertagnolli,A.D.,Ulloa,O.,2017.Hydrography shapes community composition and diversity of amoA-containing Thaumarchaeota in the coastal waters off central Chile.Environ.Microbiol.Rep.9,717-728.
Cao,H.L.,Li,M.,Hong,Y.G.,Gu,J.D.,2011.Diversity and abundance of ammonia-oxidizing archaea and bacteria in polluted mangrove sediment.Syst.Appl.Microbiol.34,513-523.
Chen,J.,Bittinger,K.,Charlson,E.S.,Hoffmann,C.,Lewis,J.,Wu,G.D.,et al.,2012.Associating microbiome composition with environmental covariates using generalized UniFrac distances.Bioinformatics 28,2106-2113.
Costa,P.S.,Reis,M.P.,Avila,M.P.,Leite,L.R.,de Araujo,F.M.G.,Salim,A.C.M.,et al.,2015.Metagenome of a microbial community inhabiting a metal-rich tropical stream sediment.PLoS One 10 UNSP e0119465.
Di,H.J.,Cameron,K.C.,Shen,J.P.,Winefield,C.S.,O'Callaghan,M.,Bowatte,S.,et al.,2009.Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils.Nat.Geosci.2,621-624.
Duff,A.M.,Zhang,L.M.,Smith,C.J.,2017.Small-scale variation of ammonia oxidisers within intertidal sediments dominated by ammonia-oxidising bacteria Nitrosomonas sp.amoA genes and transcripts.Sci.Rep.7,13200.
Edgar,R.C.,2013.UPARSE,highly accurate OTU sequences from microbial amplicon reads.Nat.Methods 10,996.
Edgar,R.C.,Haas,B.J.,Clemente,J.C.,Quince,C.,Knight,R.,2011.UCHIME improves sensitivity and speed of chimera detection.Bioinformatics 27,2194-2200.
Erguder,T.H.,Boon,N.,Wittebolle,L.,Marzorati,M.,Verstraete,W.,2009.Environmental actors shaping the ecological niches of ammonia oxidizing archaea.FEMS Microbiol.Rev.33,855-869.
Francis,C.A.,Roberts,K.J.,Beman,J.M.,Santoro,A.E.,Oakley,B.B.,2005.Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean.Proc.Natl.Acad.Sci.U.S.A.102,14683-14688.
Gough,H.L.,Stahl,D.A.,2011.Microbial community structures in anoxic freshwater lake sediment along a metal contamination gradient.ISME J.5,543-558.
Guo,Q.W.,Li,N.N.,Bing,Y.X.,Chen,S.L.,Zhang,Z.K.,Chang,S.,et al.,2018.Denitrifier communities impacted by heavy metal contamination in freshwater sediment.Environ.Pollut.242,426-432.
He,H.,Zhen,Y.,Mi,T.Z.,Lu,X.L.,Yu,Z.G.,2015.Seasonal and spatial distribution of ammonia-oxidizing microorganism communities in surface sediments from the East China Sea.Acta Oceanol.Sin.34,83-92.
He,H.,Zhen,Y.,Mi,T.Z.,Yu,Z.G.,2016.Community composition and abundance of ammonia-oxidizing archaea in sediments from the Changjiang Estuary and its adjacent area in the East China Sea.Geomicrobiol J.33,416-425.
He,H.,Zhen,Y.,Mi,T.Z.,Fu,L.L.,Yu,Z.G.,2018.Ammoniaoxidizing archaea and bacteria differentially contribute to ammonia oxidation in sediments from adjacent waters of Rushan Bay,China.Front.Microbiol.9,116.
Huang,L.Q.,Dong,H.L.,Jiang,H.C.,Wang,S.,Yang,J.,2016a.Relative importance of advective flow versus environmental gradient in shaping aquatic ammonium oxidizers near the Three Gorges Dam of the Yangtze River,China.Environ.Microbiol.Rep.8,667-674.
Huang,R.,Zhao,D.Y.,Zeng,J.,Tian,M.Y.,Shen,F.,Jiang,C.L.,et al.,2016b.Bioturbation of Tubificid worms affects the abundance and community composition of ammonia-oxidizing archaea and bacteria in surface lake sediments.Ann.Microbiol.66,1065-1073.
K?nneke,M.,Bernhard,A.E.,de la Torre,J.R.,Walker,C.B.,Waterbury,J.B.,Stahl,D.A.,2005.Isolation of an autotrophic ammonia-oxidizing marine archaeon.Nature 437,543-546.
Kumar,S.,Stecher,G.,Tamura,K.,2016.MEGA7,Molecular evolutionary genetics analysis version 7.0 for bigger datasets.Mol.Biol.Evol.33,1870-1874.
Letunic,I.,Bork,P.,2016.Interactive tree of life(iTOL)v3,an online tool for the display and annotation of phylogenetic and other trees.Nucleic Acids Res.44,W242-W245.
Li,X.F.,Zhu,Y.G.,Cavagnaro,T.R.,Chen,M.M.,Sun,J.W.,Chen,X.P.,2009.Do ammonia-oxidizing archaea respond to soil Cu contamination similarly as ammonia-oxidizing bacteria?Plant Soil 324,209-217.
Li,M.C.,Wei,G.S.,Shi,W.C.,Sun,Z.T.,Li,H.,Wang,X.Y.,et al.,2018.Distinct distribution patterns of ammonia-oxidizing archaea and bacteria in sediment and water column of the Yellow River estuary.Sci.Rep.8,1584.
Liu,Y.R.,Zheng,Y.M.,Shen,J.P.,Zhang,L.M.,He,J.Z.,2010.Effects of mercury on the activity and community composition of soil ammonia oxidizers.Environ.Sci.Pollut.Res.17,1237-1244.
Liu,Y.,Liu,Y.Z.,Ding,Y.J.,Zheng,J.W.,Zhou,T.,Pan,G.X.,et al.,2014a.Abundance,composition and activity of ammonia oxidizer and denitrifier communities in metal polluted rice paddies from South China.PLoS One 9 UNSP e102000.
Liu,B.,Li,Y.M.,Zhang,J.P.,Zhou,X.H.,Wu,C.D.,2014b.Abundance and diversity of ammonia-oxidizing microorganisms in the sediments of Jinshan Lake.Curr.Microbiol.69,751-757.
Mertens,J.,Broos,K.,Wakelin,S.A.,Kowalchuk,G.A.,Springae,D.,Smolders,E.,2009.Bacteria,not archaea,restore nitrification in a zinc-contaminated soil.ISME J.3,916-923.
Mosier,A.C.,Francis,C.A.,2008.Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary.Environ.Microbiol.10,3002-3016.
Nacke,H.,Schoning,I.,Schindler,M.,Schrumpf,M.,Daniel,R.,Nicol,G.W.,et al.,2017.Links between seawater flooding,soil ammonia oxidiser communities and their response to changes in salinity.FEMS Microbiol.Ecol.93 fix144.
Nunoura,T.,Hirai,M.,Yoshida-Takashima,Y.,Nishizawa,M.,Kawagucci,S.,Yokokawa,T.,et al.,2016.Distribution and niche separation of planktonic microbial communities in the water columns from the surface to the hadal waters of the Japan Trench under the eutrophic ocean.Front.Microbiol.7,1261.
Porat,I.,Vishnivetskaya,T.A.,Mosher,J.J.,Brandt,C.C.,Yang,Z.M.K.,Brooks,S.C.,et al.,2010.Characterization of archaeal community in contaminated and uncontaminated surface stream sediments.Microb.Ecol.60,784-795.
Qin,W.,Heal,K.R.,Ramdasi,R.,Kobelt,J.N.,Martens-Habbena,W.,Bertagnolli,A.D.,et al.,2017.Nitrosopumilus maritimus gen.nov.,sp nov.,Nitrosopumilus cobalaminigenes sp nov.,Nitrosopumilus oxyclinae sp nov.,and Nitrosopumilus ureiphilus sp nov.,four marine ammonia-oxidizing archaea of the phylum Thaumarchaeota.Int.J.Syst.Evol.Microbiol.67,5067-5079.
Rotthauwe,J.H.,Witzel,K.P.,Liesack,W.,1997.The ammonia monooxygenase structural gene amoA as a functional marker,molecular fine-scale analysis of natural ammonia-oxidizing populations.Appl.Environ.Microbiol.63,4704-4712.
Ruyters,S.,Mertens,J.,Springael,D.,Smolders,E.,2010.Stimulated activity of the soil nitrifying community accelerates community adaptation to Zn stress.Soil Biol.Biochem.42,766-772.
Subrahmanyam,G.,Hu,H.W.,Zheng,Y.M.,Archana,G.,He,J.Z.,Liu,Y.R.,2014.Response of ammonia oxidizing microbes to the stresses of arsenic and copper in two acidic alfisols.Appl.Soil Ecol.77,59-67.
Volant,A.,Desoeuvre,A.,Casiot,C.,Lauga,B.,Delpoux,S.,Morin,G.,et al.,2012.Archaeal diversity,temporal variation in the arsenic-rich creek sediments of Carnoules Mine,France.Extremophiles 16,645-657.
Wang,C.,Shan,B.Q.,Zhang,H.,Zhao,Y.,2014a.Limitation of spatial distribution of ammonia-oxidizing microorganisms in the Haihe River,China,by heavy metals.J.Environ.Sci.26,502-511.
Wang,X.Y.,Wang,C.,Bao,L.L.,Xie,S.G.,2014b.Abundance and community structure of ammonia-oxidizing microorganisms in reservoir sediment and adjacent soils.Appl.Microbiol.Biotechnol.98,1883-1892.
Wang,J.H.,Wang,L.J.,Zhu,L.S.,Wang,J.,2018a.Individual and combined effects of enrofloxacin and cadmium on soil microbial biomass and the ammonia-oxidizing functional gene.Sci.Total Environ.624,900-907.
Wang,L.,Wang,J.,Zhu,L.,Wang,J.,2018b.Toxic effects of oxytetracycline and copper,separately or combined,on soil microbial biomasses.Environ.Geochem.Health 40,763-776.
Yang,Y.Y.,Zhang,J.X.,Zhao,Q.,Zhou,Q.H.,Li,N.N.,Wang,Y.L.,et al.,2016.Sediment ammonia-oxidizing microorganisms in two plateau freshwater lakes at different trophic states.Microb.Ecol.71,257-265.
Yin,Y.N.,Song,W.,Gu,J.,Zhang,K.Y.,Qian,X.,Zhang,X.,et al.,2016.Effects of copper on the abundance and diversity of ammonia oxidizers during dairy cattle manure composting.Bioresour.Technol.221,181-187.
Zeng,J.,Zhao,D.Y.,Yu,Z.B.,Huang,R.,Wu,Q.L.L.,2014.Temperature responses of ammonia-oxidizing prokaryotes in freshwater sediment microcosms.PLoS One 9,e100653.
Zhang,M.,Zhu,G.R.,Zhou,M.,Li,H.M.,Lu,Y.W.,Liu,Z.G.,2015.Eutrophication assessment and estimation of water environmental capacity in Lake Xiannv of Jiangxi.Resour.Environ.Yangtze Basin 24,1395-1404.
Zhang,Y.,Chen,L.J.,Sun,R.H.,Dai,T.J.,Tian,J.P.,Zheng,W.,et al.,2016.Population and diversity of ammonia-oxidizing archaea and bacteria in a pollutants'receiving area in Hangzhou Bay.Appl.Microbiol.Biotechnol.100,6035-6045.
Zhang,X.J.,Lin,P.F.,Chen,C.,2017.Emergent water supply in environmental accident of cadmium,thallium and arsenic in Xiannvhu Lake in Xinyu City.China Water Wastewater 33,1-10.
Zhao,K.,Kong,W.D.,Khan,A.,Liu,J.B.,Guo,G.X.,Muhanmmad,S.,et al.,2017.Elevational diversity and distribution of ammonia-oxidizing archaea community in meadow soils on the Tibetan Plateau.Appl.Microbiol.Biotechnol.101,7065-7074.
Zhou,Z.F.,Liu,Y.R.,Sun,G.X.,Zheng,Y.M.,2015.Responses of soil ammonia oxidizers to a short-term severe mercury stress.J.Environ.Sci.38,8-13.