Diversity of As Metabolism Functional Genes in Pb-Zn Mine Tailings
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摘要
Microbial activities impact arsenic(As) transformation in mine tailings substantially, yet little is understood on the functional diversity of As metabolism genes. This study explored this issue using a metagenomic approach coupled by a local BLASTN procedure established in our recent studies. An assembled metagenome, recovered from hypersaline and sulfidic mine tailings, was screened for As metabolism genes aio A, arr A, ars C and ars M. This was done using a local BLASTN procedure against databases of the As metabolism genes built in this study. Putative As metabolism genes detected in the assembled metagenome included 11 ars M, 20 ars C and 1 arr A full-length sequences. Together with the rRNA-based phylogenetic profiling results, a picture depicting microbial As cycling in the tailings to the genus level was obtained. It was found that most of the dominant genera in the tailings potentially harboured the genes for As reduction and/or methylation. In particular, a typical pyrite-eater present in the tailings, Thioalkalivibrio sp., was found to harbour not only ars C and ars M, but also arr A. These results highlight the unexpected diversity of As metabolism genes in the tailings, especially considering the extremely low species diversity therein. The microbial As cycling picture established here has potential use for guiding the purposeful manipulation of As biogeochemistry in the tailings.
Microbial activities impact arsenic(As) transformation in mine tailings substantially, yet little is understood on the functional diversity of As metabolism genes. This study explored this issue using a metagenomic approach coupled by a local BLASTN procedure established in our recent studies. An assembled metagenome, recovered from hypersaline and sulfidic mine tailings, was screened for As metabolism genes aio A, arr A, ars C and ars M. This was done using a local BLASTN procedure against databases of the As metabolism genes built in this study. Putative As metabolism genes detected in the assembled metagenome included 11 ars M, 20 ars C and 1 arr A full-length sequences. Together with the rRNA-based phylogenetic profiling results, a picture depicting microbial As cycling in the tailings to the genus level was obtained. It was found that most of the dominant genera in the tailings potentially harboured the genes for As reduction and/or methylation. In particular, a typical pyrite-eater present in the tailings, Thioalkalivibrio sp., was found to harbour not only ars C and ars M, but also arr A. These results highlight the unexpected diversity of As metabolism genes in the tailings, especially considering the extremely low species diversity therein. The microbial As cycling picture established here has potential use for guiding the purposeful manipulation of As biogeochemistry in the tailings.
Microbial activities impact arsenic(As) transformation in mine tailings substantially, yet little is understood on the functional diversity of As metabolism genes. This study explored this issue using a metagenomic approach coupled by a local BLASTN procedure established in our recent studies. An assembled metagenome, recovered from hypersaline and sulfidic mine tailings, was screened for As metabolism genes aio A, arr A, ars C and ars M. This was done using a local BLASTN procedure against databases of the As metabolism genes built in this study. Putative As metabolism genes detected in the assembled metagenome included 11 ars M, 20 ars C and 1 arr A full-length sequences. Together with the rRNA-based phylogenetic profiling results, a picture depicting microbial As cycling in the tailings to the genus level was obtained. It was found that most of the dominant genera in the tailings potentially harboured the genes for As reduction and/or methylation. In particular, a typical pyrite-eater present in the tailings, Thioalkalivibrio sp., was found to harbour not only ars C and ars M, but also arr A. These results highlight the unexpected diversity of As metabolism genes in the tailings, especially considering the extremely low species diversity therein. The microbial As cycling picture established here has potential use for guiding the purposeful manipulation of As biogeochemistry in the tailings.
引文
Anderson G L,Williams J,Hille R.1992.The purification and characterization of arsenite oxidase from Alcaligenes faecalis,a molybdenum-containing hydroxylase.J Biol Chem.267:23674-23682.
Arkesteyn G J M W.1979.Pyrite oxidation by Thiobacillus ferrooxidans with special reference to the sulfur moiety of the mineral.A Van Leeuw J Microb.45:423-435.
Bertin P N,Heinrich-Salmeron A,Pelletier E,Goulhen-Chollet F,Arsène-Ploetze F,Gallien S,Lauga B,Casiot C,Calteau A,Vallenet D,Bonnefoy V,Bruneel O,Chane-Woon-Ming B,Cleiss-Arnold J,Duran R,Elbaz-Poulichet F,Fonknechten N,Giloteaux L,Halter D,Koechler S,Marchal M,Mornico D,Schaeffer C,Smith A A T,Van Dorsselaer A,Weissenbach J,Medigue C,Le Paslier D.2011.Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta-and proteo-genomics.Isme J.5:1735-1747.
Boyd E S,Barkay T.2012.The mercury resistance operon:from an origin in a geothermal environment to an efficient detoxification machine.Front Microbiol.3:349.
Boyle R W,Jonasson I R.1973.The geochemistry of arsenic and its use as an indicator element in geochemical prospecting.J Geochem Explor.2:251-296.
Bublitz M,Morth J P,Nissen P.2011.P-type ATPases at a glance.J Cell Sci.124:2515-2519.
Cai L,Yu K,Yang Y,Chen B W,Li X D,Zhang T.2013.Metagenomic exploration reveals high levels of microbial arsenic metabolism genes in activated sludge and coastal sediments.Appl Microbiol Biot.97:9579-9588.
Chevreux B,Pfisterer T,Drescher B,Driesel A J,Müller W E G,Wetter T,Suhai S.2004.Using the mira EST assembler for reliable and automated m RNA transcript assembly and SNPdetection in sequenced ESTs.Genome Res.14:1147-1159.
Hutchison T C,Meema K M.1987.Lead,Mercury,Cadmium and Arsenic in the Environment.John Wiley&Sons,Chichester,New York,Brisbane,Toronto.
Delcher A L,Bratke K A,Powers E C,Salzberg S L.2007.Identifying bacterial genes and endosymbiont DNA with Glimmer.Bioinformatics.23:673-679.
Dhuldhaj U P,Yadav I C,Singh S,Sharma N K.2013.Microbial interactions in the arsenic cycle:Adoptive strategies and applications in environmental management.Rev Environ Contam T.224:1-38.
Dold B,Fontboté L.2001.Element cycling and secondary mineralogy in porphyry copper tailings as a function of climate,primary mineralogy,and mineral processing.J Geochem Explor.74:3-55.
Fierer N,Leff J W,Adams B J,Nielsen U N,Bates S T,Lauber C L,Owens S,Gilbert J A,Wall D H,Caporaso J G.2012.Cross-biome metagenomic analyses of soil microbial communities and their functional attributes.P Natl Acad Sci USA.109:21390-21395.
Foster A L,Brown G E,Tingle T N,Parks G A.1998.Quantitative arsenic speciation in mine tailings using x-ray absorption spectroscopy.Am Mineral.83:553-568.
Hall T A.1999.Bioedit:A user-friendly biological sequence alignment editor and analysis program for windows 95/98/nt.Nucleic Acids Symposium Ser.41:95-98.
Huang L B,Li X F,Nguyen T A H.2015.Extremely high phosphate sorption capacity in Cu-Pb-Zn mine tailings.PLo SONE.10:e0135364.
Inskeep W P,Macur R E,Hamamura N,Warelow T P,Ward SA,Santini J M.2007.Detection,diversity and expression of aerobic bacterial arsenite oxidase genes.Environ Microbiol.9:934-943.
Jia Y,Huang H,Zhong M,Wang F H,Zhang L M,Zhu Y G.2013.Microbial arsenic methylation in soil and rice rhizosphere.Environ Sci Technol.47:3141-3148.
Jiang H S,Lei R,Ding S W,Zhu S F.2014.Skewer:A fast and accurate adapter trimmer for next-generation sequencing paired-end reads.BMC Bioinform.15:182.
Langhans D,Lord A,Lampshire D,Burbank A,Baglin E.1995.Biooxidation of an arsenic-bearing refractory gold ore.Miner Eng.8:147-158.
Li X,Bond P L,Van Nostrand J D,Zhou J,Huang L.2015a.From lithotroph-to organotroph-dominant:directional shift of microbial community in sulphidic tailings during phytostabilization.Sci Rep.5:12978.
Li X,You F,Huang L,Bond P L.2015b.Establishing microbial diversity and functions in weathered and neutral Cu-Pb-Zn tailings with native soil addition.Geoderma.247-248:108-116.
Li X,Zhu Y-G,Shaban B,Bruxner T J C,Bond P L,Huang L.2015c.Assessing the genetic diversity of Cu resistance in mine tailings through high-throughput recovery of full-length cop A genes.Sci Rep.5:13258.
Li X F,Huang L B.2015.Toward a new paradigm for tailings phytostabilization-nature of the substrates,amendment options,and anthropogenic pedogenesis.Crit Rev Env Sci Tec.45:813-839.
Li X F,Huang L B,Bond P L,Lu Y,Vink S.2014.Bacterial diversity in response to direct revegetation in the Pb-ZnCu tailings under subtropical and semi-arid conditions.Ecol Eng.68:233-240.
Luo J M,Bai Y H,Liang J S,Qu J H.2014.Metagenomic approach reveals variation of microbes with arsenic and antimony metabolism genes from highly contaminated soil.PLo SONE.9:e108185.
Macur R E,Wheeler J T,Mc Dermott T R,Inskeep W P.2001.Microbial populations associated with the reduction and enhanced mobilization of arsenic in mine tailings.Environ Sci Technol.35:3676-3682.
Malasarn D,Keeffe J R,Newman D K.2008.Characterization of the arsenate respiratory reductase from Shewanella sp.strain ANA-3.J Bacteriol.190:135-142.
Malasarn D,Saltikov C W,Campbell K M,Santini J M,Hering J G,Newman D K.2004.arr A is a reliable marker for As(V)respiration.Science.306:455.
Meharg A A,F-J Zhao.2012.Arsenic&Rice.Springer,Dordrecht,Heidelberg,Landon,New York.
Meyer F,Paarmann D,D’Souza M,Olson R,Glass E M,Kubal M,Paczian T,Rodriguez A,Stevens R,Wilke A,Wilkening J,Edwards R A.2008.The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes.BMC Bioinform.9:386.
Mukhopadhyay R,Rosen B P,Phung L T,Silver S.2002.Microbial arsenic:from geocycles to genes and enzymes.FEMSMicrobiol Rev.26:311-325.
Muller D,Simeonova D D,Riegel P,Mangenot S,Koechler S,Lièvremont D,Bertin P N,Lett M C.2006.Herminiimonas arsenicoxydans sp.nov.,a metalloresistant bacterium.Int JSyst Evol Micr.56:1765-1769.
Muyzer G,Sorokin D Y,Mavromatis K,Lapidus A,Foster B,Sun H,Ivanova N,Pati A,D’haeseleer P,Woyke T,Kyrpides N C.2011.Complete genome sequence of Thioalkalivibrio sp.K90mix.Stand Genomic Sci.5:341-355.
National Center for Biotechnology Information(NCBI).2016.Open Reading Frame(ORF)Finder.Available oline at https://www.ncbi.nlm.nih.gov/orffinder/(verified on Aril 18,20-17).
Oremland R S,Kulp T R,Blum J S,Hoeft S E,Baesman S,Miller L G,Stolz J F.2005.A microbial arsenic cycle in a salt-saturated,extreme environment.Science.308:1305-1308.
Robertson L A,Kuenen J G.2006.The genus Thiobacillus.Prokaryotes.5:812-827.
Sentchilo V,Mayer A P,Guy L,Miyazaki R,Tringe S G,Barry K,Malfatti S,Goessmann A,Robinson-Rechavi M,Van der Meer J R.2013.Community-wide plasmid gene mobilization and selection.Isme J.7:1173-1186.
Song B,Chyun E,Jaffé P R,Ward B B.2009.Molecular methods to detect and monitor dissimilatory arsenate-respiring bacteria(DARB)in sediments.FEMS Microbiol Ecol.68:108-117.
Sun Y M,Polishchuk E A,Radoja U,Cullen W R.2004.Identification and quantification of ars C genes in environmental samples by using real-time PCR.J Microbiol Meth.58:335-349.
Tamura K,Stecher G,Peterson D,Filipski A,Kumar S.2013.MEGA6:Molecular evolutionary genetics analysis version6.0.Mol Biol Evol.30:2725-2729.
Warelow T P,Oke M,Schoepp-Cothenet B,Dahl J U,Bruselat N,Sivalingam G N,Leimkühler S,Thalassinos K,Kappler U,Naismith J H,Santini J M.2013.The respiratory arsenite oxidase:Structure and the role of residues surrounding the rieske cluster.PLo S ONE.8:e72535.
Xiao K Q,Li L G,Ma L P,Zhang S Y,Bao P,Zhang T,Zhu YG.2016.Metagenomic analysis revealed highly diverse microbial arsenic metabolism genes in paddy soils with low-arsenic contents.Environ Pollut.211:1-8.
Zhang S-Y,Zhao F-J,Sun G-X,Su J-Q,Yang X-R,Li H,Zhu Y-G.2015.Diversity and abundance of arsenic biotransformation genes in paddy soils from southern China.Environ Sci Technol.49:4138-4146.
Arkesteyn G J M W.1979.Pyrite oxidation by Thiobacillus ferrooxidans with special reference to the sulfur moiety of the mineral.A Van Leeuw J Microb.45:423-435.
Bertin P N,Heinrich-Salmeron A,Pelletier E,Goulhen-Chollet F,Arsène-Ploetze F,Gallien S,Lauga B,Casiot C,Calteau A,Vallenet D,Bonnefoy V,Bruneel O,Chane-Woon-Ming B,Cleiss-Arnold J,Duran R,Elbaz-Poulichet F,Fonknechten N,Giloteaux L,Halter D,Koechler S,Marchal M,Mornico D,Schaeffer C,Smith A A T,Van Dorsselaer A,Weissenbach J,Medigue C,Le Paslier D.2011.Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta-and proteo-genomics.Isme J.5:1735-1747.
Boyd E S,Barkay T.2012.The mercury resistance operon:from an origin in a geothermal environment to an efficient detoxification machine.Front Microbiol.3:349.
Boyle R W,Jonasson I R.1973.The geochemistry of arsenic and its use as an indicator element in geochemical prospecting.J Geochem Explor.2:251-296.
Bublitz M,Morth J P,Nissen P.2011.P-type ATPases at a glance.J Cell Sci.124:2515-2519.
Cai L,Yu K,Yang Y,Chen B W,Li X D,Zhang T.2013.Metagenomic exploration reveals high levels of microbial arsenic metabolism genes in activated sludge and coastal sediments.Appl Microbiol Biot.97:9579-9588.
Chevreux B,Pfisterer T,Drescher B,Driesel A J,Müller W E G,Wetter T,Suhai S.2004.Using the mira EST assembler for reliable and automated m RNA transcript assembly and SNPdetection in sequenced ESTs.Genome Res.14:1147-1159.
Hutchison T C,Meema K M.1987.Lead,Mercury,Cadmium and Arsenic in the Environment.John Wiley&Sons,Chichester,New York,Brisbane,Toronto.
Delcher A L,Bratke K A,Powers E C,Salzberg S L.2007.Identifying bacterial genes and endosymbiont DNA with Glimmer.Bioinformatics.23:673-679.
Dhuldhaj U P,Yadav I C,Singh S,Sharma N K.2013.Microbial interactions in the arsenic cycle:Adoptive strategies and applications in environmental management.Rev Environ Contam T.224:1-38.
Dold B,Fontboté L.2001.Element cycling and secondary mineralogy in porphyry copper tailings as a function of climate,primary mineralogy,and mineral processing.J Geochem Explor.74:3-55.
Fierer N,Leff J W,Adams B J,Nielsen U N,Bates S T,Lauber C L,Owens S,Gilbert J A,Wall D H,Caporaso J G.2012.Cross-biome metagenomic analyses of soil microbial communities and their functional attributes.P Natl Acad Sci USA.109:21390-21395.
Foster A L,Brown G E,Tingle T N,Parks G A.1998.Quantitative arsenic speciation in mine tailings using x-ray absorption spectroscopy.Am Mineral.83:553-568.
Hall T A.1999.Bioedit:A user-friendly biological sequence alignment editor and analysis program for windows 95/98/nt.Nucleic Acids Symposium Ser.41:95-98.
Huang L B,Li X F,Nguyen T A H.2015.Extremely high phosphate sorption capacity in Cu-Pb-Zn mine tailings.PLo SONE.10:e0135364.
Inskeep W P,Macur R E,Hamamura N,Warelow T P,Ward SA,Santini J M.2007.Detection,diversity and expression of aerobic bacterial arsenite oxidase genes.Environ Microbiol.9:934-943.
Jia Y,Huang H,Zhong M,Wang F H,Zhang L M,Zhu Y G.2013.Microbial arsenic methylation in soil and rice rhizosphere.Environ Sci Technol.47:3141-3148.
Jiang H S,Lei R,Ding S W,Zhu S F.2014.Skewer:A fast and accurate adapter trimmer for next-generation sequencing paired-end reads.BMC Bioinform.15:182.
Langhans D,Lord A,Lampshire D,Burbank A,Baglin E.1995.Biooxidation of an arsenic-bearing refractory gold ore.Miner Eng.8:147-158.
Li X,Bond P L,Van Nostrand J D,Zhou J,Huang L.2015a.From lithotroph-to organotroph-dominant:directional shift of microbial community in sulphidic tailings during phytostabilization.Sci Rep.5:12978.
Li X,You F,Huang L,Bond P L.2015b.Establishing microbial diversity and functions in weathered and neutral Cu-Pb-Zn tailings with native soil addition.Geoderma.247-248:108-116.
Li X,Zhu Y-G,Shaban B,Bruxner T J C,Bond P L,Huang L.2015c.Assessing the genetic diversity of Cu resistance in mine tailings through high-throughput recovery of full-length cop A genes.Sci Rep.5:13258.
Li X F,Huang L B.2015.Toward a new paradigm for tailings phytostabilization-nature of the substrates,amendment options,and anthropogenic pedogenesis.Crit Rev Env Sci Tec.45:813-839.
Li X F,Huang L B,Bond P L,Lu Y,Vink S.2014.Bacterial diversity in response to direct revegetation in the Pb-ZnCu tailings under subtropical and semi-arid conditions.Ecol Eng.68:233-240.
Luo J M,Bai Y H,Liang J S,Qu J H.2014.Metagenomic approach reveals variation of microbes with arsenic and antimony metabolism genes from highly contaminated soil.PLo SONE.9:e108185.
Macur R E,Wheeler J T,Mc Dermott T R,Inskeep W P.2001.Microbial populations associated with the reduction and enhanced mobilization of arsenic in mine tailings.Environ Sci Technol.35:3676-3682.
Malasarn D,Keeffe J R,Newman D K.2008.Characterization of the arsenate respiratory reductase from Shewanella sp.strain ANA-3.J Bacteriol.190:135-142.
Malasarn D,Saltikov C W,Campbell K M,Santini J M,Hering J G,Newman D K.2004.arr A is a reliable marker for As(V)respiration.Science.306:455.
Meharg A A,F-J Zhao.2012.Arsenic&Rice.Springer,Dordrecht,Heidelberg,Landon,New York.
Meyer F,Paarmann D,D’Souza M,Olson R,Glass E M,Kubal M,Paczian T,Rodriguez A,Stevens R,Wilke A,Wilkening J,Edwards R A.2008.The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes.BMC Bioinform.9:386.
Mukhopadhyay R,Rosen B P,Phung L T,Silver S.2002.Microbial arsenic:from geocycles to genes and enzymes.FEMSMicrobiol Rev.26:311-325.
Muller D,Simeonova D D,Riegel P,Mangenot S,Koechler S,Lièvremont D,Bertin P N,Lett M C.2006.Herminiimonas arsenicoxydans sp.nov.,a metalloresistant bacterium.Int JSyst Evol Micr.56:1765-1769.
Muyzer G,Sorokin D Y,Mavromatis K,Lapidus A,Foster B,Sun H,Ivanova N,Pati A,D’haeseleer P,Woyke T,Kyrpides N C.2011.Complete genome sequence of Thioalkalivibrio sp.K90mix.Stand Genomic Sci.5:341-355.
National Center for Biotechnology Information(NCBI).2016.Open Reading Frame(ORF)Finder.Available oline at https://www.ncbi.nlm.nih.gov/orffinder/(verified on Aril 18,20-17).
Oremland R S,Kulp T R,Blum J S,Hoeft S E,Baesman S,Miller L G,Stolz J F.2005.A microbial arsenic cycle in a salt-saturated,extreme environment.Science.308:1305-1308.
Robertson L A,Kuenen J G.2006.The genus Thiobacillus.Prokaryotes.5:812-827.
Sentchilo V,Mayer A P,Guy L,Miyazaki R,Tringe S G,Barry K,Malfatti S,Goessmann A,Robinson-Rechavi M,Van der Meer J R.2013.Community-wide plasmid gene mobilization and selection.Isme J.7:1173-1186.
Song B,Chyun E,Jaffé P R,Ward B B.2009.Molecular methods to detect and monitor dissimilatory arsenate-respiring bacteria(DARB)in sediments.FEMS Microbiol Ecol.68:108-117.
Sun Y M,Polishchuk E A,Radoja U,Cullen W R.2004.Identification and quantification of ars C genes in environmental samples by using real-time PCR.J Microbiol Meth.58:335-349.
Tamura K,Stecher G,Peterson D,Filipski A,Kumar S.2013.MEGA6:Molecular evolutionary genetics analysis version6.0.Mol Biol Evol.30:2725-2729.
Warelow T P,Oke M,Schoepp-Cothenet B,Dahl J U,Bruselat N,Sivalingam G N,Leimkühler S,Thalassinos K,Kappler U,Naismith J H,Santini J M.2013.The respiratory arsenite oxidase:Structure and the role of residues surrounding the rieske cluster.PLo S ONE.8:e72535.
Xiao K Q,Li L G,Ma L P,Zhang S Y,Bao P,Zhang T,Zhu YG.2016.Metagenomic analysis revealed highly diverse microbial arsenic metabolism genes in paddy soils with low-arsenic contents.Environ Pollut.211:1-8.
Zhang S-Y,Zhao F-J,Sun G-X,Su J-Q,Yang X-R,Li H,Zhu Y-G.2015.Diversity and abundance of arsenic biotransformation genes in paddy soils from southern China.Environ Sci Technol.49:4138-4146.