Skip to main content
SpringerLink
Log in

nirS-type denitrifying bacterial communities in relation to soil physicochemical conditions and soil depths of two montane riparian meadows in North China

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Mountain riparian zones are excellent buffers for protecting aquatic ecosystems from nutrient runoff in nitrogen deposition processes due to fertilization and manure. Denitrification is a critical process for transferring soil N to the atmosphere. Denitrifying bacterial communities in soil are indicative of the soil quality of a functional ecosystem. We investigated the effects of physicochemical properties of soil on the diversity and activity of denitrifiers in the top-soil and sub-soil of two typical montane riparian meadows: a multi-colored and a flood-plain meadow. Illumina MiSeq 2500 sequencing of nirS showed that the multi-colored meadow had greater diversity and abundance of nirS-type denitrifiers than the flood-plain meadow and that the total N content, ammonium content, and denitrification enzyme activity (DEA) in soil differed significantly between the two types of meadows. The abundances of dominant denitrifiers at phylum and genus levels showed different responses to the two soil layers of the two meadow types. In top-soils, the highest abundance of Firmicutes was recorded in the multi-colored meadow, while in the flood-plain meadow, there was the highest abundance of Proteobacteria. The Actinobacteria abundance was the highest in top-soil and sub-soil of the flood-plain meadow. The abundance of Chloroflexi was the highest in top-soil of the flood-plain meadow and in sub-soil of the multi-colored meadow. The diversity of denitrifying bacteria was strongly influenced by variations of soil properties down the soil profile. Spearman’s rank correlation analyses showed that the diversity and community composition of denitrifying bacteria were strongly associated with most of the soil properties. Therefore, physicochemical soil properties, and particularly the organic carbon, nitrate, and ammonium contents, influence the diversity and abundance of denitrifiers in soil.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abell GC, Revill AT, Smith C, Bissett AP, Volkman JK, Robert SS (2010) Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary. ISME J 4:286–300

    CAS  Google Scholar 

  • Achat DL, Augusto L, Bakker MR, Gallet-Budynek A, Morel C (2012) Microbial processes controlling P availability in forest spodosols as affected by soil depth and soil properties. Soil Biol Biochem 44:39–48

    CAS  Google Scholar 

  • Al-Agely A, Reeves F (1995) Inland sand dune mycorrhizae: effects of soil depth, moisture, and pH on colonization of Oryzopsis hymenoides. Mycologia 87:54–60

    Google Scholar 

  • Anderson CR, Peterson ME, Frampton RA, Bulman SR, Keenan S, Curtin D (2018) Rapid increases in soil pH solubilise organic matter, dramatically increase denitrification potential and strongly stimulate microorganisms from the Firmicutes phylum. PeerJ 6:e6090

    Google Scholar 

  • Attard E, Recous S, Chabbi A, Berranger CD, Guillaumaud N, Labreuche J, Philippot L, Schmid B, Roux XL (2011) Soil environmental conditions rather than denitrifier abundance and diversity drive potential denitrification after changes in land uses. Glob Chang Biol 17:1975–1989

    Google Scholar 

  • Augustaitis A, Bytnerowicz A, Bytnerowicz A, Arbaugh M, Fenn M, Gimeno BS, Paoletti E (2008) Contribution of ambient ozone to Scots pine defoliation and reduced growth in the Central European forests: a Lithuanian case study. Environ Pollut 155:436–445

    CAS  Google Scholar 

  • Barrett M, Khalil M, Jahangir MMR, Lee C, Cárdenas LM, Collins G, Richards KG, O’Flaherty V (2016) Carbon amendment and soil depth affect the distribution and abundance of denitrifiers in agricultural soils. Environ Sci Pollut Res 23:7899–7910

    CAS  Google Scholar 

  • Bernhard A (2010) The nitrogen cycle: processes, players, and human impact. Nat Educ Knowl 3(10):25

    Google Scholar 

  • Billy C, Billen G, Sebilo M, Birgand F, Tournebize J (2010) Nitrogen isotopic composition of leached nitrate and soil organic matter as an indicator of denitrification in a sloping drained agricultural plot and adjacent uncultivated riparian buffer strips. Soil Biol Biochem 42:108–117

    CAS  Google Scholar 

  • Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59

    CAS  Google Scholar 

  • Booth MS, Stark JM, Rastetter E (2005) Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol Monogr 75:139–157

    Google Scholar 

  • Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46

    CAS  Google Scholar 

  • Bremner J (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci 55:11–33

    CAS  Google Scholar 

  • Bru D, Ramette A, Saby N, Dequiedt S, Ranjard L, Jolivet C, Arrouays D, Philippot L (2011) Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J 5:532–542

    CAS  Google Scholar 

  • Buske TC, Robaina AD, Peiter MX, Rosso RB, Torres RR, Nunes MS (2013) Performance evaluation of the weighing method for the determination of soil moisture. Rev Bras Agric Irrigada 7:340–348

    Google Scholar 

  • Campbell CA, Lafond GP, Biederbeck VO, Winkleman GE (1993) Influence of legumes and fertilization of deep distribution of available phosphorus (Olsen-P) in a thin black chernozemic soil. Can J Soil Sci 73:555–565

    CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335

  • Cavigelli M, Robertson G (2001) Role of denitrifier diversity in rates of nitrous oxide consumption in a terrestrial ecosystem. Soil Biol Biochem 33:297–310

    CAS  Google Scholar 

  • Chapuis-Lardy L, Wrage N, Metay A, Chotte JL, Bernoux M (2007) Soils, a sink for N2O? A review. Glob Chang Biol 13:1–17

    Google Scholar 

  • Chen L, Ding N, Fu Q, Brookes PC, Xu J, Guo B, Lin Y, Hua L, Li N (2016) The influence of soil properties on the size and structure of bacterial and fungal communities along a paddy soil chronosequence. Eur J Soil Biol 76:9–18

    Google Scholar 

  • Christianl L, Michaels S, Marka B, Noah F (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415

    Google Scholar 

  • Clough TJ, Lanigan GJ, de Klein CA, Samad MS, Morales SE, Rex D, Bakken LR, Johns C, Condron LM, Grant J (2017) Influence of soil moisture on codenitrification fluxes from a urea-affected pasture soil. Sci Rep 7:1–12

    CAS  Google Scholar 

  • Critchley C, Chambers B, Fowbert J, Sanderson R, Bhogal A, Rose S (2002) Association between lowland grassland plant communities and soil properties. Biol Conserv 105:199–215

    Google Scholar 

  • Dandie CE, Wertz S, Leclair CL, Goyer C, Burton DL, Patten CL, Zebarth BJ, Trevors JT (2011) Abundance, diversity and functional gene expression of denitrifier communities in adjacent riparian and agricultural zones. FEMS Microbiol Ecol 77:69–82. https://doi.org/10.1111/j.1574-6941.2011.01084.x

    Article  CAS  Google Scholar 

  • Davinic M, Fultz LM, Acosta-Martinez V, Calderón FJ, Cox SB, Dowd SE, Allen VG, Zak JC, Moore-Kucera J (2012) Pyrosequencing and mid-infrared spectroscopy reveal distinct aggregate stratification of soil bacterial communities and organic matter composition. Soil Biol Biochem 46:63–72

    CAS  Google Scholar 

  • Ding J, Fu L, Ding Z-W, Lu Y-Z, Cheng SH, Zeng RJ (2016) Environmental evaluation of coexistence of denitrifying anaerobic methane-oxidizing archaea and bacteria in a paddy field. Appl Microbiol Biotechnol 100:439–446

    CAS  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    CAS  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    CAS  Google Scholar 

  • Ellis RC, Graley AM (2010) Soil chemical properties as related to forest succession in a highland area in north-east Tasmania. Austral Ecol 12:307–317

    Google Scholar 

  • Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microbiol 71:8335–8343

    CAS  Google Scholar 

  • Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176

    CAS  Google Scholar 

  • Fitter A, Gilligan C, Hollingworth K, Kleczkowski A, Twyman R, Pitchford J (2005) Biodiversity and ecosystem function in soil. Funct Ecol 19:369–377

    Google Scholar 

  • Gregorich EG, Reynolds WD, Culley JLB, Mcgovern MA, Curnoe WE (1993) Changes in soil physical properties with depth in a conventionally tilled soil after no-tillage. Soil Tillage Res 26:289–299

    Google Scholar 

  • Hallin S, Jones CM, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597–605

    CAS  Google Scholar 

  • Hill AR, Cardaci M (2004) Denitrification and organic carbon availability in riparian wetland soils and subsurface sediments. Soil Sci Soc Am J 68:320–325

    CAS  Google Scholar 

  • Kramer C, Gleixner G (2008) Soil organic matter in soil depth profiles: distinct carbon preferences of microbial groups during carbon transformation. Soil Biol Biochem 40:425–433

    CAS  Google Scholar 

  • Kuramae EE, Yergeau E, Wong LC, Pijl AS, van Veen JA, Kowalchuk GA (2012) Soil characteristics more strongly influence soil bacterial communities than land-use type. FEMS Microbiol Ecol 79:12–24

    CAS  Google Scholar 

  • Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676

    Article  CAS  Google Scholar 

  • Laslett GM, Mcbratney AB, Pahl PJ, Hutchinson MF (2010) Comparison of several spatial prediction methods for soil pH. J Soil Sci 38:325–341

    Google Scholar 

  • Li C, Yan K, Tang L, Jia Z, Li Y (2014) Change in deep soil microbial communities due to long-term fertilization. Soil Biol Biochem 75:264–272. https://doi.org/10.1016/j.soilbio.2014.04.023

    Article  CAS  Google Scholar 

  • Li Y, Wang S, Jiang L, Zhang L, Cui S, Meng F, Wang Q, Li X, Zhou Y (2016) Changes of soil microbial community under different degraded gradients of alpine meadow. Agric Ecosyst Environ 222:213–222

    Google Scholar 

  • Ligi T, Oopkaup K, Truu M, Preem J-K, Nõlvak H, Mitsch WJ, Mander Ü, Truu J (2014a) Characterization of bacterial communities in soil and sediment of a created riverine wetland complex using high-throughput 16S rRNA amplicon sequencing. Ecol Eng 72:56–66

    Google Scholar 

  • Ligi T, Truu M, Truu J, Nõlvak H, Kaasik A, Mitsch WJ, Mander Ü (2014b) Effects of soil chemical characteristics and water regime on denitrification genes (nirS, nirK, and nosZ) abundances in a created riverine wetland complex. Ecol Eng 72:47–55

    Google Scholar 

  • Lorenz K, Lal R, Ehlers K (2019) Soil organic carbon stock as an indicator for monitoring land and soil degradation in relation to United Nations’ Sustainable Development Goals. Land Degrad Dev 30:824–838. https://doi.org/10.1002/ldr.3270

    Article  Google Scholar 

  • Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507

    Article  CAS  Google Scholar 

  • Mathieu O, Leveque J, Henault C, Milloux M, Bizouard F, Andreux F (2006) Emissions and spatial variability of N2O, N2 and nitrous oxide mole fraction at the field scale, revealed with 15N isotopic techniques. Soil Biol Biochem 38:941–951

    CAS  Google Scholar 

  • Mayer PM, Reynolds SK, McCutchen MD, Canfield TJ (2007) Meta-analysis of nitrogen removal in riparian buffers. J Environ Qual 36:1172–1180. https://doi.org/10.2134/jeq2006.0462

    Article  CAS  Google Scholar 

  • Mergel A, Schmitz O, Mallmann T, Bothe H (2001) Relative abundance of denitrifying and dinitrogen-fixing bacteria in layers of a forest soil. FEMS Microbiol Ecol 36:33–42

    CAS  Google Scholar 

  • Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62–71

    CAS  Google Scholar 

  • Mitsch WJ, Day JW, Zhang L, Lane RR (2005) Nitrate-nitrogen retention in wetlands in the Mississippi River Basin. Ecol Eng 24:267–278

    Google Scholar 

  • Moebius BN, Es HMV, Schindelbeck RR, Idowu OJ, Clune DJ, Thies JE (2007) Evaluation of laboratory-measured soil properties as indicators of soil physical quality. Soil Sci 172:895–912

    CAS  Google Scholar 

  • Müller C, Stevens R, Laughlin R, Azam F, Ottow J (2002) The nitrification inhibitor DMPP had no effect on denitrifying enzyme activity. Soil Biol Biochem 34:1825–1827

    Google Scholar 

  • Naiman RJ, Decamps H (1997) The ecology of interfaces: riparian zones. Annu Rev Ecol Syst 28:621–658

    Google Scholar 

  • Norton JB, Jungst LJ, Norton U, Olsen HR, Tate KW, Horwath WR (2011) Soil carbon and nitrogen storage in upper montane riparian meadows. Ecosystems 14:1217–1231

    CAS  Google Scholar 

  • Okach DO, Ondier JO, Kumar A, Rambold G, Tenhunen J, Huwe B, Otieno D (2019) Interactive influence of livestock grazing and manipulated rainfall on soil properties in a humid tropical savanna. J Soils Sediments 19:1088–1098

    CAS  Google Scholar 

  • Oles KM, Weixelman DA, Lile DF, Tate KW, Snell LK, Roche LM (2017) Riparian meadow response to modern conservation grazing management. Environ Manag 60:383–395

    Google Scholar 

  • Pastorelli R, Landi S, Trabelsi D, Piccolo R, Mengoni A, Bazzicalupo M, Pagliai M (2011) Effects of soil management on structure and activity of denitrifying bacterial communities. Appl Soil Ecol 49:46–58

    Google Scholar 

  • Philippot L, Hallin S (2005) Finding the missing link between diversity and activity using denitrifying bacteria as a model functional community. Curr Opin Microbiol 8:234–239

    CAS  Google Scholar 

  • Philippot L, Spor A, Hénault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron P-A (2013) Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7:1609–1619

    CAS  Google Scholar 

  • Pouyat RV, Yesilonis ID, Russellanelli J, Neerchal NK (2007) Soil chemical and physical properties that differentiate urban land-use and cover types. Soilence Soc Am J 71:1010–1019

    CAS  Google Scholar 

  • Priemé A, Braker G, Tiedje JM (2002) Diversity of nitrite reductase (nirK and nirS) gene fragments in forested upland and wetland soils. Appl Environ Microbiol 68:1893–1900

    Google Scholar 

  • Qin S, Hu C, Oenema O (2012) Quantifying the underestimation of soil denitrification potential as determined by the acetylene inhibition method. Soil Biol Biochem 47:14–17

    CAS  Google Scholar 

  • Qin HL, Zhang ZX, Lu J, Zhu YJ, Webster R, Liu XL, Yuan HZ, Hou HJ, Chen CL, Wei WX (2016) Change from paddy rice to vegetable growing changes nitrogen-cycling microbial communities and their variation with depth in the soil. Eur J Soil Sci 67:650–658

    CAS  Google Scholar 

  • Rengel Z (2011) Soil pH, soil health and climate change. In: Soil Health and Climate Change. Springer, Berlin, pp 69–85. https://doi.org/10.1007/978-3-642-20256-8_4

    Chapter  Google Scholar 

  • Rich JJ, Myrold DD (2004) Community composition and activities of denitrifying bacteria from adjacent agricultural soil, riparian soil, and creek sediment in Oregon, USA. Soil Biol Biochem 36:1431–1441

    CAS  Google Scholar 

  • Rich J, Heichen R, Bottomley P, Cromack K, Myrold D (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microbiol 69:5974–5982

    CAS  Google Scholar 

  • Rosa SM, Kraemer FB, Soria MA, Guerrero LD, Morrás HJM, Figuerola ELM, Erijman L (2014) The influence of soil properties on denitrifying bacterial communities and denitrification potential in no-till production farms under contrasting management in the Argentinean Pampas. Appl Soil Ecol 75:172–180

    Google Scholar 

  • Ryden JC (2010) Denitrification loss from a grassland soil in the field receiving different rates of nitrogen as ammonium nitrate. J Soil Sci 34:355–365

    Google Scholar 

  • Santi C, Certini G, D'Acqui LP (2006) Direct determination of organic carbon by dry combustion in soils with carbonates. Commun Soil Sci Plant Anal 37:155–162

    CAS  Google Scholar 

  • Schipper L, Cooper A, Harfoot C, Dyck W (1993) Regulators of denitrification in an organic riparian soil. Soil Biol Biochem 25:925–933

    CAS  Google Scholar 

  • Schlatter DC, Bakker MG, Bradeen JM, Kinkel LL (2015) Plant community richness and microbial interactions structure bacterial communities in soil. Ecology 96:134–142

    Google Scholar 

  • Sgouridis F, Heppell C, Wharton G, Lansdown K, Trimmer M (2011) Denitrification and dissimilatory nitrate reduction to ammonium (DNRA) in a temperate re-connected floodplain. Water Res 45:4909–4922

    CAS  Google Scholar 

  • Šimek M, Cooper J (2002) The influence of soil pH on denitrification: progress towards the understanding of this interaction over the last 50 years. Eur J Soil Sci 53:345–354

    Google Scholar 

  • Stein LY, Klotz MG (2016) The nitrogen cycle. Curr Biol 26:R94–R98

    CAS  Google Scholar 

  • Takoutsing B, Weber JC, Tchoundjeu Z, Shepherd K (2016) Soil chemical properties dynamics as affected by land use change in the humid forest zone of Cameroon. Agrofor Syst 90:1089–1102

    Google Scholar 

  • Tang Y, Zhang X, Li D, Wang H, Chen F, Fu X, Fang X, Sun X, Yu G (2016) Impacts of nitrogen and phosphorus additions on the abundance and community structure of ammonia oxidizers and denitrifying bacteria in Chinese fir plantations. Soil Biol Biochem 103:284–293

    CAS  Google Scholar 

  • Thomson BC, Ostle N, McNamara N, Bailey MJ, Whiteley AS, Griffiths RI (2010) Vegetation affects the relative abundances of dominant soil bacterial taxa and soil respiration rates in an upland grassland soil. Microb Ecol 59:335–343

    Google Scholar 

  • Throbäck IN, Enwall K, Jarvis Å, Hallin S (2010) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49:401–417

    Google Scholar 

  • Wang J, Borsboom AC, Smith GC (2010) Flora diversity of farm forestry plantations in southeast Queensland. Ecol Manag Restor 5:43–51

    Google Scholar 

  • Wang B, Zhang GH, Yang YF, Li PP, Liu JX (2018) The effects of varied soil properties induced by natural grassland succession on the process of soil detachment. Catena 166:192–199

    CAS  Google Scholar 

  • Weber CF, Vilgalys R, Kuske CR (2013) Changes in fungal community composition in response to elevated atmospheric CO2 and nitrogen fertilization varies with soil horizon. Front Microbiol 4:78

    CAS  Google Scholar 

  • Webster CP, Goulding KW (1989) Influence of soil carbon content on denitrification from fallow land during autumn. J Sci Food Agric 49:131–142

    Google Scholar 

  • White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5:e1000352. https://doi.org/10.1371/journal.pcbi.1000352

    Article  CAS  Google Scholar 

  • Will C, Thürmer A, Wollherr A, Nacke H, Herold N, Schrumpf M, Gutknecht J, Wubet T, Buscot F, Daniell R (2010) Horizon-specific bacterial community composition of German grassland soils, as revealed by pyrosequencing-based analysis of 16S rRNA genes. Appl Environ Microbiol 76:6751–6759

    CAS  Google Scholar 

  • Willits CO (1951) Methods for determination of moisture-oven drying. Anal Chem 23:1058–1062

    CAS  Google Scholar 

  • Wrage N, Velthof GL, Beusichem MLV, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732

    CAS  Google Scholar 

  • Xu YG, Yu WT (2014) Effects of different fertilization regimes on denitrifying bacteria in Luvisols soil. Adv Mater Res 988:424–429

    Google Scholar 

  • Ye C, Chen C, Du M, Liu W, Zhang Q (2017) Revegetation affects soil denitrifying communities in a riparian ecotone. Ecol Eng 103:256–263

    Google Scholar 

  • Yuan H, Hou F (2015) Grazing intensity and soil depth effects on soil properties in alpine meadow pastures of Qilian Mountain in northwest China. Acta Agric Scand Sect B Soil Plant Sci 65:222–232

    CAS  Google Scholar 

  • Yuan Q, Liu P, Lu Y (2012) Differential responses of nirK-and nirS-carrying bacteria to denitrifying conditions in the anoxic rice field soil. Environ Microbiol Rep 4:113–122

    CAS  Google Scholar 

  • Zhang X, Wang M, She B, Xiao Y (2006a) Quantitative classification and ordination of forest communities in Pangquangou National Nature Reserve. Acta Ecol Sin 26:754–761

    Google Scholar 

  • Zhang X, Wang M, She B, Yang X (2006b) Numerical classification and ordination of forest communities in Pangquangou National Nature Reserve. Acta Ecol Sin 26:754–761

    Google Scholar 

  • Zhang Y, Li D, Wang H, Xiao Q, Liu X (2006c) The diversity of denitrifying bacteria in the alpine meadow soil of Sanjiangyuan natural reserve in Tibet Plateau. Chin Sci Bull 51:1245–1254

    CAS  Google Scholar 

  • Zhao Y, Peth S, Horn R, Wang Z, Steffens M, Hoffmann C, Peng X (2007) Spatial variability of soil properties affected by grazing intensity in Inner Mongolia grassland. Ecol Model 205:241–254. https://doi.org/10.1016/j.ecolmodel.2007.02.019

    Article  Google Scholar 

  • Zheng Y, Hou L, Liu M, Gao J, Yin G, Li X, Deng F, Lin X, Jiang X, Chen F (2015) Diversity, abundance, and distribution of nirS-harboring denitrifiers in intertidal sediments of the Yangtze Estuary. Microb Ecol 70:30–40

    CAS  Google Scholar 

  • Zhu G, Wang S, Li Y, Zhuang L, Zhao S, Wang C, Kuypers MM, Jetten MS, Zhu Y (2018) Microbial pathways for nitrogen loss in an upland soil. Environ Microbiol 20:1723–1738

    CAS  Google Scholar 

  • Zornoza R, Mataix-Solera J, Guerrero C, Arcenegui V, García-Orenes F, Mataix-Beneyto J, Morugán A (2007) Evaluation of soil quality using multiple lineal regression based on physical, chemical and biochemical properties. Sci Total Environ 378:233–237

    CAS  Google Scholar 

Download references

Funding

This study was supported by the Shanxi Key Technology Research & Development Program of China (2018LYCX32), Shanxi Key Laboratory of Functional Oil Tree Cultivation and Research (201805D111010), and Science and Technology Innovation Fund of Shanxi Agricultural University (20132-14).

Author information

Authors and Affiliations

  1. College of Forestry, Shanxi Agricultural University, Taigu, 030801, China

    Xiaoli Han, Yunxiang Zhang & Jinping Guo

  2. Shanxi Key Laboratory of Functional Oil Tree Cultivation and Research, Taigu, 030801, China

    Xiaoli Han, Yunxiang Zhang & Jinping Guo

  3. College of Agriculture, Shanxi Agricultural University, Taigu, 030801, China

    Chunguo Huang & Shahbaz Khan

  4. Institute of Agriculture, UWA School of Agriculture and Environment, The University of Western Australia, Perth, 6009, Australia

    Yinglong Chen

  5. Institute of Soil and Water Conservation, Northwest A&F University, and Chinese Academy of Sciences, Yangling, 712100, China

    Yinglong Chen

Authors
  1. Xiaoli Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chunguo Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shahbaz Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yunxiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yinglong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jinping Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, and data collection, and analyses were performed by Xiaoli Han and Chunguo Huang. The first draft of the manuscript was written by Xiaoli Han, and all authors commented on previous versions of the manuscript. All authors read and approved the final version of the manuscript for publication.

Corresponding author

Correspondence to Jinping Guo.

Additional information

Responsible Editor: Robert Duran

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 19 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, X., Huang, C., Khan, S. et al. nirS-type denitrifying bacterial communities in relation to soil physicochemical conditions and soil depths of two montane riparian meadows in North China. Environ Sci Pollut Res 27, 28899–28911 (2020). https://doi.org/10.1007/s11356-020-09171-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-09171-8

Keywords

Search

Navigation