Skip to main content
Log in

Manure fertilization enhanced microbial immigration in the wheat rhizosphere

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Microbial immigration is essential for understanding microbial mechanisms involved in nutrient cycling under different fertilization strategies. Here, we aimed to illustrate the effects of fertilization on microbial immigration in the wheat rhizosphere.

Materials and methods

Bacterial 16S rRNA gene and fungal ITS sequencing were applied to determine the microbial composition in the wheat rhizosphere. Co-occurrence networks, spatiotemporal source models, and structural equation models (SEMs) were conducted to investigate microbial immigration in two different niches (bulk soil and rhizosphere) and at two growth stages with different fertilization strategies (control without fertilization (CK), chemical fertilization (NPK), and organic manure fertilization (OM)).

Results and discussion

OM greatly decreased the network complexity ratio of the rhizosphere to bulk soil for bacteria (CK/NPK/OM ratio: 4.14/1.65/0.64) and fungi (CK/NPK/OM ratio: 1.09/1.35/0.72). The proportion of bacterial and fungal communities in the rhizosphere sourcing from the bulk soil was highest under OM treatment (94.34%; 88.78%), followed by NPK (88.69%; 83.86%) and CK (85.30%; 76.40%) treatments. The jointing stage contributed more than the flowering stage to microbial immigration. In comparison to fungi, the proportion of bacteria in the rhizosphere derived from the bulk soil was much higher. Structural equation model indicated that the increase of total carbon under OM treatment affected the composition of bacteria and fungi by promoting microbial immigration from the bulk soil to the rhizosphere.

Conclusions

OM treatment enhanced microbial immigration in the wheat rhizosphere, providing novel insights into plant-soil-microbiota interactions in the wheat rhizosphere.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AF, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi-recent updates and future perspectives. New Phytol 186(2):281–285

    Article  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open-source software for exploring and manipulating networks. Third International AAAI Conference on Weblogs and Social Media 3(1):361–362

    Google Scholar 

  • Bellemain E, Carlsen T, Brochmann C, Coissac E, Taberlet P, Kauserud H (2010) ITS as an environmental DNA barcode for fungi: an in-silico approach reveals potential PCR biases. BMC Microbiol 10:189

    Article  CAS  Google Scholar 

  • Blagodatskaya E, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fertil Soils 45:115–131

    Article  Google Scholar 

  • Blanco-Canqui H, Ferguson RB, Shapiro CA, Drijber RA, Walters DT (2014) Does inorganic nitrogen fertilization improve soil aggregation? Insights from two long-term tillage experiments. J Environ Qual 43:995–1003

    Article  CAS  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120

    Article  CAS  Google Scholar 

  • Cao Y, He Z, Zhu T, Zhao F (2021) Organic-C quality as a key driver of microbial nitrogen immobilization in soil: a meta-analysis. Geoderma 383:114784

  • Challacombe JF, Hesse CN, Bramer LM, McCue LA, Lipton M, Purvine S, Nicora C, Gallegos-Graves V, Porras-Alfaro A, Kuske CR (2019) Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis. BMC Genomics 20(1):976

    Article  CAS  Google Scholar 

  • Chen S, Waghmode TR, Sun R, Kuramae EE, Hu C, Liu B (2019) Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization. Microbiome 7:136

    Article  CAS  Google Scholar 

  • Deng Y, Jiang Y, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinformatics 13:113

    Article  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

    Article  CAS  Google Scholar 

  • Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA 112:E911–E920

    Article  CAS  Google Scholar 

  • Essel E, Xie J, Deng C, Peng Z, Wang J, Shen J, Xie J, Coulter JA, Li L (2019) Bacterial and fungal diversity in rhizosphere and bulk soil under different long-term tillage and cereal/legume rotation. Soil Tillage Res 194(3):1–11

    Google Scholar 

  • Fan K, Weisenhorn P, Gilbert JA, Chu H (2018) Wheat rhizosphere harbors a less complex and more stable microbial co-occurrence pattern than bulk soil. Soil Biol Biochem 125:251–260

    Article  CAS  Google Scholar 

  • Feng J, Zhu B (2021) Global patterns and associated drivers of priming effect in response to nutrient addition. Soil Biol Biochem 153:108–118

    Article  CAS  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  Google Scholar 

  • Fliessbach A, Oberholzer H, Gunst L, Maeder P (2007) Soil organic matter and biological soil quality indicators after 21 years of organic and conventional farming. Agric Ecosyst Environ 118:273–284

    Article  Google Scholar 

  • Haichar FEZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230

    Article  CAS  Google Scholar 

  • Han Q, Ma Q, Chen Y, Tian B, Xu L, Bai Y, Chen W, Li X (2020) Variation in rhizosphere microbial communities and its association with the symbiotic efficiency of rhizobia in soybean. ISME J 14(8):1915–1928

    Article  CAS  Google Scholar 

  • Hartmann M, Frey B, Mayer J, Maeder P, Widmer F (2015) Distinct soil microbial diversity under long-term organic and conventional farming. ISME J 9:1177–1194

    Article  Google Scholar 

  • Houlden A, Timms-Wilson TM, Day MJ, Bailey MJ (2008) Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops. FEMS Microbiol Ecol 65:193–201

    Article  CAS  Google Scholar 

  • Hu L, Robert CAM, Cadot S, Zhang X, Ye M, Li B, Manzo D, Chervet N, Steinger T, van der Heijden MGA, Schlaeppi K, Erb M (2018) Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun 9(1):2738

    Article  CAS  Google Scholar 

  • Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198(3):656–669

    Article  CAS  Google Scholar 

  • Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130

    Article  CAS  Google Scholar 

  • Li YC, Li YF, Chang SX, Yang YF, Fu SL, Jiang PK, Luo Y, Yang M, Chen ZH, Hu SD, Zhao MX, Liang X, Xu QF, Zhou GM, Zhou JZ (2018) Biochar reduces soil heterotrophic respiration in a subtropical plantation through increasing soil organic carbon recalcitrancy and decreasing carbon-degrading microbial activity. Soil Biol Biochem 122:173–185

    Article  CAS  Google Scholar 

  • Lundberg DS, Teixeira PJPL (2018) Root-exuded coumarin shapes the root microbiome. Proc Natl Acad Sci USA 115:5629–5631

    Article  CAS  Google Scholar 

  • Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963

    Article  CAS  Google Scholar 

  • Mau RL, Liu CM, Aziz M, Schwartz E, Dijkstra P, Marks JC, Price LB, Keim P, Hungate BA (2015) Linking soil bacterial biodiversity and soil carbon stability. ISME J 9:1477–1480

    Article  CAS  Google Scholar 

  • Mei R, Liu W (2019) Quantifying the contribution of microbial immigration in engineered water systems. Microbiome 7(1):144

    Article  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2020) The vegan package version 2.5–2. Community Ecol package. https://cran.r-project.org/web/packages/vegan

  • Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799

    Article  CAS  Google Scholar 

  • Pontes AP, Souza RD, Granada CE, Passaglia LMP (2015) Screening of plant growth promoting bacteria associated with barley plants (Hordeum vulgare L.) cultivated in South Brazil. Biota Neotropica 15(2):e20140105

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596

    Article  CAS  Google Scholar 

  • Schmidt JE, Kent AD, Brisson VL, Gaudin ACM (2019) Agricultural management and plant selection interactively affect rhizosphere microbial community structure and nitrogen cycling. Microbiome 7:164

    Article  Google Scholar 

  • Setala H, McLean MA (2004) Decomposition rate of organic substrates in relation to the species diversity of soil saprophytic fungi. Oecologia 139:98–107

    Article  Google Scholar 

  • Shenhav L, Thompson M, Joseph TA, Briscoe L, Furman O, Bogumil D, Mizrahi I, Pe’Er I, Halperin E (2019) FEAST: fast expectation-maximization for microbial source tracking. Nat Methods 16:627

    Article  CAS  Google Scholar 

  • Shi S, Nuccio EE, Shi ZJ, He Z, Zhou J, Firestone MK (2016) The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett 19(8):926–936

    Article  Google Scholar 

  • Shi Y, Delgado-Baquerizo M, Li Y, Yang Y, Zhu Y, Penuelas J, Chu H (2020) Abundance of kinless hubs within soil microbial networks are associated with high functional potential in agricultural ecosystems. Environ Int 142:105869

  • Sloan WT, Lunn M, Woodcock S, Head IM, Nee S, Curtis TP (2006) Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ Microbiol 8:732–740

    Article  Google Scholar 

  • Sul WJ, Asuming-Brempong S, Wang Q, Tourlousse DM, Penton CR, Deng Y, Rodrigues JLM, Adiku SGK, Jones JW, Zhou J, Cole JR, Tiedje JM (2013) Tropical agricultural land management influences on soil microbial communities through its effect on soil organic carbon. Soil Biol Biochem 65:33–38

    Article  CAS  Google Scholar 

  • Sun R, Chen Y, Han W, Dong W, Zhang Y, Hu C, Liu B, Wang F (2020) Different contribution of species sorting and exogenous species immigration from manure to soil fungal diversity and community assemblage under long-term fertilization. Soil Biol Biochem 151:108049

  • Tamaki H, Wright CL, Li X, Lin Q, Hwang C, Wang S, Thimmapuram J, Kamagata Y, Liu W (2011) Analysis of 16S rRNA amplicon sequencing options on the Roche/454 next-generation titanium sequencing platform. PLoS One 6(9):e25263

  • Tao C, Li R, Xiong W, Shen Z, Liu S, Wang B, Ruan Y, Geisen S, Shen Q, Kowalchuk GA (2020) Bio-organic fertilizers stimulate indigenous soil Pseudomonas populations to enhance plant disease suppression. Microbiome 8(1):137

    Article  CAS  Google Scholar 

  • Vejan P, Abdullah R, Khadiran T, Ismail S, Boyce AN (2016) Role of plant growth promoting Rhizobacteria in agricultural sustainability—a review. Molecules 21(5):573

    Article  CAS  Google Scholar 

  • Veresoglou SD, Halley JM, Rillig MC (2015) Extinction risk of soil biota. Nat Commun 6:8862

    Article  CAS  Google Scholar 

  • Větrovský T, Steffen KT, Baldrian P, Freitag M (2014) Potential of cometabolic transformation of polysaccharides and lignin in lignocellulose by soil Actinobacteria. PLoS One 9:e89108

  • Wagg C, Schlaeppi K, Banerjee S, Kuramae EE, van der Heijden MGA (2019) Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat Commun 10:4841

    Article  CAS  Google Scholar 

  • Wattenburger CJ, Halverson LJ, Hofmockel KS (2019) Agricultural management affects root-associated microbiome recruitment over maize development. Phytobiomes J 3:260–272

    Article  Google Scholar 

  • Wu X, Liu Y, Shang Y, Liu D, Liesack W, Cui Z, Peng J, Zhang F (2021) Peat-vermiculite alters microbiota composition towards increased soil fertility and crop productivity. Plant Soil 470:21–34

    Article  CAS  Google Scholar 

  • Xiong C, Zhu Y, Wang J, Singh B, Han L, Shen J, Li P, Wang G, Wu C, Ge A, Zhang L, He J (2021) Host selection shapes crop microbiome assembly and network complexity. New Phytol 229:1091–1104

    Article  CAS  Google Scholar 

  • Xun W, Liu Y, Li W, Ren Y, Xiong W, Xu Z, Zhang N, Miao Y, Shen Q, Zhang R (2021) Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome 9(1):35

    Article  CAS  Google Scholar 

  • Yang Y, Li X, Liu J, Zhou Z, Zhang T, Wang X (2020) Fungal community structure in relation to manure rate in red soil in southern China. Appl Soil Ecol 147:103442

Download references

Funding

This study was financially supported by the National Key Research and Development Program of China (2021YFD1900100), the Project for the China Agricultural University (2020TC050 & 2020TC144), and the Program of Advanced Discipline Construction in Beijing, and 2115 Talent Development Program of China Agricultural University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jingjing Peng.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible editor: Hang-Wei Hu

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 385 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y., Bei, S., Olatunde, O. et al. Manure fertilization enhanced microbial immigration in the wheat rhizosphere. J Soils Sediments 22, 1828–1837 (2022). https://doi.org/10.1007/s11368-022-03185-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-022-03185-0

Keywords

Navigation