Long-and short-chain AHLs affect AOA and AOB microbial community composition and ammonia oxidation rate in activated sludge
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摘要
Quorum sensing(QS)regulation of the composition of ammonia-oxidising archaea(AOA)and ammonia-oxidising bacteria(AOB)communities and functions in wastewater treatment was investigated.Specifically,we explored the role of N-acyl-L-homoserine lactones(AHLs)in microbial community dynamics in activated sludge.On average,the specific ammoniaoxidising-rate increased from 1.6 to 2.8 mg NH_4~+-N/g MLSS/hr after treatment with long-chain AHLs for 16 days,and the addition of AHLs to sludge resulted in an increased number of AOA/AOB amoA genes.Significant differences were observed in the AOA communities of control and AHL-treated cultures,but not the AOB community.Furthermore,the dominant functional AOA strains of the Crenarchaeota altered their ecological niche in response to AHL addition.These results provide evidence that AHLs play an important role in mediating AOA/AOB microbial community parameters and demonstrate the potential for application of QS to the regulation of nitrogen compound metabolism in wastewater treatment.
Quorum sensing(QS)regulation of the composition of ammonia-oxidising archaea(AOA)and ammonia-oxidising bacteria(AOB)communities and functions in wastewater treatment was investigated.Specifically,we explored the role of N-acyl-L-homoserine lactones(AHLs)in microbial community dynamics in activated sludge.On average,the specific ammoniaoxidising-rate increased from 1.6 to 2.8 mg NH_4~+-N/g MLSS/hr after treatment with long-chain AHLs for 16 days,and the addition of AHLs to sludge resulted in an increased number of AOA/AOB amoA genes.Significant differences were observed in the AOA communities of control and AHL-treated cultures,but not the AOB community.Furthermore,the dominant functional AOA strains of the Crenarchaeota altered their ecological niche in response to AHL addition.These results provide evidence that AHLs play an important role in mediating AOA/AOB microbial community parameters and demonstrate the potential for application of QS to the regulation of nitrogen compound metabolism in wastewater treatment.
Quorum sensing(QS)regulation of the composition of ammonia-oxidising archaea(AOA)and ammonia-oxidising bacteria(AOB)communities and functions in wastewater treatment was investigated.Specifically,we explored the role of N-acyl-L-homoserine lactones(AHLs)in microbial community dynamics in activated sludge.On average,the specific ammoniaoxidising-rate increased from 1.6 to 2.8 mg NH_4~+-N/g MLSS/hr after treatment with long-chain AHLs for 16 days,and the addition of AHLs to sludge resulted in an increased number of AOA/AOB amoA genes.Significant differences were observed in the AOA communities of control and AHL-treated cultures,but not the AOB community.Furthermore,the dominant functional AOA strains of the Crenarchaeota altered their ecological niche in response to AHL addition.These results provide evidence that AHLs play an important role in mediating AOA/AOB microbial community parameters and demonstrate the potential for application of QS to the regulation of nitrogen compound metabolism in wastewater treatment.
引文
An,D.,Danhorn,T.,Fuqua,C.,Parsek,M.R.,2006.Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures.Proc.Natl.Acad.Sci.U.S.A.103,3828-3833.
Bassler,B.L.,1999.How bacteria talk to each other:regulation of gene expression by quorum sensing.Curr.Opin.Microbiol.2,582-587.
Batchelor,S.,Cooper,M.,Chhabra,S.,Glover,L.,Stewart,G.,Williams,P.,et al.,1997.Cell density-regulated recovery of starved biofilm populations of ammonia-oxidizing bacteria.Appl.Environ.Microbiol.63,2281-2286.
Berube,P.M.,Stahl,D.A.,2012.The divergent AmoC3 subunit of ammonia monooxygenase functions as part of a stress response system in Nitrosomonas europaea.J.Bacteriol.194,3448-3456.
Bollinger,N.,Hassett,D.J.,Iglewski,B.H.,Costerton,J.W.,McDermott,T.R.,2001.Gene expression in Pseudomonas aeruginosa:evidence of iron override effects on quorum sensing and biofilm-specific gene regulation.J.Bacteriol.183,1990-1996.
Burton,E.,Read,H.,Pellitteri,M.,Hickey,W.,2005.Identification of acyl-homoserine lactone signal molecules produced by Nitrosomonas europaea strain Schmidt.Appl.Environ.Microbiol.71,4906-4909.
Chowdhury,T.R.,Dick,R.P.,2013.Ecology of aerobic methanotrophs in controlling methane fluxes from wetlands.Appl.Soil Ecol.65,8-22.
De Boer,W.,Gunnewiek,K.,Laanbroek,H.,1995.Ammonium-oxidation at low pH by a chemolithotrophic bacterium belonging to the genus Nitrosospira.Soil Biol.Biochem.27,127-132.
De Clippeleir,H.,Defoirdt,T.,Vanhaecke,L.,Vlaeminck,S.E.,Carballa,M.,Verstraete,W.,et al.,2011.Long-chain acylhomoserine lactones increase the anoxic ammonium oxidation rate in an OLAND biofilm.Appl.Microbiol.Biotechnol.90,1511-1519.
Decho,A.W.,Norman,R.S.,Visscher,P.T.,2010.Quorum sensing in natural environments:emerging views from microbial mats.Trends Microbiol.18,73-80.
Diggle,S.P.,Griffin,A.S.,Campbell,G.S.,West,S.A.,2007.Cooperation and conflict in quorum-sensing bacterial populations.Nature 450,411-414.
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.
Fuqua,C.,Parsek,M.R.,Greenberg,E.P.,2001.Regulation of gene expression by cell-to-cell communication:acyl-homoserine lactone quorum sensing.Annu.Rev.Genet.35,439-468.
Gao,J.,Ma,A.,Zhuang,X.,Zhuang,G.,2014.An N-acyl homoserine lactone synthase in the ammonia-oxidizing bacterium Nitrosospira multiformis.Appl.Environ.Microbiol.80,951-958.
Kirisits,M.J.,Margolis,J.J.,Purevdorj-Gage,B.L.,Vaughan,B.,Chopp,D.L.,Stoodley,P.,et al.,2007.Influence of the hydrodynamic environment on quorum sensing in Pseudomonas aeruginosa biofilms.J.Bacteriol.189,8357-8360.
Li,A.J.,Hou,B.L.,Li,M.X.,2015.Cell adhesion,ammonia removal and granulation of autotrophic nitrifying sludge facilitated by N-acyl-homoserine lactones.Bioresour.Technol.196,550-558.
Li,H.,Yang,M.,Zhang,Y.,Yu,T.,Kamagata,Y.,2006.Nitrification performance and microbial community dynamics in a submerged membrane bioreactor with complete sludge retention.J.Biotechnol.123,60-70.
Limpiyakorn,T.,Sonthiphand,P.,Rongsayamanont,C.,Polprasert,C.,2011.Abundance of amoA genes of ammonia-oxidizing archaea and bacteria in activated sludge of full-scale wastewater treatment plants.Bioresour.Technol.102,3694-3701.
Mahmood,S.,Freitag,T.E.,Prosser,J.I.,2006.Comparison of PCRprimer-based strategies for characterization of ammonia oxidizer communities in environmental samples.FEMSMicrobiol.Ecol.56,482-493.
McClean,K.H.,Winson,M.K.,Fish,L.,Taylor,A.,Chhabra,S.R.,Camara,M.,et al.,1997.Quorum sensing and Chromobacterium violaceum:exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones.Microbiology143,3703-3711.
McLean,R.J.C.,Whiteley,M.,Stickler,D.J.,Fuqua,W.C.,1997.Evidence of autoinducer activity in naturally occurring biofilms.FEMS Microbiol.Lett.154,259-263.
Paggi,R.A.,Martone,C.B.,Fuqua,C.,Castro,R.E.,2003.Detection of quorum sensing signals in the haloalkaliphilic archaeon Natronococcus occultus.FEMS Microbiol.Lett.221,49-52.
Park,H.D.,Wells,G.F.,Bae,H.,Criddle,C.S.,Francis,C.A.,2006.Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors.Appl.Environ.Microbiol.72,5643-5647.
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.
Shrout,J.D.,Chopp,D.L.,Just,C.L.,Hentzer,M.,Givskov,M.,Parsek,M.R.,2006.The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional.Mol.Microbiol.62,1264-1277.
Shrout,J.D.,Nerenberg,R.,2012.Monitoring bacterial twitter:does quorum sensing determine the behavior of water and wastewater treatment biofilms?Environ.Sci.Technol.46,1995-2005.
Song,X.N.,Cheng,Y.Y.,Li,W.W.,Li,B.B.,Sheng,G.P.,Fang,C.Y.,et al.,2014.Quorum quenching is responsible for the underestimated quorum sensing effects in biological wastewater treatment reactors.Bioresour.Technol.171,472-476.
Taga,M.E.,Semmelhack,J.L.,Bassler,B.L.,2001.The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium.Mol.Microbiol.42,777-793.
Tan,C.H.,Koh,K.S.,Xie,C.,Tay,M.,Zhou,Y.,Williams,R.,et al.,2014.The role of quorum sensing signalling in EPS production and the assembly of a sludge community into aerobic granules.ISME J.8,1186-1197.
Tan,C.H.,Koh,K.S.,Xie,C.,Zhang,J.,Tan,X.H.,Lee,G.P.,et al.,2015.Community quorum sensing signalling and quenching:microbial granular biofilm assembly.NPJ Biofilms Microbiomes 1,15006.
Valle,A.,Bailey,M.J.,Whiteley,A.S.,Manefield,M.,2004.N-acyl-L-homoserine lactones(AHLs)affect microbial community composition and function in activated sludge.Environ.Microbiol.6,424-433.
Wittebolle,L.,Verstraete,W.,Boon,N.,2009.The inoculum effect on the ammonia-oxidizing bacterial communities in parallel sequential batch reactors.Water Res.43,4149-4158.
Xie,C.,Tan,C.H.,Koh,K.S.,Tay,M.,Williams,R.,Rice,S.A.,et al.,2014.The role of quorum sensing signalling in EPS production and the assembly of a sludge community into aerobic granules.ISME J.8,1186-1197.
Yang,Y.,Shan,J.,Zhang,J.,Zhang,X.,Xie,S.,Liu,Y.,2014.Ammonia-and methane-oxidizing microorganisms in high-altitude wetland sediments and adjacent agricultural soils.Appl.Microbiol.Biotechnol.98,10197-10209.
Zhang,G.,Zhang,F.,Ding,G.,Li,J.,Guo,X.,Zhu,J.,et al.,2012.Acyl homoserine lactone-based quorum sensing in a methanogenic archaeon.ISME J.6,1336-1344.
Bassler,B.L.,1999.How bacteria talk to each other:regulation of gene expression by quorum sensing.Curr.Opin.Microbiol.2,582-587.
Batchelor,S.,Cooper,M.,Chhabra,S.,Glover,L.,Stewart,G.,Williams,P.,et al.,1997.Cell density-regulated recovery of starved biofilm populations of ammonia-oxidizing bacteria.Appl.Environ.Microbiol.63,2281-2286.
Berube,P.M.,Stahl,D.A.,2012.The divergent AmoC3 subunit of ammonia monooxygenase functions as part of a stress response system in Nitrosomonas europaea.J.Bacteriol.194,3448-3456.
Bollinger,N.,Hassett,D.J.,Iglewski,B.H.,Costerton,J.W.,McDermott,T.R.,2001.Gene expression in Pseudomonas aeruginosa:evidence of iron override effects on quorum sensing and biofilm-specific gene regulation.J.Bacteriol.183,1990-1996.
Burton,E.,Read,H.,Pellitteri,M.,Hickey,W.,2005.Identification of acyl-homoserine lactone signal molecules produced by Nitrosomonas europaea strain Schmidt.Appl.Environ.Microbiol.71,4906-4909.
Chowdhury,T.R.,Dick,R.P.,2013.Ecology of aerobic methanotrophs in controlling methane fluxes from wetlands.Appl.Soil Ecol.65,8-22.
De Boer,W.,Gunnewiek,K.,Laanbroek,H.,1995.Ammonium-oxidation at low pH by a chemolithotrophic bacterium belonging to the genus Nitrosospira.Soil Biol.Biochem.27,127-132.
De Clippeleir,H.,Defoirdt,T.,Vanhaecke,L.,Vlaeminck,S.E.,Carballa,M.,Verstraete,W.,et al.,2011.Long-chain acylhomoserine lactones increase the anoxic ammonium oxidation rate in an OLAND biofilm.Appl.Microbiol.Biotechnol.90,1511-1519.
Decho,A.W.,Norman,R.S.,Visscher,P.T.,2010.Quorum sensing in natural environments:emerging views from microbial mats.Trends Microbiol.18,73-80.
Diggle,S.P.,Griffin,A.S.,Campbell,G.S.,West,S.A.,2007.Cooperation and conflict in quorum-sensing bacterial populations.Nature 450,411-414.
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.
Fuqua,C.,Parsek,M.R.,Greenberg,E.P.,2001.Regulation of gene expression by cell-to-cell communication:acyl-homoserine lactone quorum sensing.Annu.Rev.Genet.35,439-468.
Gao,J.,Ma,A.,Zhuang,X.,Zhuang,G.,2014.An N-acyl homoserine lactone synthase in the ammonia-oxidizing bacterium Nitrosospira multiformis.Appl.Environ.Microbiol.80,951-958.
Kirisits,M.J.,Margolis,J.J.,Purevdorj-Gage,B.L.,Vaughan,B.,Chopp,D.L.,Stoodley,P.,et al.,2007.Influence of the hydrodynamic environment on quorum sensing in Pseudomonas aeruginosa biofilms.J.Bacteriol.189,8357-8360.
Li,A.J.,Hou,B.L.,Li,M.X.,2015.Cell adhesion,ammonia removal and granulation of autotrophic nitrifying sludge facilitated by N-acyl-homoserine lactones.Bioresour.Technol.196,550-558.
Li,H.,Yang,M.,Zhang,Y.,Yu,T.,Kamagata,Y.,2006.Nitrification performance and microbial community dynamics in a submerged membrane bioreactor with complete sludge retention.J.Biotechnol.123,60-70.
Limpiyakorn,T.,Sonthiphand,P.,Rongsayamanont,C.,Polprasert,C.,2011.Abundance of amoA genes of ammonia-oxidizing archaea and bacteria in activated sludge of full-scale wastewater treatment plants.Bioresour.Technol.102,3694-3701.
Mahmood,S.,Freitag,T.E.,Prosser,J.I.,2006.Comparison of PCRprimer-based strategies for characterization of ammonia oxidizer communities in environmental samples.FEMSMicrobiol.Ecol.56,482-493.
McClean,K.H.,Winson,M.K.,Fish,L.,Taylor,A.,Chhabra,S.R.,Camara,M.,et al.,1997.Quorum sensing and Chromobacterium violaceum:exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones.Microbiology143,3703-3711.
McLean,R.J.C.,Whiteley,M.,Stickler,D.J.,Fuqua,W.C.,1997.Evidence of autoinducer activity in naturally occurring biofilms.FEMS Microbiol.Lett.154,259-263.
Paggi,R.A.,Martone,C.B.,Fuqua,C.,Castro,R.E.,2003.Detection of quorum sensing signals in the haloalkaliphilic archaeon Natronococcus occultus.FEMS Microbiol.Lett.221,49-52.
Park,H.D.,Wells,G.F.,Bae,H.,Criddle,C.S.,Francis,C.A.,2006.Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors.Appl.Environ.Microbiol.72,5643-5647.
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.
Shrout,J.D.,Chopp,D.L.,Just,C.L.,Hentzer,M.,Givskov,M.,Parsek,M.R.,2006.The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional.Mol.Microbiol.62,1264-1277.
Shrout,J.D.,Nerenberg,R.,2012.Monitoring bacterial twitter:does quorum sensing determine the behavior of water and wastewater treatment biofilms?Environ.Sci.Technol.46,1995-2005.
Song,X.N.,Cheng,Y.Y.,Li,W.W.,Li,B.B.,Sheng,G.P.,Fang,C.Y.,et al.,2014.Quorum quenching is responsible for the underestimated quorum sensing effects in biological wastewater treatment reactors.Bioresour.Technol.171,472-476.
Taga,M.E.,Semmelhack,J.L.,Bassler,B.L.,2001.The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium.Mol.Microbiol.42,777-793.
Tan,C.H.,Koh,K.S.,Xie,C.,Tay,M.,Zhou,Y.,Williams,R.,et al.,2014.The role of quorum sensing signalling in EPS production and the assembly of a sludge community into aerobic granules.ISME J.8,1186-1197.
Tan,C.H.,Koh,K.S.,Xie,C.,Zhang,J.,Tan,X.H.,Lee,G.P.,et al.,2015.Community quorum sensing signalling and quenching:microbial granular biofilm assembly.NPJ Biofilms Microbiomes 1,15006.
Valle,A.,Bailey,M.J.,Whiteley,A.S.,Manefield,M.,2004.N-acyl-L-homoserine lactones(AHLs)affect microbial community composition and function in activated sludge.Environ.Microbiol.6,424-433.
Wittebolle,L.,Verstraete,W.,Boon,N.,2009.The inoculum effect on the ammonia-oxidizing bacterial communities in parallel sequential batch reactors.Water Res.43,4149-4158.
Xie,C.,Tan,C.H.,Koh,K.S.,Tay,M.,Williams,R.,Rice,S.A.,et al.,2014.The role of quorum sensing signalling in EPS production and the assembly of a sludge community into aerobic granules.ISME J.8,1186-1197.
Yang,Y.,Shan,J.,Zhang,J.,Zhang,X.,Xie,S.,Liu,Y.,2014.Ammonia-and methane-oxidizing microorganisms in high-altitude wetland sediments and adjacent agricultural soils.Appl.Microbiol.Biotechnol.98,10197-10209.
Zhang,G.,Zhang,F.,Ding,G.,Li,J.,Guo,X.,Zhu,J.,et al.,2012.Acyl homoserine lactone-based quorum sensing in a methanogenic archaeon.ISME J.6,1336-1344.