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Responses of soil microbiota and nematodes to application of organic and inorganic fertilizers in grassland columns


Enhancing the role of the soil microbiota in plant phosphorus (P) and sulfur (S) supply through application of organic fertilizer could reduce dependencies on non-sustainable synthetic fertilizers. To compare the effects of organic/inorganic fertilizers on the soil microbiota, soil columns with Lolium perenne (ryegrass) were set up in a greenhouse and amended with an inorganic fertilizer, cattle slurry (organic), or urea (P- and S-free control). Ryegrass rhizosphere of the slurry treatment had significantly higher abundances of bacterial feeding nematodes, mycorrhizal colonization, cultivable heterotrophic bacteria, phosphonate- and sulfonate-utilizing bacteria, arylsulfatase activity, available P, and Variovorax asfA gene copies compared to the inorganic and urea treatments. Phosphomonoesterase activities, and gene abundances involved in organic P and S transformations (phoD, phoC, Burkholderia, and Polaromonas asfA) were similar in all treatments. Grass dry matter yield and shoot uptake of N, P, and S were significantly higher in the inorganic treatment compared to the urea and slurry treatments. Community compositions differed significantly between the three fertilizer treatments and included the bacterial, alkaline phosphomonoesterase-producing bacterial, fungal, AM fungal, and nematode communities. Bacteriodetes were found in higher relative abundance in the organic treatment, while Acidobacteria were more abundant in the urea and inorganic fertilizer treatments. These community shifts correlated significantly with grass dry matter yield, uptake of N, P, and S, mycorrhizal colonization, enzyme activities, abundances of bacteria, and bacterial feeding nematodes. We concluded that organic fertilization promoted soil microbes and nematodes which have the potential to support sustainable plant growth, provided that the overall nutrient requirements are met.

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  1. Abubaker J, Risberg K, Pell M (2012) Biogas residues as fertilisers—effects on wheat growth and soil microbial activities. Appl Energy 99:126–134

  2. Acosta-Martínez V, Cotton J, Gardner T, Moore-Kucera J, Zak J, Wester D, Cox S (2014) Predominant bacterial and fungal assemblages in agricultural soils during a record drought/heat wave and linkages to enzyme activities of biogeochemical cycling. Appl Soil Ecol 84:69–82

  3. Andrássy I (1984) Klasse Nematoda:(Ordnungen Monhysterida, Desmoscolecida, Araeolaimida, Chromadorida, Rhabditida). Akademie-Verlag, Berlin

  4. Apel AK, Sola-Landa A, Rodríguez-García A, MartíN JF (2007) Phosphate control of phoA, phoC and phoD gene expression in Streptomyces coelicolor reveals significant differences in binding of PhoP to their promoter regions. Microbiology 153:3527–3537

  5. Bardgett RD, Griffiths BS (1997) Ecology and biology of soil protozoa, nematodes and microarthropods. In: Van Elsas J, Trevors J, Wellington EW (eds) Modern soil microbiology. Marcel Dekker, New York, pp 129–164

  6. Baum C, Makeschin F (2000) Effects of nitrogen and phosphorus fertilization on mycorrhizal formation of two poplar clones (Populus trichocarpa and P. tremula x tremuloides). J Plant Nutr Soil Sci 163:491–497

  7. Bentivenga S, Hetrick B (1992) The effect of prairie management practices on mycorrhizal symbiosis. Mycologia 84:522–527

  8. Bi QF, Li KJ, Zheng BX, Zheng BX, Liu XP, Li HZ, Jin BJ, Ding K, Yang XR, Lin XY, Zhu YG (2020) Partial replacement of inorganic phosphorus (P) by organic manure reshapes phosphate mobilizing bacterial community and promotes P bioavailability in a paddy soil. Sci Total Environ 703:134977

  9. Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Caporaso JG (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6:90

  10. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver L, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS 2nd, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft J, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857

  11. Bongers T (1988) De nematoden van Nederland; een identificatietabel voor de in Nederland aangetroffen zoetwater-en bodembewonende nematoden

  12. Cai F, Pang G, Li R-X, Li R, Gu X-L, Shen Q-R, Chen W (2017) Bioorganic fertilizer maintains a more stable soil microbiome than chemical fertilizer for monocropping. Biol Fertil Soils 53:861–872

  13. Calderon FJ, Mccarty GW, Van Kessel JAS, Reeves JB (2004) Carbon and nitrogen dynamics during incubation of manured soil. Soil Sci Soc Am J 68:1592–1599

  14. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583

  15. Chardon W, Aalderink G, Van Der Salm C (2007) Phosphorus leaching from cow manure patches on soil columns. J Environ Qual 36:17–22

  16. Chee-Sanford JC, Mackie RI, Koike S, Krapac IG, Lin YF, Yannarell AC, Maxwell S, Aminov RI (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 38:1086–1108

  17. Chen Y, Camps-Arbestain M, Shen Q, Singh B, Cayuela ML (2018) The long-term role of organic amendments in building soil nutrient fertility: a meta-analysis and review. Nutr Cycl Agroecosyst 111:103–125

  18. Chhabra S, Brazil D, Morrissey J, Burke J, O’Gara F, Dowling DN (2013) Fertilization management affects the alkaline phosphatase bacterial community in barley rhizosphere soil. Biol Fertil Soils 49:31–39

  19. Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252

  20. Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305

  21. Delgado MJ, Casella S, Bedmar EJ (2007) Denitrification in rhizobia-legume symbiosis. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, Amsterdam, pp 3–20

  22. Dordas CA, Lithourgidis AS, Matsi T, Barbayiannis N (2008) Application of liquid cattle manure and inorganic fertilizers affect dry matter, nitrogen accumulation, and partitioning in maize. Nutr Cycl Agroecosyst 80:283–296

  23. Elser JJ (2012) Phosphorus: a limiting nutrient for humanity? Curr Opin Biotechnol 23:833–838

  24. Estrada-De Los Santos P, Bustillos-Cristales R, Caballero-Mellado J (2001) Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol 67:2790–2798

  25. Fageria N, Baligar V (2005) Enhancing nitrogen use efficiency in crop plants. Adv Agron 88:97–185

  26. Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10

  27. Ferris H, Venette RC, Scow KM (2004) Soil management to enhance bacterivore and fungivore nematode populations and their nitrogen mineralization function. Appl Soil Ecol 24:19–35

  28. Forge T, Bittman S, Kowalenko C (2005) Responses of grassland soil nematodes and protozoa to multi-year and single-year applications of dairy manure slurry and fertilizer. Soil Biol Biochem 37:1751–1762

  29. Fowler D, Smith R, Muller J, Hayman G, Vincent K (2005) Changes in the atmospheric deposition of acidifying compounds in the UK between 1986 and 2001. Environ Pollut 137:15–25

  30. Fox A, Ikoyi I, Creamer R, Lanigan G, Schmalenberger A (2017) Microbial community structure and function respond more strongly to temporal progression than to the application of slurry in an Irish grassland. Appl Soil Ecol 120:97–104

  31. Fox A, Kwapinski W, Griffiths BS, Schmalenberger A (2014) The role of sulfur-and phosphorus-mobilizing bacteria in biochar-induced growth promotion of Lolium perenne. FEMS Microbiol Ecol 90:78–91

  32. Fraser T, Lynch DH, Entz MH, Dunfield KE (2015a) Linking alkaline phosphatase activity with bacterial phoD gene abundance in soil from a long-term management trial. Geoderma 257:115–122

  33. Fraser TD, Lynch DH, Bent E, Entz MH, Dunfield KE (2015b) Soil bacterial phoD gene abundance and expression in response to applied phosphorus and long-term management. Soil Biol Biochem 88:137–147

  34. Fraser TD, Lynch DH, Gaiero J, Khosla K, Dunfield KE (2017) Quantification of bacterial non-specific acid (phoC) and alkaline (phoD) phosphatase genes in bulk and rhizosphere soil from organically managed soybean fields. Appl Soil Ecol 111:48–56

  35. Gandhi NU, Chandra SB (2012) A comparative analysis of three classes of bacterial non-specific acid phosphatases and archaeal phosphoesterases: evolutionary perspective. Acta Inform Med 20:167-173

  36. Gansauge MT, Meyer M (2013) Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nat Protoc 8:737–748

  37. Gebremikael MT, Steel H, Buchan D, Bert W, De Neve S (2016) Nematodes enhance plant growth and nutrient uptake under C and N-rich conditions. Sci Rep 6:32862

  38. Griffiths BS, Wheatley R, Olesen T, Henriksen K, Ekelund F, Rønn R (1998) Dynamics of nematodes and protozoa following the experimental addition of cattle or pig slurry to soil. Soil Biol Biochem 30:1379–1387

  39. Harris J, Tyrrel S, Ritz K, Lanigan G, Griffiths B, Brennan F, Bourdin F, Massey P, Moynihan E, Rogers N (2011) Does soil biology hold the key to optimized slurry management? A manifesto for research. Soil Use Manag 27:464–469

  40. Hartman WH, Richardson CJ (2013) Differential nutrient limitation of soil microbial biomass and metabolic quotients (qCO2): is there a biological stoichiometry of soil microbes? PLoS One 8:e57127

  41. Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218

  42. Haynes R, Williams P (1993) Nutrient cycling and soil fertility in the grazed pasture ecosystem. Adv Agron 49:119–199

  43. Hejna M, Gottardo D, Baldi A, Dell’Orto V, Cheli F, Zaninelli M, Rossi L (2018) Review: nutritional ecology of heavy metals. Animal 12:2156–2170

  44. Holden N, Fitzgerald D, Ryan D, Tierney H, Murphy F (2004) Rainfall climate limitation to slurry spreading in Ireland. Agric For Meteorol 122:207–214

  45. Ikoyi I, Fowler A, Schmalenberger A (2018) One-time phosphate fertilizer application to grassland columns modifies the soil microbiota and limits its role in ecosystem services. Sci Total Environ 630:849–858

  46. Ikoyi I, Fowler A, Storey S, Doyle E, Schmalenberger A (2020) Sulfate fertilization supports growth of ryegrass in soil columns but changes microbial community structures and reduces abundances of nematodes and arbuscular mycorrhiza. Sci Total Environ 704: 135315.

  47. Ingham E, Trofymow J, Ames R, Hunt H, Morley C, Moore J, Coleman D (1986) Trophic interactions and nitrogen cycling in a semi-arid grassland soil. II. System responses to removal of different groups of soil microbes or fauna. J Appl Ecol 23:615–630

  48. Ingham RE, Trofymow J, Ingham ER, Coleman DC (1985) Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecol Monogr 55:119–140

  49. Irshad U, Villenave C, Brauman A, Plassard C (2011) Grazing by nematodes on rhizosphere bacteria enhances nitrate and phosphorus availability to Pinus pinaster seedlings. Soil Biol Biochem 43:2121–2126

  50. Istina IN, Widiastuti H, Joy B, Antralina M (2015) Phosphate solubilizing microbe from Saprists peat soil and their potency to enhance oil palm growth and P uptake. Procedia Food Sci 3:426–435

  51. Jairajpuri MS, Ahmad W (1992) Dorylaimida: free-living, predaceous and plant-parasitic nematodes. Oxford and IBH Publishing Co., Delhi

  52. Jiang Y, Liu M, Zhang J, Chen Y, Chen X, Chen L, Li H, Zhang XX, Sun B (2017) Nematode grazing promotes bacterial community dynamics in soil at the aggregate level. ISME J 11:2705–2717

  53. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

  54. Kertesz MA, Mirleau P (2004) The role of soil microbes in plant sulphur nutrition. J Exp Bot 55:1939–1945

  55. Kircher M, Sawyer S, Meyer M (2012) Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Res 40:e3

  56. Lidbury IDEA, Murphy ARJ, Scanlan DJ, Bending GD, Jones AME, Moore JD, Goodall A, Hammond JP, Wellington EMH (2016) Comparative genomic, proteomic and exoproteomic analyses of three Pseudomonas strains reveals novel insights into the phosphorus scavenging capabilities of soil bacteria. Environ Microbiol 18:3535–3549

  57. Lori M, Symnaczik S, Mäder P, De Deyn G, Gattinger A (2017) Organic farming enhances soil microbial abundance and activity—a meta-analysis and meta-regression. PLoS One 12:e0180442

  58. Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73:1576–1585

  59. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

  60. Marschner P, Kandeler E, Marschner B (2003) Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol Biochem 35:453–461

  61. Martínez-García LB, Korthals G, Brussaard L, Jørgensen HB, De Deyn GB (2018) Organic management and cover crop species steer soil microbial community structure and functionality along with soil organic matter properties. Agric Ecosyst Environ 263:7–17

  62. Matsi T, Lithourgidis AS, Gagianas AA (2003) Effects of injected liquid cattle manure on growth and yield of winter wheat and soil characteristics. Agron J 95:592–596

  63. McCormack S (2002) Analysis of agricultural materials: methods used at Johnstown Castle Research Centre. Teagasc, Johnstown Castle Environment Research Centre, Wexford, Ireland

  64. McGonigle T, Miller M, Evans D, Fairchild G, Swan J (1990) A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol 115:495–501

  65. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

  66. Myrold D (1999) Transformation of nitrogen. In: Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA (eds) Principles and applications of soil microbiology. Pearson Prentice Hall, Upper Saddle River, p 550

  67. Neher DA (1999) Nematode communities in organically and conventionally managed agricultural soils. J Nematol 31:142–154

  68. Neufeld KR, Grayston SJ, Bittman S, Krzic M, Hunt DE, Smukler SM (2017) Long-term alternative dairy manure management approaches enhance microbial biomass and activity in perennial forage grass. Biol Fertil Soils 53:613–626

  69. Noll M, Wellinger M (2008) Changes of the soil ecosystem along a receding glacier: testing the correlation between environmental factors and bacterial community structure. Soil Biol Biochem 40:2611–2619

  70. O’Mara F (2008) Country pasture/forage resource profile/Ireland. FAO of the UN, Rome

  71. Okada H, Oba H (2008) Comparison of nematode community similarities assessed by polymerase chain reaction-denaturing gradient gel electrophoresis (DGGE) and by morphological identification. Nematology 10:689–700

  72. Pascual J, Garcia C, Hernandez T, Moreno J, Ros M (2000) Soil microbial activity as a biomarker of degradation and remediation processes. Soil Biol Biochem 32:1877–1883

  73. Peech M, English L (1944) Rapid microchemical soil tests. Soil Sci 57:167–196

  74. Porazinska DL, Giblin-Davis RM, Faller L, Farmerie W, Kanzaki N, Morris K, Powers TO, Tucker AE, Sung W, Thomas WK (2009) Evaluating high-throughput sequencing as a method for metagenomic analysis of nematode diversity. Mol Ecol Resour 9:1439–1450

  75. Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490

  76. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

  77. Ragot SA, Kertesz MA, Bünemann EK (2015) Diversity of the phoD alkaline phosphatase gene in soil. Appl Environ Microbiol 81:7281–7289

  78. Sakurai M, Wasaki J, Tomizawa Y, Shinano T, Osaki M (2008) Analysis of bacterial communities on alkaline phosphatase genes in soil supplied with organic matter. Soil Sci Plant Nutr 54:62–71

  79. Schmalenberger A, Noll M (2014) Bacterial communities in grassland turfs respond to sulphonate addition while fungal communities remain largely unchanged. Eur J Soil Biol 61:12–19

  80. Schmalenberger A, Hodge S, Bryant A, Hawkesford MJ, Singh BK, Kertesz MA (2008) The role of Variovorax and other Comamonadaceae in sulfur transformations by microbial wheat rhizosphere communities exposed to different sulfur fertilization regimes. Environ Microbiol 10:1486–1500

  81. Shi Y, Ziadi N, Hamel C, Bittman S, Hunt D, Lalande R, Shang J (2018) Soil microbial biomass, activity, and community composition as affected by dairy manure slurry applications in grassland production. Appl Soil Ecol 125:97–107

  82. Siddiqi MR (1986) Tylenchida: parasites of plants and insects. Commonwealth Agricultural Bureaux

  83. Sieh D, Watanabe M, Devers EA, Brueckner F, Hoefgen R, Krajinski F (2013) The arbuscular mycorrhizal symbiosis influences sulfur starvation responses of Medicago truncatula. New Phytol 197:606–616

  84. Singh D, Slik JF, Jeon YS, Tomlinson KW, Yang X, Wang J, Kerfahi D, Porazinska DL, Adams JM (2019) Tropical forest conversion to rubber plantation affects soil micro- & mesofaunal community & diversity. Sci Rep 9:5893

  85. Smith SE, Smith FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104:1–13

  86. Steiner C, Teixeira WG, Lehmann J, Nehls T, De Macêdo JLV, Blum WE, Zech W (2007) Long term effects of manure, charcoal and mineral fertilization on crop production and fertility on a highly weathered Central Amazonian upland soil. Plant Soil 291:275–290

  87. Tabatabai M, Bremner J (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

  88. Tabatabai M, Bremner J (1970a) Arylsulfatase activity of soils. Soil Sci Soc Am J 34:225–229

  89. Tabatabai M, Bremner J (1970b) Factors affecting soil arylsulfatase activity. Soil Sci Soc Am J 34:427–429

  90. Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M (2014) Development of a prokaryotic universal primer for simultaneous analysis of Bacteria and Archaea using next-generation sequencing. PLoS One 9:e105592

  91. Taupe N (2016) Thermal treatment technologies for low moisture and dehydrated manure feedstock. Thesis (PhD), University of Limerick, URI:

  92. Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397

  93. Visioli G, Sanangelantoni AM, Vamerali T, Dal Cortivo C, Blandino M (2018) 16S rDNA profiling to reveal the influence of seed-applied biostimulants on the rhizosphere of young maize plants. Molecules 23:1–18

  94. Wei X, Hu Y, Razavi BS, Zhou J, Shen J, Nannipieri P, Wu J, Ge T (2019) Rare taxa of alkaline phosphomonoesterase-harboring microorganisms mediate soil phosphorus mineralization. Soil Biol Biochem 131:62–70

  95. Whitehead A, Hemming J (1965) A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Ann Appl Biol 55:25–38

  96. Williams PH, Haynes RJ (1993) Forms of sulphur in sheep excreta and their fate after application on to pasture soil. J Sci Food Agric 62:323–329

  97. Xue C, Penton CR, Zhu C, Chen H, Duan Y, Peng C, Guo S, Ling N, Shen Q (2018) Alterations in soil fungal community composition and network assemblage structure by different long-term fertilization regimes are correlated to the soil ionome. Biol Fertil Soils 54:95

  98. Zhang Y, Shen H, He X, Thomas BW, Lupwayi NZ, Hao X, Thomas MC, Shi X (2017) Fertilization shapes bacterial community structure by alteration of soil pH. Front Microbiol 8:1325

  99. Zhao J, Wang F, Li J, Zou B, Wang X, Li Z, Fu S (2014) Effects of experimental nitrogen and/or phosphorus additions on soil nematode communities in a secondary tropical forest. Soil Biol Biochem 75:1–10

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We are grateful to Con Traas for providing soil used in this study.


Funding for this project was provided by Science Foundation Ireland Grant (Grant Number SFI/13/IA/1923). Bastian Egeter and Cátia Chaves were supported via the European Union’s Horizon 2020 research and innovation program under Grant Agreement No. 668981.

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Ikoyi, I., Egeter, B., Chaves, C. et al. Responses of soil microbiota and nematodes to application of organic and inorganic fertilizers in grassland columns. Biol Fertil Soils (2020).

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  • Phosphorus
  • Sulfur
  • Nematodes
  • Slurry fertilization
  • Illumina sequencing
  • Lolium perenne