Register      Login
Soil Research Soil Research Society
Soil, land care and environmental research
RESEARCH ARTICLE

Effects of alpine meadow degradation on nitrifying and denitrifying microbial communities, and N2O emissions on the Tibetan Plateau

Lu Zhang A B , Xiangtao Wang C , Jie Wang D , Qian Wan D , Lirong Liao A B , Guobin Liu A D and Chao Zhang https://orcid.org/0000-0003-2647-2922 A D *
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water Conservation, Chinese Academy of Sciences and Ministry of Water Resources, Yangling 712100, PR China.

B University of Chinese Academy of Sciences, Beijing 100049, PR China.

C Department of Animal Sciences, Xizang Agriculture and Animal Husbandry College, Linzhi 860000, PR China.

D State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Yangling 712100, PR China.

* Correspondence to: zhangchaolynn@163.com

Handling Editor: Sander Bruun

Soil Research 60(2) 158-172 https://doi.org/10.1071/SR21097
Submitted: 10 April 2021  Accepted: 6 August 2021   Published: 25 October 2021

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Meadow degradation is often accompanied by significant changes in nitrogen (N)-cycling and nitrous oxide (N2O) emission potential, and leads to challenges in meadow management. However, the mechanisms of soil N-cycling and N2O emissions remain poorly understood, especially in alpine ecosystems. In this study, we investigated the soil N-cycling process in four alpine meadows on the Tibetan Plateau along a degradation gradient using real-time quantitative polymerase chain reaction and amplicon sequencing to elucidate the mechanisms. Compared to non-degraded meadows, meadow degradation reduced N2O emissions by 38.5–140.2%. Meadow degradation reduced the abundance of amoA of ammonia-oxidising archaea (AOA) and ammonia-oxidising bacteria (AOB), whereas light and moderate degradation increased the abundance of genes nirS, nirK, and nosZ. Lightly degraded meadow exhibited the highest α-diversity of both nitrifiers and denitrifiers, but this higher diversity was not accompanied by higher N2O emissions, with only 32.3% of the microbial taxa identified as predictors of N2O emissions, suggesting that functional redundancy exists in the N-cycling process in meadow ecosystems. Nitrosospira and Mesorhizobium from the AOB and nirK communities, respectively, were identified as the key taxa that may contribute to N2O emissions. Soil properties, especially N reaction substrates, including ammonium-N, nitrate-N, dissolved organic N, and total N, were the primary drivers for N2O emissions via mediation of the N-cycling community, especially nitrifiers. Our results emphasised the importance of environmental factors in shaping nitrifying, denitrifying, and N2O emissions, providing insights for the restoration of degraded meadow ecosystems.

Keywords: alpine meadow, denitrification, functional genes, functional microbial diversity, meadow degradation gradient, N2O emissions, N-cycling, nitrification, partial least squares path model.


References

Ali M, Shaw DR, Albertsen M, Saikaly PE (2020) Comparative genome-centric analysis of freshwater and marine ANAMMOX cultures suggests functional redundancy in nitrogen removal processes. Frontiers in Microbiology 11, 16
Comparative genome-centric analysis of freshwater and marine ANAMMOX cultures suggests functional redundancy in nitrogen removal processes.Crossref | GoogleScholarGoogle Scholar |

Attard E, Recous S, Chabbi A, De Berranger C, Guillaumaud N, Labreuche J, Philippot L, Schmid B, Le Roux X (2011) Soil environmental conditions rather than denitrifier abundance and diversity drive potential denitrification after changes in land uses. Global Change Biology 17, 1975–1989.
Soil environmental conditions rather than denitrifier abundance and diversity drive potential denitrification after changes in land uses.Crossref | GoogleScholarGoogle Scholar |

Banerjee S, Schlaeppi K, van der Heijden MGA (2018) Keystone taxa as drivers of microbiome structure and functioning. Nature Reviews Microbiology 16, 567–576.

Butterbach-Bahl K, Baggs EM, Dannenman M, Kiese R, Zechmeister-Boltenstern S (2013) Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philosophical Transactions of the Royal Society B-Biological Sciences 368,
Nitrous oxide emissions from soils: how well do we understand the processes and their controls?Crossref | GoogleScholarGoogle Scholar |

Cardoso AS, Quintana BG, Janusckiewicz ER, Brito LF, Morgado ES, Reis RA, Ruggieri AC (2017) N2O emissions from urine-treated tropical soil: effects of soil moisture and compaction, urine composition, and dung addition. Catena 157, 325–332.
N2O emissions from urine-treated tropical soil: effects of soil moisture and compaction, urine composition, and dung addition.Crossref | GoogleScholarGoogle Scholar |

Chen J, Li S, Li C, Wang H, Geng Y, Kong D, Liu S, Zou J (2019) Post-seasonal effects of water-saving rice production regimes on N2O emissions in an annual rice-barley rotation system. Catena 182, 104112
Post-seasonal effects of water-saving rice production regimes on N2O emissions in an annual rice-barley rotation system.Crossref | GoogleScholarGoogle Scholar |

Dai X, Song D, Guo Q, Zhou W, Liu G, Ma R, Liang G, He P, Sun G, Yuan F, Liu Z (2021) Predicting the influence of fertilization regimes on potential N fixation through their effect on free-living diazotrophic community structure in double rice cropping systems. Soil Biology and Biochemistry 156, 108220
Predicting the influence of fertilization regimes on potential N fixation through their effect on free-living diazotrophic community structure in double rice cropping systems.Crossref | GoogleScholarGoogle Scholar |

Dang DM, Macdonald B, Warneke S, White I (2017) Available carbon and nitrate increase greenhouse gas emissions from soils affected by salinity. Soil Research 55, 47–57.
Available carbon and nitrate increase greenhouse gas emissions from soils affected by salinity.Crossref | GoogleScholarGoogle Scholar |

Domeignoz-Horta LA, Philippot L, Peyrard C, Bru D, Breuil M-C, Bizouard F, Justes E, Mary B, Leonard J, Spor A (2018) Peaks of in situ N2O emissions are influenced by N2O-producing and reducing microbial communities across arable soils. Global Change Biology 24, 360–370.
Peaks of in situ N2O emissions are influenced by N2O-producing and reducing microbial communities across arable soils.Crossref | GoogleScholarGoogle Scholar | 28752605PubMed |

Du Y, Ke X, Li J, Wang Y, Cao G, Guo X, Chen K (2021) Nitrogen deposition increases global grassland N2O emission rates steeply: a meta-analysis. Catena 199, 105105
Nitrogen deposition increases global grassland N2O emission rates steeply: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.
Search and clustering orders of magnitude faster than BLAST.Crossref | GoogleScholarGoogle Scholar | 20709691PubMed |

Fan X, Yin C, Chen H, Ye M, Zhao Y, Li T, Wakelin SA, Liang Y (2019) The efficacy of 3,4-dimethylpyrazole phosphate on N2O emissions is linked to niche differentiation of ammonia oxidizing archaea and bacteria across four arable soils. Soil Biology and Biochemistry 130, 82–93.
The efficacy of 3,4-dimethylpyrazole phosphate on N2O emissions is linked to niche differentiation of ammonia oxidizing archaea and bacteria across four arable soils.Crossref | GoogleScholarGoogle Scholar |

Fish JA, Chai BL, Wang Q, Sun YN, Brown CT, Tiedje JM, Cole JR (2013) FunGene: the functional gene pipeline and repository. Frontiers in Microbiology 4, 14
FunGene: the functional gene pipeline and repository.Crossref | GoogleScholarGoogle Scholar |

Gao X, Thomas BW, Beck R, Thompson DJ, Zhao M, Willms WD, Hao X (2018) Long-term grazing alters soil trace gas fluxes from grasslands in the foothills of the Rocky Mountains, Canada. Land Degradation & Development 29, 292–302.
Long-term grazing alters soil trace gas fluxes from grasslands in the foothills of the Rocky Mountains, Canada.Crossref | GoogleScholarGoogle Scholar |

Hall MKD, Winters AJ, Rogers GS (2014) Variations in the diurnal flux of greenhouse gases from soil and optimizing the sampling protocol for closed static chambers. Communications in Soil Science and Plant Analysis 45, 2970–2978.
Variations in the diurnal flux of greenhouse gases from soil and optimizing the sampling protocol for closed static chambers.Crossref | GoogleScholarGoogle Scholar |

Harris E, Diaz-Pines E, Stoll E, Schloter M, Schulz S, Duffner C, Li K, Moore KL, Ingrisch J, Reinthaler D, Zechmeister-Boltenstern S, Glatzel S, Brueggemann N, Bahn M (2021) Denitrifying pathways dominate nitrous oxide emissions from managed grassland during drought and rewetting. Science Advances 7,
Denitrifying pathways dominate nitrous oxide emissions from managed grassland during drought and rewetting.Crossref | GoogleScholarGoogle Scholar | 33547069PubMed |

Harter J, Krause H-M, Schuettler S, Ruser R, Fromme M, Scholten T, Kappler A, Behrens S (2014) Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community. ISME Journal 8, 660–674.
Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community.Crossref | GoogleScholarGoogle Scholar |

Kooch Y, Moghimian N, Wirth S, Noghre N (2020) Effects of grazing management on leaf litter decomposition and soil microbial activities in northern Iranian rangeland. Geoderma 361, 114100
Effects of grazing management on leaf litter decomposition and soil microbial activities in northern Iranian rangeland.Crossref | GoogleScholarGoogle Scholar |

Le Roux X, Poly F, Currey P, Commeaux C, Hai B, Nicol GW, Prosser JI, Schloter M, Attard E, Klumpp K (2008) Effects of aboveground grazing on coupling among nitrifier activity, abundance and community structure. ISME Journal 2, 221–232.
Effects of aboveground grazing on coupling among nitrifier activity, abundance and community structure.Crossref | GoogleScholarGoogle Scholar |

Levy-Booth DJ, Prescott CE, Grayston SJ (2014) Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biology and Biochemistry 75, 11–25.
Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems.Crossref | GoogleScholarGoogle Scholar |

Li G, Xu G, Shen C, Tang Y, Zhang Y, Ma K (2016) Contrasting elevational diversity patterns for soil bacteria between two ecosystems divided by the treeline. Science China-Life Sciences 59, 1177–1186.
Contrasting elevational diversity patterns for soil bacteria between two ecosystems divided by the treeline.Crossref | GoogleScholarGoogle Scholar | 27601034PubMed |

Li JW, Shangguan Z, Deng L (2020) Variations of belowground C and N cycling between arbuscular mycorrhizal and ectomycorrhizal forests across China. Soil Research 58, 441–451.
Variations of belowground C and N cycling between arbuscular mycorrhizal and ectomycorrhizal forests across China.Crossref | GoogleScholarGoogle Scholar |

Mafa-Attoye TG, Baskerville MA, Ofosu E, Oelbermann M, Thevathasan NV, Dunfield KE (2020) Riparian land-use systems impact soil microbial communities and nitrous oxide emissions in an agro-ecosystem. Science of the Total Environment 724, 138148
Riparian land-use systems impact soil microbial communities and nitrous oxide emissions in an agro-ecosystem.Crossref | GoogleScholarGoogle Scholar |

Pan H, Liu H, Liu Y, Zhang Q, Luo Y, Liu X, Liu Y, Xu J, Di H, Li Y (2018) Understanding the relationships between grazing intensity and the distribution of nitrifying communities in grassland soils. Science of the Total Environment 634, 1157–1164.
Understanding the relationships between grazing intensity and the distribution of nitrifying communities in grassland soils.Crossref | GoogleScholarGoogle Scholar |

Pan H, Yuan D, Liu W, Pi Y, Wang S, Zhu G (2020) Biogeographical distribution of dissimilatory nitrate reduction to ammonium (DNRA) bacteria in wetland ecosystems around the world. Journal of Soils and Sediments 20, 3769–3778.
Biogeographical distribution of dissimilatory nitrate reduction to ammonium (DNRA) bacteria in wetland ecosystems around the world.Crossref | GoogleScholarGoogle Scholar |

Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, Waldrop M (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environmental Microbiology 14, 993–1008.
Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska.Crossref | GoogleScholarGoogle Scholar | 22225623PubMed |

Qin H, Xing X, Tang Y, Zhu B, Wei X, Chen X, Liu Y (2020) Soil moisture and activity of nitrite- and nitrous oxide-reducing microbes enhanced nitrous oxide emissions in fallow paddy soils. Biology and Fertility of Soils 56, 53–67.
Soil moisture and activity of nitrite- and nitrous oxide-reducing microbes enhanced nitrous oxide emissions in fallow paddy soils.Crossref | GoogleScholarGoogle Scholar |

Saarenheimo J, Tiirola MA, Rissanen AJ (2015) Functional gene pyrosequencing reveals core proteobacterial denitrifiers in boreal lakes. Frontiers in Microbiology 6, 674
Functional gene pyrosequencing reveals core proteobacterial denitrifiers in boreal lakes.Crossref | GoogleScholarGoogle Scholar | 26191058PubMed |

Schirmann J, de Bastos DF, Weiler DA, Veloso MG, Dieckow J, Carvalho PCD, Bayer C (2020) Nitrous oxide emission factor from cattle urine and dung in native grassland of the Pampa biome, South Brazil. Soil Research 58, 198–206.
Nitrous oxide emission factor from cattle urine and dung in native grassland of the Pampa biome, South Brazil.Crossref | GoogleScholarGoogle Scholar |

Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 7537–7541.
Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.Crossref | GoogleScholarGoogle Scholar | 19801464PubMed |

Schwenke GD, Brock PM, Haigh BM, Herridge DF (2018) Greenhouse gas emission reductions in subtropical cereal-based cropping sequences using legumes, DMPP-coated urea and split timings of urea application. Soil Research 56, 724–736.
Greenhouse gas emission reductions in subtropical cereal-based cropping sequences using legumes, DMPP-coated urea and split timings of urea application.Crossref | GoogleScholarGoogle Scholar |

Shaaban M, Wu Y, Khalid MS, Peng Q-A, Xu XY, Wu L, Younas A, Bashir S, Mo YL, Lin S, Zafar-ul-Hye M, Abid M, Hu RG (2018) Reduction in soil N2O emissions by pH manipulation and enhanced nosZ gene transcription under different water regimes. Environmental Pollution 235, 625–631.
Reduction in soil N2O emissions by pH manipulation and enhanced nosZ gene transcription under different water regimes.Crossref | GoogleScholarGoogle Scholar | 29331895PubMed |

Shaw LJ, Nicol GW, Smith Z, Fear J, Prosser JI, Baggs EM (2006) Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environmental Microbiology 8, 214–222.
Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway.Crossref | GoogleScholarGoogle Scholar | 16423010PubMed |

Shi Y, Liu X, Zhang Q (2019) Effects of combined biochar and organic fertilizer on nitrous oxide fluxes and the related nitrifier and denitrifier communities in a saline-alkali soil. Science of the Total Environment 686, 199–211.
Effects of combined biochar and organic fertilizer on nitrous oxide fluxes and the related nitrifier and denitrifier communities in a saline-alkali soil.Crossref | GoogleScholarGoogle Scholar |

Solomon S (2007) IPCC (2007): Climate change the physical science basis. AGU Fall Meeting Abstracts 9, 01

Song Z, Wang J, Liu G, Zhang C (2019) Changes in nitrogen functional genes in soil profiles of grassland under long-term grazing prohibition in a semiarid area. Science of the Total Environment 673, 92–101.
Changes in nitrogen functional genes in soil profiles of grassland under long-term grazing prohibition in a semiarid area.Crossref | GoogleScholarGoogle Scholar |

Stone M, Kan J, Plante AF (2015) Parent material and vegetation influence bacterial community structure and nitrogen functional genes along deep tropical soil profiles at the Luquillo Critical Zone Observatory. Soil Biology and Biochemistry 80, 273–282.
Parent material and vegetation influence bacterial community structure and nitrogen functional genes along deep tropical soil profiles at the Luquillo Critical Zone Observatory.Crossref | GoogleScholarGoogle Scholar |

Sun S, Badgley BD (2019) Changes in microbial functional genes within the soil metagenome during forest ecosystem restoration. Soil Biology and Biochemistry 135, 163–172.
Changes in microbial functional genes within the soil metagenome during forest ecosystem restoration.Crossref | GoogleScholarGoogle Scholar |

Tang L, Zhong L, Xue K, Wang S, Xu Z, Lin Q, Luo C, Rui Y, Li X, Li M, Liu W, Yang Y, Zhou J, Wang Y (2019a) Warming counteracts grazing effects on the functional structure of the soil microbial community in a Tibetan grassland. Soil Biology and Biochemistry 134, 113–121.
Warming counteracts grazing effects on the functional structure of the soil microbial community in a Tibetan grassland.Crossref | GoogleScholarGoogle Scholar |

Tang S, Wang K, Xiang Y, Tian D, Wang J, Liu Y, Cao B, Guo D, Niu S (2019b) Heavy grazing reduces grassland soil greenhouse gas fluxes: a global meta-analysis. Science of the Total Environment 654, 1218–1224.
Heavy grazing reduces grassland soil greenhouse gas fluxes: a global meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Trivedi P, Delgado-Baquerizo M, Anderson IC, Singh BK (2016) Response of soil properties and microbial communities to agriculture: implications for primary productivity and soil health indicators. Frontiers in Plant Science 7, 990
Response of soil properties and microbial communities to agriculture: implications for primary productivity and soil health indicators.Crossref | GoogleScholarGoogle Scholar | 27462326PubMed |

Tzanakakis VA, Taylor AE, Bakken LR, Bottomley PJ, Myrold DD, Dörsch P (2019) Relative activity of ammonia oxidizing archaea and bacteria determine nitrification-dependent N2O emissions in Oregon forest soils. Soil Biology and Biochemistry 139, 107612
Relative activity of ammonia oxidizing archaea and bacteria determine nitrification-dependent N2O emissions in Oregon forest soils.Crossref | GoogleScholarGoogle Scholar |

Wang J, Wang X, Liu G, Zhang C, Wang G (2021) Bacterial richness is negatively related to potential soil multifunctionality in a degraded alpine meadow. Ecological Indicators 121, 106996
Bacterial richness is negatively related to potential soil multifunctionality in a degraded alpine meadow.Crossref | GoogleScholarGoogle Scholar |

Wen L, Dong SK, Zhu L, Li XY, Shi JJ, Wang YL, Ma YS (2010) The construction of grassland degradation index for Alpine Meadow in Qinghai-Tibetan Plateau. Procedia Environmental Sciences 2, 1966–1969.
The construction of grassland degradation index for Alpine Meadow in Qinghai-Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar |

Wolf B, Zheng X, Brueggemann N, Chen W, Dannenmann M, Han X, Sutton MA, Wu H, Yao Z, Butterbach-Bahl K (2010) Grazing-induced reduction of natural nitrous oxide release from continental steppe. Nature 464, 881–884.
Grazing-induced reduction of natural nitrous oxide release from continental steppe.Crossref | GoogleScholarGoogle Scholar | 20376147PubMed |

Yan R, Tang H, Xin X, Chen B, Murray PJ, Yan Y, Wang X, Yang G (2016) Grazing intensity and driving factors affect soil nitrous oxide fluxes during the growing seasons in the Hulunber meadow steppe of China. Environmental Research Letters 11, 054004
Grazing intensity and driving factors affect soil nitrous oxide fluxes during the growing seasons in the Hulunber meadow steppe of China.Crossref | GoogleScholarGoogle Scholar |

Yao P, Pan H, Qin Y, Zhang Z, Wang J, Li X, Liu X, Wang P, Ye X (2021) Greenhouse gas emissions and net ecosystem carbon budget from tobacco-planted soil with different organic amendments. Soil Research 59, 452–462.
Greenhouse gas emissions and net ecosystem carbon budget from tobacco-planted soil with different organic amendments.Crossref | GoogleScholarGoogle Scholar |

Yin M, Gao X, Tenuta M, Li L, Gui D, Li X, Zeng F (2020) Enhancement of N2O emissions by grazing is related to soil physicochemical characteristics rather than nitrifier and denitrifier abundances in alpine grassland. Geoderma 375, 114511
Enhancement of N2O emissions by grazing is related to soil physicochemical characteristics rather than nitrifier and denitrifier abundances in alpine grassland.Crossref | GoogleScholarGoogle Scholar |

Zhang C, Liu G, Song Z, Wang J, Guo L (2018) Interactions of soil bacteria and fungi with plants during long-term grazing exclusion in semiarid grasslands. Soil Biology and Biochemistry 124, 47–58.
Interactions of soil bacteria and fungi with plants during long-term grazing exclusion in semiarid grasslands.Crossref | GoogleScholarGoogle Scholar |

Zhang D, Qi Q, Tong S, Wang X, An Y, Zhang M, Lu X (2019a) Soil degradation effects on plant diversity and nutrient in Tussock Meadow Wetlands. Journal of Soil Science and Plant Nutrition 19, 535–544.
Soil degradation effects on plant diversity and nutrient in Tussock Meadow Wetlands.Crossref | GoogleScholarGoogle Scholar |

Zhang K, Li X, Cheng X, Zhang Z, Zhang Q (2019b) Changes in soil properties rather than functional gene abundance control carbon and nitrogen mineralization rates during long-term natural revegetation. Plant and Soil 443, 293–306.
Changes in soil properties rather than functional gene abundance control carbon and nitrogen mineralization rates during long-term natural revegetation.Crossref | GoogleScholarGoogle Scholar |

Zhang Y, Zhang N, Yin J, Yang F, Zhao Y, Jiang Z, Tao J, Yan X, Qiu Y, Guo H, Hu S (2020) Combination of warming and N inputs increases the temperature sensitivity of soil N2O emission in a Tibetan alpine meadow. Science of the Total Environment 704, 135450
Combination of warming and N inputs increases the temperature sensitivity of soil N2O emission in a Tibetan alpine meadow.Crossref | GoogleScholarGoogle Scholar |

Zhong L, Du R, Ding K, Kang X, Li FY, Bowatte S, Hoogendoorn CJ, Wang Y, Rui Y, Jiang L, Wang S (2014) Effects of grazing on N2O production potential and abundance of nitrifying and denitrifying microbial communities in meadow-steppe grassland in northern China. Soil Biology and Biochemistry 69, 1–10.
Effects of grazing on N2O production potential and abundance of nitrifying and denitrifying microbial communities in meadow-steppe grassland in northern China.Crossref | GoogleScholarGoogle Scholar |

Zhong L, Zhou X, Wang Y, Li FY, Zhou S, Bai Y, Rui Y (2017) Mixed grazing and clipping is beneficial to ecosystem recovery but may increase potential N2O emissions in a semi-arid grassland. Soil Biology and Biochemistry 114, 42–51.
Mixed grazing and clipping is beneficial to ecosystem recovery but may increase potential N2O emissions in a semi-arid grassland.Crossref | GoogleScholarGoogle Scholar |