Two years of nitrogen addition altered soil microbial community structure and function in a desert steppe of northern China
Xiongkui Lin A # , Bo Wang A # , Xudong Wu B , Jing Liu A , Zihao Zhang A , Lingfei Xiang A and Zhigang Li
A C *
+ Author Affiliations
- Author Affiliations
A School of Agriculture, Ningxia University, Yinchuan, Ningxia 7500021, China.
B Institute of Desertification Control, Ningxia Academy of Agricultural and Forestry Sciences, Yinchuan, Ningxia 750021, China.
C Ningxia Grassland and Animal Husbandry Engineering Technology Research Centre, Yinchuan, Ningxia 750021, China.
* Correspondence to: lizg001@sina.com
# These authors contributed equally to this paper
Handling Editor: Mark Farrell
Soil Research 61(4) 345-356 https://doi.org/10.1071/SR22139
Submitted: 9 June 2022 Accepted: 14 November 2022 Published: 1 December 2022
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Although nitrogen (N) deposition application has resulted in excess N entering grassland ecosystems, our understanding of how short-term N enrichment affects soil microbial community in a desert steppe is incomplete.
Aims: This study assessed the effects of 2 years of N addition on structure and function of soil microbial community at the soil depth of 0–10 cm in a desert steppe.
Methods: Six addition rates of N (equivalent to 0, 5, 10, 15, 20 and 40 g N m−2 year−1) were applied in a desert steppe of northern China, and the 16S rRNA and ITS1 genes were sequenced for the prokaryotic and fungal communities, respectively.
Key results: N addition altered prokaryotic taxa composition, but not fungal taxa composition and α-diversities of prokaryotic and fungal communities. N shifted microbial β-diversities, and prokaryotic β-diversity was more sensitive than fungal β-diversity. Abundances of predicted prokaryotic functions decreased as N rates increased, whereas predicted fungal functions presented no obvious variations among N additions. Predicted enzyme activities related to N cycling in prokaryotes were similar to fungi, but variations of C and P cycling-related enzyme activities were opposite to fungi. Additionally, phylum abundance, α-diversity, and β-diversity of prokaryotes were more closely influenced by soil and plant properties than fungi.
Conclusions: Two years of N addition altered both microbial community structure and function, but the prokaryotic community responded more sensitive than the fungal community.
Implications: Topsoil should be considered when exploring the impact of short-term N addition on soil microbial community in the desert steppe.
Keywords: 2-year nitrogen addition, C cycling, desert steppe, microbial community composition, microbial community diversity, N cycling, P cycling, predicted enzyme activities, predicted microbial function.
References
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581–583.| DADA2: high-resolution sample inference from Illumina amplicon data.Crossref | GoogleScholarGoogle Scholar |
Chen X, Hao B, Jing X, He J-S, Ma W, Zhu B (2019) Minor responses of soil microbial biomass, community structure and enzyme activities to nitrogen and phosphorus addition in three grassland ecosystems. Plant and Soil 444, 21–37.
| Minor responses of soil microbial biomass, community structure and enzyme activities to nitrogen and phosphorus addition in three grassland ecosystems.Crossref | GoogleScholarGoogle Scholar |
Chen W, Zhou H, Wu Y, Wang J, Zhao Z, Li Y, Qiao L, Chen K, Liu G, Xue S (2020) Direct and indirect influences of long-term fertilisation on microbial carbon and nitrogen cycles in an alpine grassland. Soil Biology and Biochemistry 149, 107922
| Direct and indirect influences of long-term fertilisation on microbial carbon and nitrogen cycles in an alpine grassland.Crossref | GoogleScholarGoogle Scholar |
Chun L, Han WJ, Wang H, Na RS (2015) Effect of fertilisations on vegetation of the degraded desert steppe. Grassland and Prataculture 27, 22–26.
Cusack DF, Silver WL, Torn MS, Burton SD, Firestone MK (2011) Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92, 621–632.
| Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests.Crossref | GoogleScholarGoogle Scholar |
Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecology Letters 12, 1238–1249.
| Global patterns in belowground communities.Crossref | GoogleScholarGoogle Scholar |
Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. The ISME Journal 6, 1007–1017.
| Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients.Crossref | GoogleScholarGoogle Scholar |
Guo D, Fan Z, Lu S, Ma Y, Nie X, Tong F, Peng X (2019) Changes in rhizosphere bacterial communities during remediation of heavy metal-accumulating plants around the Xikuangshan mine in southern China. Scientific Reports 9, 1947
| Changes in rhizosphere bacterial communities during remediation of heavy metal-accumulating plants around the Xikuangshan mine in southern China.Crossref | GoogleScholarGoogle Scholar |
Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075.
| QUAST: quality assessment tool for genome assemblies.Crossref | GoogleScholarGoogle Scholar |
He D, Li XL, Wan LQ, He F, Li CR (2009) Influence of urea application on aboveground biomass and important value of the species in the degraded grassland. Act Prataculturae Sinica 18, 154–158.
| Influence of urea application on aboveground biomass and important value of the species in the degraded grassland.Crossref | GoogleScholarGoogle Scholar |
Huang J, Xu Y, Yu H, Zhu W, Wang P, Wang B, Na X (2021) Soil prokaryotic community shows no response to 2 years of simulated nitrogen deposition in an arid ecosystem in northwestern China. Environmental Microbiology 23, 1222–1237.
| Soil prokaryotic community shows no response to 2 years of simulated nitrogen deposition in an arid ecosystem in northwestern China.Crossref | GoogleScholarGoogle Scholar |
Institute of Soil Science, Chinese Academy of Sciences (ISSCAS) (1978) ‘Physical and chemical analysis methods of soils.’ (China Shanghai Science Technology Press: Shanghai)
Jia M, Gao Z, Gu H, Zhao C, Liu M, Liu F, Xie L, Wang L, Zhang G, Liu Y, Han G (2021) Effects of precipitation change and nitrogen addition on the composition, diversity, and molecular ecological network of soil bacterial communities in a desert steppe. PLoS ONE 16, e0248194
| Effects of precipitation change and nitrogen addition on the composition, diversity, and molecular ecological network of soil bacterial communities in a desert steppe.Crossref | GoogleScholarGoogle Scholar |
Jianbo W, Na L, Xiaodan W (2020) Nitrogen deposition strengthens the relationship between plants and the soil fungal community in alpine steppe, North Tibet. Applied Soil Ecology 147, 103441
| Nitrogen deposition strengthens the relationship between plants and the soil fungal community in alpine steppe, North Tibet.Crossref | GoogleScholarGoogle Scholar |
Kaiser C, Franklin O, Dieckmann U, Richter A (2014) Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecology Letters 17, 680–690.
| Microbial community dynamics alleviate stoichiometric constraints during litter decay.Crossref | GoogleScholarGoogle Scholar |
Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson K-H (2013) Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology 22, 5271–5277.
| Towards a unified paradigm for sequence-based identification of fungi.Crossref | GoogleScholarGoogle Scholar |
Li Y, Bezemer TM, Yang J, Lü X, Li X, Liang W, Han X, Li Q (2019) Changes in litter quality induced by N deposition alter soil microbial communities. Soil Biology and Biochemistry 130, 33–42.
| Changes in litter quality induced by N deposition alter soil microbial communities.Crossref | GoogleScholarGoogle Scholar |
Li B, Xu R, Sun X, Han F, Xiao E, Chen L, Qiu L, Sun W (2021) Microbiome–environment interactions in antimony-contaminated rice paddies and the correlation of core microbiome with arsenic and antimony contamination. Chemosphere 263, 128227
| Microbiome–environment interactions in antimony-contaminated rice paddies and the correlation of core microbiome with arsenic and antimony contamination.Crossref | GoogleScholarGoogle Scholar |
Liu W, Liu L, Yang X, Deng M, Wang Z, Wang P, Yang S, Li P, Peng Z, Yang L, Jiang L (2021) Long-term nitrogen input alters plant and soil bacterial, but not fungal beta diversity in a semiarid grassland. Global Change Biology 27, 3939–3950.
| Long-term nitrogen input alters plant and soil bacterial, but not fungal beta diversity in a semiarid grassland.Crossref | GoogleScholarGoogle Scholar |
Luo R, Luo J, Fan J, Liu D, He J-S, Perveen N, Ding W (2020) Responses of soil microbial communities and functions associated with organic carbon mineralisation to nitrogen addition in a Tibetan grassland. Pedosphere 30, 214–225.
| Responses of soil microbial communities and functions associated with organic carbon mineralisation to nitrogen addition in a Tibetan grassland.Crossref | GoogleScholarGoogle Scholar |
McHugh TA, Morrissey EM, Mueller RC, Gallegos-Graves LV, Kuske CR, Reed SC (2017) Bacterial, fungal, and plant communities exhibit no biomass or compositional response to two years of simulated nitrogen deposition in a semiarid grassland. Environmental Microbiology 19, 1600–1611.
| Bacterial, fungal, and plant communities exhibit no biomass or compositional response to two years of simulated nitrogen deposition in a semiarid grassland.Crossref | GoogleScholarGoogle Scholar |
Meiqing J, Jing H, Yinghua Y, Guodong H, Guogang Z (2019) Effects of simulated nitrogen deposition and precipitation manipulation on soil microorganisms in the desert Steppe of northern China. Revista Brasileira de Ciência do Solo 43, e0180031
| Effects of simulated nitrogen deposition and precipitation manipulation on soil microorganisms in the desert Steppe of northern China.Crossref | GoogleScholarGoogle Scholar |
Moore JAM, Anthony MA, Pec GJ, Trocha LK, Trzebny A, Geyer KM, van Diepen LTA, Frey SD (2021) Fungal community structure and function shifts with atmospheric nitrogen deposition. Global Change Biology 27, 1349–1364.
| Fungal community structure and function shifts with atmospheric nitrogen deposition.Crossref | GoogleScholarGoogle Scholar |
Mueller RC, Belnap J, Kuske CR (2015) Soil bacterial and fungal community responses to nitrogen addition across soil depth and microhabitat in an arid shrubland. Frontiers in Microbiology 6, 891
| Soil bacterial and fungal community responses to nitrogen addition across soil depth and microhabitat in an arid shrubland.Crossref | GoogleScholarGoogle Scholar |
Niu G, Hasi M, Wang R, Wang Y, Geng Q, Hu S, Xu X, Yang J, Wang C, Han X, Huang J (2021) Soil microbial community responses to long-term nitrogen addition at different soil depths in a typical steppe. Applied Soil Ecology 167, 104054
| Soil microbial community responses to long-term nitrogen addition at different soil depths in a typical steppe.Crossref | GoogleScholarGoogle Scholar |
Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. The ISME Journal 4, 1340–1351.
| Soil bacterial and fungal communities across a pH gradient in an arable soil.Crossref | GoogleScholarGoogle Scholar |
Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B, Richter A, Eberl L, Zechmeister-Boltenstern S, Riedel K (2012) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. The ISME Journal 6, 1749–1762.
| Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions.Crossref | GoogleScholarGoogle Scholar |
Sha M, Xu J, Zheng Z, Fa K (2021) Enhanced atmospheric nitrogen deposition triggered little change in soil microbial diversity and structure in a desert ecosystem. Global Ecology and Conservation 31, e01879
| Enhanced atmospheric nitrogen deposition triggered little change in soil microbial diversity and structure in a desert ecosystem.Crossref | GoogleScholarGoogle Scholar |
Sinsabaugh RL, Belnap J, Rudgers J, Kuske CR, Martinez N, Sandquist D (2015) Soil microbial responses to nitrogen addition in arid ecosystems. Frontiers in Microbiology 6, 819
| Soil microbial responses to nitrogen addition in arid ecosystems.Crossref | GoogleScholarGoogle Scholar |
Wang C, Liu D, Bai E (2018) Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition. Soil Biology and Biochemistry 120, 126–133.
| Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition.Crossref | GoogleScholarGoogle Scholar |
Wang Q, Ma M, Jiang X, Guan D, Wei D, Zhao B, Chen S, Cao F, Li L, Yang X, Li J (2019) Impact of 36 years of nitrogen fertilisation on microbial community composition and soil carbon cycling-related enzyme activities in rhizospheres and bulk soils in northeast China. Applied Soil Ecology 136, 148–157.
| Impact of 36 years of nitrogen fertilisation on microbial community composition and soil carbon cycling-related enzyme activities in rhizospheres and bulk soils in northeast China.Crossref | GoogleScholarGoogle Scholar |
Wei H-W, Wang X-G, Li Y-B, Yang J-J, Wang J-F, Lü X-T, Han X-G (2020) Simulated nitrogen deposition decreases soil microbial diversity in a semiarid grassland, with little mediation of this effect by mowing. Pedobiologia 80, 150644
| Simulated nitrogen deposition decreases soil microbial diversity in a semiarid grassland, with little mediation of this effect by mowing.Crossref | GoogleScholarGoogle Scholar |
Widdig M, Heintz-Buschart A, Schleuss P-M, Guhr A, Borer ET, Seabloom EW, Spohn M (2020) Effects of nitrogen and phosphorus addition on microbial community composition and element cycling in a grassland soil. Soil Biology and Biochemistry 151, 108041
| Effects of nitrogen and phosphorus addition on microbial community composition and element cycling in a grassland soil.Crossref | GoogleScholarGoogle Scholar |
Wu Q, Ren H, Wang Z, Li Z, Liu Y, Wang Z, Li Y, Zhang R, Zhao M, Chang SX, Han G (2020) Additive negative effects of decadal warming and nitrogen addition on grassland community stability. Journal of Ecology 108, 1442–1452.
| Additive negative effects of decadal warming and nitrogen addition on grassland community stability.Crossref | GoogleScholarGoogle Scholar |
Wu Q, Ren H, Bisseling T, Chang SX, Wang Z, Li Y, Pan Z, Liu Y, Cahill JF, Cheng X, Zhao M, Wang Z, Li Z, Han G (2021) Long-term warming and nitrogen addition have contrasting effects on ecosystem carbon exchange in a desert Steppe. Environmental Science & Technology 55, 7256–7265.
| Long-term warming and nitrogen addition have contrasting effects on ecosystem carbon exchange in a desert Steppe.Crossref | GoogleScholarGoogle Scholar |
Xiao J, Lu S, Wei Z, Zhang S, Bai Y (2017) Response of community diversity of Stipa breviflora in desert steppe to fertilisation. Chinese Journal of Grassland 39, 84–89.
| Response of community diversity of Stipa breviflora in desert steppe to fertilisation.Crossref | GoogleScholarGoogle Scholar |
Xing W, Lu X, Ying J, Lan Z, Chen D, Bai Y (2022) Disentangling the effects of nitrogen availability and soil acidification on microbial taxa and soil carbon dynamics in natural grasslands. Soil Biology and Biochemistry 164, 108495
| Disentangling the effects of nitrogen availability and soil acidification on microbial taxa and soil carbon dynamics in natural grasslands.Crossref | GoogleScholarGoogle Scholar |
Yang Y, Cheng H, Gao H, An S (2020) Response and driving factors of soil microbial diversity related to global nitrogen addition. Land Degradation & Development 31, 190–204.
| Response and driving factors of soil microbial diversity related to global nitrogen addition.Crossref | GoogleScholarGoogle Scholar |
Yang X, Liu Y, Tian H, Shen Y (2021) Short-term nitrogen and phosphorus additions rather than mycorrhisal suppression determine plant community composition and productivity in desert steppe. Applied Soil Ecology 168, 104144
| Short-term nitrogen and phosphorus additions rather than mycorrhisal suppression determine plant community composition and productivity in desert steppe.Crossref | GoogleScholarGoogle Scholar |
Yao M, Rui J, Li J, Dai Y, Bai Y, Heděnec P, Wang J, Zhang S, Pei K, Liu C, Wang Y, He Z, Frouz J, Li X (2014) Rate-specific responses of prokaryotic diversity and structure to nitrogen deposition in the Leymus chinensis steppe. Soil Biology and Biochemistry 79, 81–90.
| Rate-specific responses of prokaryotic diversity and structure to nitrogen deposition in the Leymus chinensis steppe.Crossref | GoogleScholarGoogle Scholar |
Yayi N, Yulong D, Yuqiang L, Xuyang W, Yun C, Lilong W (2021) Soil microbial community responses to short-term nitrogen addition in China’s Horqin Sandy Land. PLoS ONE 16, e0242643
| Soil microbial community responses to short-term nitrogen addition in China’s Horqin Sandy Land.Crossref | GoogleScholarGoogle Scholar |
Yu Y, Liu L, Zhao J, Wang S, Zhou Y, Xiao C (2022) The diversity and function of soil bacteria and fungi under altered nitrogen and rainfall patterns in a temperate Steppe. Frontiers in Microbiology 13, 906818
| The diversity and function of soil bacteria and fungi under altered nitrogen and rainfall patterns in a temperate Steppe.Crossref | GoogleScholarGoogle Scholar |
Zhao Y, Zhang L, Chen Y, Liu X, Xu W, Pan Y, Duan L (2017) Atmospheric nitrogen deposition to China: a model analysis on nitrogen budget and critical load exceedance. Atmospheric Environment 153, 32–40.
| Atmospheric nitrogen deposition to China: a model analysis on nitrogen budget and critical load exceedance.Crossref | GoogleScholarGoogle Scholar |
Zhou J, Ning D (2017) Stochastic community assembly: does it matter in microbial ecology? Microbiology and Molecular Biology Reviews 81, e00002–e00017.
| Stochastic community assembly: does it matter in microbial ecology?Crossref | GoogleScholarGoogle Scholar |
