Shifts in community structure and function of ammoniaoxidizing archaea in biological soil crusts along a revegetation chronosequence in the Tengger Desert
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摘要
Metagenomic studies have demonstrated the existence of ammonia-oxidizing archaea(AOA) and revealed they are responsible for ammoxidation in some extreme environments. However, the changes in compositional structure and ammonia-oxidation capacity of AOA communities in biological soil crusts(BSCs) of desert ecosystems remain poorly understood.Here, we utilized Illumina MiSeq sequencing and microbial functional gene array(GeoChip 5.0) to assess the above changes along a 51-year revegetation chronosequence in the Tengger Desert, China. The results showed a significant difference in AOA-community richness between 5-year-old BSCs and older ones. The most dominant phylum during BSC development was Crenarchaeota, and the corresponding species were ammonia-oxidizing_Crenarchaeote and environmental_samples_Crenarchaeota. Network analysis revealed that the positive correlations among dominant taxa increased, and their cooperation was reinforced in AOA communities during BSC succession. Redundancy analysis showed that the dominant factor influencing the change in AOA-community structure was soil texture. GeoChip 5.0 indicated that the amoA gene abundances of AOA and ammonia-oxidizing bacteria(AOB) were basically the same, demonstrating that AOA and AOB played an equally important role during BSCs development. Our study of the long-term succession of BSC demonstrated a persistent response of AOA communities to revegetation development in desert ecosystems.
Metagenomic studies have demonstrated the existence of ammonia-oxidizing archaea(AOA) and revealed they are responsible for ammoxidation in some extreme environments. However, the changes in compositional structure and ammonia-oxidation capacity of AOA communities in biological soil crusts(BSCs) of desert ecosystems remain poorly understood.Here, we utilized Illumina MiSeq sequencing and microbial functional gene array(GeoChip 5.0) to assess the above changes along a 51-year revegetation chronosequence in the Tengger Desert, China. The results showed a significant difference in AOA-community richness between 5-year-old BSCs and older ones. The most dominant phylum during BSC development was Crenarchaeota, and the corresponding species were ammonia-oxidizing_Crenarchaeote and environmental_samples_Crenarchaeota. Network analysis revealed that the positive correlations among dominant taxa increased, and their cooperation was reinforced in AOA communities during BSC succession. Redundancy analysis showed that the dominant factor influencing the change in AOA-community structure was soil texture. GeoChip 5.0 indicated that the amoA gene abundances of AOA and ammonia-oxidizing bacteria(AOB) were basically the same, demonstrating that AOA and AOB played an equally important role during BSCs development. Our study of the long-term succession of BSC demonstrated a persistent response of AOA communities to revegetation development in desert ecosystems.
Metagenomic studies have demonstrated the existence of ammonia-oxidizing archaea(AOA) and revealed they are responsible for ammoxidation in some extreme environments. However, the changes in compositional structure and ammonia-oxidation capacity of AOA communities in biological soil crusts(BSCs) of desert ecosystems remain poorly understood.Here, we utilized Illumina MiSeq sequencing and microbial functional gene array(GeoChip 5.0) to assess the above changes along a 51-year revegetation chronosequence in the Tengger Desert, China. The results showed a significant difference in AOA-community richness between 5-year-old BSCs and older ones. The most dominant phylum during BSC development was Crenarchaeota, and the corresponding species were ammonia-oxidizing_Crenarchaeote and environmental_samples_Crenarchaeota. Network analysis revealed that the positive correlations among dominant taxa increased, and their cooperation was reinforced in AOA communities during BSC succession. Redundancy analysis showed that the dominant factor influencing the change in AOA-community structure was soil texture. GeoChip 5.0 indicated that the amoA gene abundances of AOA and ammonia-oxidizing bacteria(AOB) were basically the same, demonstrating that AOA and AOB played an equally important role during BSCs development. Our study of the long-term succession of BSC demonstrated a persistent response of AOA communities to revegetation development in desert ecosystems.
引文
Abed RM,Al Kharusi S,Schramm A,et al.,2010.Bacterial di‐versity,pigments and nitrogen fixation of biological desert crusts from the Sultanate of Oman.FEMS Microbiology Ecology,72:418-428.DOI:10.1111/j.1574-6941.2010.00854.x.
Aitkenhead JA,Mcdowell WH,2000.Soil C:N ratio as a pre‐dictor of annual riverine DOC flux at local and global scales.Global Biogeochemical Cycles,14(1):127-138.DOI:10.1029/1999GB900083.
Andrés P,Moore JC,Simpson RT,et al.,2016.Soil food web stability in response to grazing in a semiarid prairie:the im‐portance of soil textural heterogeneity.Soil Biology and Biochemistry,97:131-143.DOI:10.1016/j.soilbio.2016.02.014.
Belnap J,2003.Factors influencing nitrogen fixation and nitro‐gen release in biological soil crusts.In:Belnap J,Lange OL(eds.).Biological Soil Crusts:Structure,Function,and Management.Springer,Berlin,pp.241-261.
Belnap J,Weber B,Büdel B,2016.Biological soil crusts as an organizing principle in drylands.In:Weber B,Büdel B,Belnap J(eds.).Biological Soil Crusts:an Organizing Prin‐ciple in Drylands.Springer,Cham,pp.3-13.
Casida LE Jr,Klein DA,Santoro T,1964.Soil dehydrogenase activity.Soil Science,98:371-376.
Chen Z,Wu WL,Shao XM,et al.,2015.Shifts in abundance and diversity of soil ammonia-oxidizing bacteria and ar‐chaea associated with land restoration in a semi-arid eco‐system.PLoS One,10(7):e0132879.
Di HJ,Cameron KC,Shen JP,et al.,2009.Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils.Nature Geoscience,2:621-624.
Erguder TH,Boon N,Wittebolle L,et al.,2009.Environmental factors shaping the ecological niches of ammonia-oxidizing archaea.FEMS Microbiology Reviews,33:855-869.DOI:10.1111/j.1574-6976.2009.00179.x.
Feng K,Zhang ZJ,Cai W,et al.,2017.Biodiversity and spe‐cies competition regulate the resilience of microbial bio‐film community.Molecular Ecology,26:6170-6182.DOI:10.1111/mec.14356.
Fierer N,Jackson RB,2006.The diversity and biogeography of soil bacterial communities.Proceedings of the National Academy of Sciences of the United States of America,103:626-631.DOI:10.1073/pnas.0507535103.
Hagberg AA,Schult DA,Swart PJ,2008.Exploring network structure,dynamics,and function using NetworkX.In:Va‐roquaux G,Vaught T,Millman J(eds.).The 7th Python in Science Conference(SciPy2008).Pasadena,CA,pp.11-15.
Hallam SJ,Mincer TJ,Schleper C,et al.,2006.Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota.PLoS Biology,4:e95.DOI:10.1371/journal.pbio.0040095.
Harris J,2009.Soil microbial communities and restoration ecology:facilitators or followers?Science,325:573-574.DOI:10.1126/science.1172975.
Hayden HL,Drake J,Imhof M,et al.,2010.The abundance of nitrogen cycle genes amoA and nifH depends on land-uses and soil types in South-Eastern Australia.Soil Biology AND Biochemistry,42:1774-1783.DOI:10.1016/j.soil‐bio.2010.06.015.
He M,Dijkstra FA,Zhang K,et al.,2016.Influence of life form,taxonomy,climate,and soil properties on shoot and root concentrations of 11 elements in herbaceous plants in a temperate desert.Plant and Soil,398:1-12.DOI:10.1007/s11104-015-2669-0.
Jesus ED,Marsh TL,Tiedje JM,et al.,2009.Changes in land use alter the structure of bacterial communities in western amazon soils.ISME Journal,3:1004-1011.DOI:10.1038/ismej.2009.47.
Jiang X,Wu Y,Liu G,et al.,2017.The effects of climate,catchment land use and local factors on the abundance and community structure of sediment ammonia-oxidizing mi‐croorganisms in Yangtze lakes.AMB Express,7(1):173.DOI:10.1186/s13568-017-0479-x.
Jin K,Sleutel S,Buchan D,et al.,2009.Changes of soil en‐zyme activities under different tillage practices in the Chi‐nese loess plateau.Soil and Tillage Research,104(1):115-120.DOI:10.1016/j.still.2009.02.004.
Kowalchuk GA,Stephen JR,2001.Ammonia-oxidizing bacte‐ria:a model for molecular microbial ecology.Annual Re‐view of Microbiology,55:485-529.DOI:10.1146/annurev.micro.55.1.485.
López-Lozano NE,Heidelberg KB,Nelson WC,et al.,2013.Microbial secondary succession in soil microcosms of a desert oasis in the Cuatro Cienegas Basin,Mexico.PeerJ,1:e47.DOI:10.7717/peerj.47.
Leininger S,Urich T,Schloter M,et al.,2006.Archaea pre‐dominate among ammonia-oxidizing prokaryotes in soils.Nature,442:806-809.DOI:10.1038/nature04983.
Li XR,Kong DS,Tan HJ,et al.,2007.Changes in soil and veg‐etation following stabilisation of dunes in the southeastern fringe of the Tengger Desert,China.Plant and Soil,300:221-231.DOI:10.1007/s11104-007-9407-1.
Li XR,Zhang P,Su YG,et al.,2012.Carbon fixation by bio‐logical soil crusts following revegetation of sand dunes in arid desert regions of China:A four-year field study.Cate‐na,97:119-126.DOI:10.1016/j.catena.2012.05.009.
Liu LC,Li SZ,Duan ZH,et al.,2006.Effects of microbiotic crusts on dew deposition in the restored vegetation area at Shapotou,northwest China.Journal of Hydrology,328:331-337.DOI:10.1016/j.jhydrol.2005.12.004.
Liu LC,Liu YB,Zhang P,et al.,2017.Development of bacteri‐al communities in biological soil crusts along a revegeta‐tion chronosequence in the Tengger Desert,northwest Chi‐na.Biogeosciences,14:3801-3814.DOI:10.5194/bg-14-3801-2017.
Mao Y,Yannarell AC,Mackie RI,2011.Changes in N-trans‐forming archaea and bacteria in soil during the establish‐ment of bioenergy crops.PLoS One,6:e24750.DOI:10.1371/journal.pone.0024750.
Martens-Habbena W,Berube PM,Urakawa H,et al.,2009.Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria.Nature,461:976-979.DOI:10.1038/nature08465.
Mayland HF,Mcintosh TH,1966.Availability of biologically fixed atmospheric nitrogen-15 to higher plants.Nature,209:421-422.DOI:10.1038/209421a0.
Moritsuka N,Izawa G,Katsura K,et al.,2015.Simple method for measuring soil sand content by nylon mesh sieving.Soil Science and Plant Nutrition,61:501-505.DOI:10.1080/00380768.2015.1016864.
Nanjing Institute of Soil Research,1980.Analysis of Soil Phys‐icochemical Features.Shanghai Science and Technology Press,Shanghai,pp.360.(in Chinese)
Neher DA,Lewins SA,Weicht TR,et al.,2009.Microarthro‐pod communities associated with biological soil crusts in the Colorado Plateau and Chihuahuan deserts.Journal of Arid Environments,73:672-677.DOI:10.1016/j.jaridenv.2009.01.013.
Nelson DW,Sommers LE,1996.Total carbon,organic carbon and organic matter.Methods of Soil Analysis Part 3-chemical Methods,(methodsofsoilan3),pp.961-1010.
Offre P,Kerou M,Spang A,et al.,2014.Variability of the transporter gene complement in ammonia-oxidizing ar‐chaea.Trends in Microbiology,22:665-675.DOI:10.1016/j.tim.2014.07.007.
Ouyang Y,Norton JM,Stark JM,et al.,2016.Ammonia-oxidiz‐ing bacteria are more responsive than archaea to nitrogen source in an agricultural soil.Soil Biology and Biochemis‐try,96:4-15.DOI:10.1016/j.soilbio.2016.01.012.
Parton WJ,Cole CV,Stewart JWB,et al.,1989.Simulating re‐gional patterns of soil C,N and P dynamics in the U.S.cen‐tral grasslands region.In:Clarholm M,Bergstr?m L(eds.).Ecology of Arable Land-Perspectives and Challenges.Kluwer Academic Publishers,Netherlands,pp.99-108.
Prosser JI,Nicol GW,2012.Archaeal and bacterial ammoniaoxidisers in soil:the quest for niche specialisation and dif‐ferentiation.Trends in Microbiology,20:523-531.DOI:10.1016/j.tim.2012.08.001.
Raun WR,Johnson GV,1999.Improving nitrogen use efficien‐cy for cereal production.Agronomy Journal,91:357-363.DOI:10.2134/agronj1999.00021962009100030001x.
Rawls WJ,Pachepsky YA,Ritchie JC,et al.,2003.Effect of soil organic carbon on soil water retention.Geoderma,116:61-76.DOI:10.1016/S0016-7061(03)00094-6.
Schleper C,Nicol GW,2010.Ammonia-oxidising archaeaphysiology,ecology and evolution.Advances in Microbial Physiology,57:1-41.DOI:10.1016/B978-0-12-381045-8.00001-1.
Schloss PD,Westcott SL,Ryabin T,et al.,2009.Introducing mothur:open-source,platform-independent,communitysupported software for describing and comparing microbial communities.Applied and Environmental Microbiology,75:7537.DOI:10.1128/AEM.01541-09.
Six J,Conant RT,Paul EA,et al.,2002.Stabilization mecha‐nisms of soil organic matter:implications for C-saturation of soils.Plant and Soil,241:155-176.DOI:10.1023/A:1016125726789.
Sommers LE,Nelson DW,1972.Determination of total phos‐phorus in soils:A rapid perchloric acid digestion proce‐dure.Soil Science Society of America Journal,36:902-904.DOI:10.2136/sssaj1972.03615995003600060020x.
Ter Braak CJF,1986.Canonical correspondence analysis:a new eigenvector technique for multivariate direct gradient analysis.Ecology,67:1167-1179.DOI:10.2307/1938672.
Tilman D,Downing JA,1994.Biodiversity and stability in grasslands.Nature,367:363-365.DOI:10.1038/367363a0.
Tu Q,Yu H,He ZL,et al.,2014.GeoChip 4:a functional genearray-based high-throughput environmental technology for microbial community analysis.Molecular Ecology Re‐sources,14(5):914-928.DOI:10.1111/1755-0998.12239.
Van der Heijden MGA,Klironomos J,Ursic M,et al.,1998.Mycorrhizal fungal diversity determines plant biodiversity,ecosystem variability and productivity.Nature,396:69-72.DOI:10.1038/23932.
Wang C,Wang X,Liu D,et al.,2014.Aridity threshold in con‐trolling ecosystem nitrogen cycling in arid and semi-arid grasslands.Nature Communications,5:4799.DOI:10.1038/ncomms5799.
Walkly A,1934.An examination of the Degtjareff method for determining soil organic matter and a proposed modifica‐tion to the chromic acid titration method.Soil Science,37:29-38.
West NE,1991.Nutrient cycling in soils of semiarid and arid regions.In:Skujins J(ed.).Semiarid Lands and Deserts,Soil Resource and Reclamation.Marcel Dekker,Inc,New York,pp.295-332.
Yang CL,Sun TH,Zhou WX,et al.,2007.Single and joint ef‐fects of pesticides and mercury on soil urease.Journal of Environmental Sciences,19:210-216.DOI:10.1016/S1001-0742(07)60034-5.
Zhalnina K,de Quadros PD,Camargo FA,et al.,2012.Drivers of archaeal ammonia-oxidizing communities in soil.Fron‐tiers in Microbiology,3:210.DOI:10.3389/fmicb.2012.00210.
Zhang LM,Hu HW,Shen JP,et al.,2012.Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils.ISMEJournal,6(5):1032-1045.DOI:10.1038/ismej.2011.168.
Aitkenhead JA,Mcdowell WH,2000.Soil C:N ratio as a pre‐dictor of annual riverine DOC flux at local and global scales.Global Biogeochemical Cycles,14(1):127-138.DOI:10.1029/1999GB900083.
Andrés P,Moore JC,Simpson RT,et al.,2016.Soil food web stability in response to grazing in a semiarid prairie:the im‐portance of soil textural heterogeneity.Soil Biology and Biochemistry,97:131-143.DOI:10.1016/j.soilbio.2016.02.014.
Belnap J,2003.Factors influencing nitrogen fixation and nitro‐gen release in biological soil crusts.In:Belnap J,Lange OL(eds.).Biological Soil Crusts:Structure,Function,and Management.Springer,Berlin,pp.241-261.
Belnap J,Weber B,Büdel B,2016.Biological soil crusts as an organizing principle in drylands.In:Weber B,Büdel B,Belnap J(eds.).Biological Soil Crusts:an Organizing Prin‐ciple in Drylands.Springer,Cham,pp.3-13.
Casida LE Jr,Klein DA,Santoro T,1964.Soil dehydrogenase activity.Soil Science,98:371-376.
Chen Z,Wu WL,Shao XM,et al.,2015.Shifts in abundance and diversity of soil ammonia-oxidizing bacteria and ar‐chaea associated with land restoration in a semi-arid eco‐system.PLoS One,10(7):e0132879.
Di HJ,Cameron KC,Shen JP,et al.,2009.Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils.Nature Geoscience,2:621-624.
Erguder TH,Boon N,Wittebolle L,et al.,2009.Environmental factors shaping the ecological niches of ammonia-oxidizing archaea.FEMS Microbiology Reviews,33:855-869.DOI:10.1111/j.1574-6976.2009.00179.x.
Feng K,Zhang ZJ,Cai W,et al.,2017.Biodiversity and spe‐cies competition regulate the resilience of microbial bio‐film community.Molecular Ecology,26:6170-6182.DOI:10.1111/mec.14356.
Fierer N,Jackson RB,2006.The diversity and biogeography of soil bacterial communities.Proceedings of the National Academy of Sciences of the United States of America,103:626-631.DOI:10.1073/pnas.0507535103.
Hagberg AA,Schult DA,Swart PJ,2008.Exploring network structure,dynamics,and function using NetworkX.In:Va‐roquaux G,Vaught T,Millman J(eds.).The 7th Python in Science Conference(SciPy2008).Pasadena,CA,pp.11-15.
Hallam SJ,Mincer TJ,Schleper C,et al.,2006.Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota.PLoS Biology,4:e95.DOI:10.1371/journal.pbio.0040095.
Harris J,2009.Soil microbial communities and restoration ecology:facilitators or followers?Science,325:573-574.DOI:10.1126/science.1172975.
Hayden HL,Drake J,Imhof M,et al.,2010.The abundance of nitrogen cycle genes amoA and nifH depends on land-uses and soil types in South-Eastern Australia.Soil Biology AND Biochemistry,42:1774-1783.DOI:10.1016/j.soil‐bio.2010.06.015.
He M,Dijkstra FA,Zhang K,et al.,2016.Influence of life form,taxonomy,climate,and soil properties on shoot and root concentrations of 11 elements in herbaceous plants in a temperate desert.Plant and Soil,398:1-12.DOI:10.1007/s11104-015-2669-0.
Jesus ED,Marsh TL,Tiedje JM,et al.,2009.Changes in land use alter the structure of bacterial communities in western amazon soils.ISME Journal,3:1004-1011.DOI:10.1038/ismej.2009.47.
Jiang X,Wu Y,Liu G,et al.,2017.The effects of climate,catchment land use and local factors on the abundance and community structure of sediment ammonia-oxidizing mi‐croorganisms in Yangtze lakes.AMB Express,7(1):173.DOI:10.1186/s13568-017-0479-x.
Jin K,Sleutel S,Buchan D,et al.,2009.Changes of soil en‐zyme activities under different tillage practices in the Chi‐nese loess plateau.Soil and Tillage Research,104(1):115-120.DOI:10.1016/j.still.2009.02.004.
Kowalchuk GA,Stephen JR,2001.Ammonia-oxidizing bacte‐ria:a model for molecular microbial ecology.Annual Re‐view of Microbiology,55:485-529.DOI:10.1146/annurev.micro.55.1.485.
López-Lozano NE,Heidelberg KB,Nelson WC,et al.,2013.Microbial secondary succession in soil microcosms of a desert oasis in the Cuatro Cienegas Basin,Mexico.PeerJ,1:e47.DOI:10.7717/peerj.47.
Leininger S,Urich T,Schloter M,et al.,2006.Archaea pre‐dominate among ammonia-oxidizing prokaryotes in soils.Nature,442:806-809.DOI:10.1038/nature04983.
Li XR,Kong DS,Tan HJ,et al.,2007.Changes in soil and veg‐etation following stabilisation of dunes in the southeastern fringe of the Tengger Desert,China.Plant and Soil,300:221-231.DOI:10.1007/s11104-007-9407-1.
Li XR,Zhang P,Su YG,et al.,2012.Carbon fixation by bio‐logical soil crusts following revegetation of sand dunes in arid desert regions of China:A four-year field study.Cate‐na,97:119-126.DOI:10.1016/j.catena.2012.05.009.
Liu LC,Li SZ,Duan ZH,et al.,2006.Effects of microbiotic crusts on dew deposition in the restored vegetation area at Shapotou,northwest China.Journal of Hydrology,328:331-337.DOI:10.1016/j.jhydrol.2005.12.004.
Liu LC,Liu YB,Zhang P,et al.,2017.Development of bacteri‐al communities in biological soil crusts along a revegeta‐tion chronosequence in the Tengger Desert,northwest Chi‐na.Biogeosciences,14:3801-3814.DOI:10.5194/bg-14-3801-2017.
Mao Y,Yannarell AC,Mackie RI,2011.Changes in N-trans‐forming archaea and bacteria in soil during the establish‐ment of bioenergy crops.PLoS One,6:e24750.DOI:10.1371/journal.pone.0024750.
Martens-Habbena W,Berube PM,Urakawa H,et al.,2009.Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria.Nature,461:976-979.DOI:10.1038/nature08465.
Mayland HF,Mcintosh TH,1966.Availability of biologically fixed atmospheric nitrogen-15 to higher plants.Nature,209:421-422.DOI:10.1038/209421a0.
Moritsuka N,Izawa G,Katsura K,et al.,2015.Simple method for measuring soil sand content by nylon mesh sieving.Soil Science and Plant Nutrition,61:501-505.DOI:10.1080/00380768.2015.1016864.
Nanjing Institute of Soil Research,1980.Analysis of Soil Phys‐icochemical Features.Shanghai Science and Technology Press,Shanghai,pp.360.(in Chinese)
Neher DA,Lewins SA,Weicht TR,et al.,2009.Microarthro‐pod communities associated with biological soil crusts in the Colorado Plateau and Chihuahuan deserts.Journal of Arid Environments,73:672-677.DOI:10.1016/j.jaridenv.2009.01.013.
Nelson DW,Sommers LE,1996.Total carbon,organic carbon and organic matter.Methods of Soil Analysis Part 3-chemical Methods,(methodsofsoilan3),pp.961-1010.
Offre P,Kerou M,Spang A,et al.,2014.Variability of the transporter gene complement in ammonia-oxidizing ar‐chaea.Trends in Microbiology,22:665-675.DOI:10.1016/j.tim.2014.07.007.
Ouyang Y,Norton JM,Stark JM,et al.,2016.Ammonia-oxidiz‐ing bacteria are more responsive than archaea to nitrogen source in an agricultural soil.Soil Biology and Biochemis‐try,96:4-15.DOI:10.1016/j.soilbio.2016.01.012.
Parton WJ,Cole CV,Stewart JWB,et al.,1989.Simulating re‐gional patterns of soil C,N and P dynamics in the U.S.cen‐tral grasslands region.In:Clarholm M,Bergstr?m L(eds.).Ecology of Arable Land-Perspectives and Challenges.Kluwer Academic Publishers,Netherlands,pp.99-108.
Prosser JI,Nicol GW,2012.Archaeal and bacterial ammoniaoxidisers in soil:the quest for niche specialisation and dif‐ferentiation.Trends in Microbiology,20:523-531.DOI:10.1016/j.tim.2012.08.001.
Raun WR,Johnson GV,1999.Improving nitrogen use efficien‐cy for cereal production.Agronomy Journal,91:357-363.DOI:10.2134/agronj1999.00021962009100030001x.
Rawls WJ,Pachepsky YA,Ritchie JC,et al.,2003.Effect of soil organic carbon on soil water retention.Geoderma,116:61-76.DOI:10.1016/S0016-7061(03)00094-6.
Schleper C,Nicol GW,2010.Ammonia-oxidising archaeaphysiology,ecology and evolution.Advances in Microbial Physiology,57:1-41.DOI:10.1016/B978-0-12-381045-8.00001-1.
Schloss PD,Westcott SL,Ryabin T,et al.,2009.Introducing mothur:open-source,platform-independent,communitysupported software for describing and comparing microbial communities.Applied and Environmental Microbiology,75:7537.DOI:10.1128/AEM.01541-09.
Six J,Conant RT,Paul EA,et al.,2002.Stabilization mecha‐nisms of soil organic matter:implications for C-saturation of soils.Plant and Soil,241:155-176.DOI:10.1023/A:1016125726789.
Sommers LE,Nelson DW,1972.Determination of total phos‐phorus in soils:A rapid perchloric acid digestion proce‐dure.Soil Science Society of America Journal,36:902-904.DOI:10.2136/sssaj1972.03615995003600060020x.
Ter Braak CJF,1986.Canonical correspondence analysis:a new eigenvector technique for multivariate direct gradient analysis.Ecology,67:1167-1179.DOI:10.2307/1938672.
Tilman D,Downing JA,1994.Biodiversity and stability in grasslands.Nature,367:363-365.DOI:10.1038/367363a0.
Tu Q,Yu H,He ZL,et al.,2014.GeoChip 4:a functional genearray-based high-throughput environmental technology for microbial community analysis.Molecular Ecology Re‐sources,14(5):914-928.DOI:10.1111/1755-0998.12239.
Van der Heijden MGA,Klironomos J,Ursic M,et al.,1998.Mycorrhizal fungal diversity determines plant biodiversity,ecosystem variability and productivity.Nature,396:69-72.DOI:10.1038/23932.
Wang C,Wang X,Liu D,et al.,2014.Aridity threshold in con‐trolling ecosystem nitrogen cycling in arid and semi-arid grasslands.Nature Communications,5:4799.DOI:10.1038/ncomms5799.
Walkly A,1934.An examination of the Degtjareff method for determining soil organic matter and a proposed modifica‐tion to the chromic acid titration method.Soil Science,37:29-38.
West NE,1991.Nutrient cycling in soils of semiarid and arid regions.In:Skujins J(ed.).Semiarid Lands and Deserts,Soil Resource and Reclamation.Marcel Dekker,Inc,New York,pp.295-332.
Yang CL,Sun TH,Zhou WX,et al.,2007.Single and joint ef‐fects of pesticides and mercury on soil urease.Journal of Environmental Sciences,19:210-216.DOI:10.1016/S1001-0742(07)60034-5.
Zhalnina K,de Quadros PD,Camargo FA,et al.,2012.Drivers of archaeal ammonia-oxidizing communities in soil.Fron‐tiers in Microbiology,3:210.DOI:10.3389/fmicb.2012.00210.
Zhang LM,Hu HW,Shen JP,et al.,2012.Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils.ISMEJournal,6(5):1032-1045.DOI:10.1038/ismej.2011.168.
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