Biology and Fertility of Soils

, Volume 54, Issue 6, pp 743–759 | Cite as

Effects of cover crop in an apple orchard on microbial community composition, networks, and potential genes involved with degradation of crop residues in soil

  • Wei Zheng
  • Zhiyuan Zhao
  • Qingli Gong
  • Bingnian ZhaiEmail author
  • Ziyan LiEmail author
Original Paper


Changes in the soil microbial communities and networks were monitored after planting the cover crop for 9 years. The field experiment included plots with a cover crop and without a cover crop but with weed control, and two subplots with or without chemical fertilizer (192 kg N ha−1, 108 kg P2O5 ha−1, and 168 kg K2O ha−1 each year). After applying the cover crop and chemical fertilizer for 9 years, the composition and activity of bacterial and fungal communities changed significantly (p < 0.05), with the cover crop had greater effects than the chemical fertilizer on the composition of the soil microbial community. The relative abundances of 22 selected genera (in Firmicutes and Bacteroidetes) and two selected classes (Ascomycota) related to cover crop residue degradation increased significantly in the presence of the cover crop (p < 0.05). Network analysis showed that the cover crop decreased the number of positive links between bacterial and fungal taxa by 25.33%, and increased the negative links by 22.89%. The positive links among bacterial taxa increased by 16.63% with the cover crop, mainly among Proteobacteria (increase of 39), Firmicutes (16), Actinobacteria (five), and Bacteroidetes (10). The links among fungal taxa were less than among bacterial taxa and were not significantly affected by cover crop. Taxa such as Thaumarchaeota, unidentified_Nitrospiraceae, unidentified_Nitrosomonadaceae, Faecalibacterium, Coprococcus_3, and Ruminococcaceae_NK4A214_group dominated the network without the cover crop but they were not dominant with the cover crop. The relative abundances of potential genes involved with the degradation of cellulose, hemicellulose, and cello-oligosaccharides increased significantly with the cover crop. Therefore, the SOC and TN contents were enhanced by the cover crop with the increase of the soil enzyme activities. Thus, the apple yield was improved by the cover crop.


Grass cover Mulch Soil enzyme Soil microbial community Soil network Soil organic matter 


Funding information

This study was supported by the Special Fund for Agro-scientific Research in the Public Interest of China (201303104, 201103005-9), Agriculture Science Technology Achievement Transformation Fund of Shaanxi (NYKJ-2015-17), the Science and Technology Innovation Project of Shaanxi Province (2011KTZB02-02-05).

Supplementary material

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  1. Acosta-Martínez V, Dowd S, Sun Y, Allen V (2008) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem 40:2762–2770. CrossRefGoogle Scholar
  2. Acuña JJ, Durán P, Lagos LM, Ogram A, de la Luz Mora M, Jorquera MA (2016) Bacterial alkaline phosphomonoesterase in the rhizospheres of plants grown in Chilean extreme environments. Biol Fertil Soils 52:763–773. CrossRefGoogle Scholar
  3. Bag S, Ghosh TS, Das B (2017) Complete genome sequence of Faecalibacterium prausnitzii isolated from the gut of a healthy Indian adult. Genome Announc 5:e01286-17. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ballhausen MB, de Boer W (2016) The sapro-rhizosphere: carbon flow from saprotrophic fungi into fungus-feeding bacteria. Soil Biol Biochem 102:14–17. CrossRefGoogle Scholar
  5. Banerjee S, Baah-Acheamfour M, Carlyle CN, Bissett A, Richardson AE, Siddique T, Bork E, Chang S (2016a) Determinants of bacterial communities in Canadian agroforestry systems. Environ Microbiol 18:1805–1816. CrossRefPubMedGoogle Scholar
  6. Banerjee S, Kirkby CA, Schmutter D, Bissett A, Kirkegaard JA, Richardson AE (2016b) Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil. Soil Biol Biochem 97:188–198. CrossRefGoogle Scholar
  7. Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343–351. CrossRefPubMedGoogle Scholar
  8. Bastolla U, Fortuna MA, Pascual-Garcia A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:1018–1020. CrossRefPubMedGoogle Scholar
  9. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Berg B (1984) Decomposition of root litter and some factors regulating the process: long-term root litter decomposition in a scots pine forest. Soil Biol Biochem 16:609–617. CrossRefGoogle Scholar
  11. Biddoccu M, Ferraris S, Pitacco A, Cavallo E (2017) Temporal variability of soil management effects on soil hydrological properties runoff and erosion at the field scale in a hillslope vineyard North-West Italy. Soil Till Res 165:46–58. CrossRefGoogle Scholar
  12. Blackwood CB, Waldrop MP, Zak DR, Sinsabaugh RL (2007) Molecular analysis of fungal communities and laccase genes in decomposing litter reveals differences among forest types but no impact of nitrogen deposition. Environ Microbiol 9:1306–1316. CrossRefPubMedGoogle Scholar
  13. 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. CrossRefPubMedGoogle Scholar
  14. Bonanomi G, De Filippis F, Cesarano G, La Storia A, Ercolini D, Scala F (2016) Organic farming induces changes in soil microbiota that affect agro-ecosystem functions. Soil Biol Biochem 103:327–336. CrossRefGoogle Scholar
  15. Bone NJ, Thomson LJ, Ridland PM, Cole P, Hoffmann AA (2009) Cover crops in Victorian apple orchards: effects on production natural enemies and pests across a season. Crop Prot 28:675–683. CrossRefGoogle Scholar
  16. Bremner JM (1996) Nitrogen total In: Sparks DL (ed) Methods of soil analysis part 3: chemical methods. Soil Science Society of America Inc, Madison, pp 1085–1121Google Scholar
  17. Brennan EB, Acosta-Martinez V (2017) Cover cropping frequency is the main driver of soil microbial changes during six years of organic vegetable production. Soil Biol Biochem 109:188–204. CrossRefGoogle Scholar
  18. Burns KN, Kluepfel DA, Strauss SL, Bokulich NA, Cantu D, Steenwerth KL (2015) Vineyard soil bacterial diversity and composition revealed by 16S rRNA genes: differentiation by geographic features. Soil Biol Biochem 91:232–247. CrossRefGoogle Scholar
  19. Burns KN, Bokulich NA, Cantu D, Greenhut RF, Kluepfel DA, O'Geen AT, Strauss SL, Steenwerth KL (2016) Vineyard soil bacterial diversity and composition revealed by 16S rRNA genes: differentiation by vineyard management. Soil Biol Biochem 103:337–348. CrossRefGoogle Scholar
  20. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. P Natl Acad Sci USA 108:4516–4522. CrossRefGoogle Scholar
  22. Celette F, Gaudin R, Gary C (2008) Spatial and temporal changes to the water regime of a Mediterranean vineyard due to the adoption of cover cropping. Eur J Agron 29:153–162. CrossRefGoogle Scholar
  23. Chapela IH, Boddy L, Rayner ADM (1988) Structure and development of fungal communities in beech logs four and a half years after felling. FEMS Microbiol Lett 53:59–69. CrossRefGoogle Scholar
  24. Chen Y, Tao L, Wu K, Wang Y (2016) Shifts in indigenous microbial communities during the anaerobic degradation of pentachlorophenol in upland and paddy soils from southern China. Environ Sci Pollut Res 23:184–194. CrossRefGoogle Scholar
  25. Chen Y, Wen X, Sun Y, Zhang J, Wu W, Liao Y (2014) Mulching practices altered soil bacterial community structure and improved orchard productivity and apple quality after five growing seasons. Sci Hortic 172:248–257. CrossRefGoogle Scholar
  26. Csardi G, Nepusz T (2006) The igraph software package for complex network research. Inter J Complex Syst pp 1695Google Scholar
  27. Curlevski NJA, Xu ZH, Anderson IC, Cairney JWG (2010) Diversity of soil and rhizosphere fungi under Araucaria bidwillii (Bunya pine) at an Australian tropical montane rainforest site. Fungal Divers 40:12–22. CrossRefGoogle Scholar
  28. de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811. CrossRefPubMedGoogle Scholar
  29. Detheridge AP, Brand G, Fychan R, Crotty FV, Sanderson R, Griffith GW, Marley CL (2016) The legacy effect of cover crops on soil fungal populations in a cereal rotation. Agric Ecosyst Environ 228:49–61. CrossRefGoogle Scholar
  30. Dodd D, Moon YH, Swaminathan K, Mackie RI, Cann IK (2010) Transcriptomic analyses of xylan degradation by Prevotella bryantii and insights into energy acquisition by xylanolytic Bacteroidetes. J Biol Chem 285:30261–30273. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Du S, Bai G, Yu J (2014) Soil properties and apricot growth under intercropping and mulching with erect milk vetch in the loess hilly-gully region. Plant Soil 390:431–442. CrossRefGoogle Scholar
  32. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. CrossRefPubMedGoogle Scholar
  34. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. CrossRefPubMedGoogle Scholar
  35. Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillota S, Maronb PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96. CrossRefGoogle Scholar
  36. Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459:193–199. CrossRefPubMedGoogle Scholar
  37. Gilbert J, Steele J, Caporaso JG, Steinbruck L, Reeder J, Temperton B, Huse S, McHardy C, Knight R, Joint I, Somerfield P, Fuhrman J, Field D (2012) Defining seasonal marine microbial community dynamics. ISME J 6:298–308. CrossRefPubMedGoogle Scholar
  38. Guan X, Wang J, Zhao H, Wang J, Luo X, Liu F, Zhao F (2013) Soil bacterial communities shaped by geochemical factors and land use in a less-explored area Tibetan Plateau. BMC Genomics 14:820. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Gulis V, Suberkropp K (2003) Interactions between stream fungi and bacteria associated with decomposing leaf litter at different levels of nutrient availability. Aquat Microb Ecol 30:149–157. CrossRefGoogle Scholar
  40. Huang X, Liu L, Wen T, Zhang J, Wang F, Cai Z (2016) Changes in the soil microbial community after reductive soil disinfestation and cucumber seedling cultivation. Appl Microbiol Biotechnol 100:5581–5593. CrossRefPubMedGoogle Scholar
  41. Kennedy AC (1999) Bacterial diversity in agroecosystems. Agric Ecosyst Environ 74:65–76CrossRefGoogle Scholar
  42. Lagos LM, Navarrete OU, Maruyama F, Crowley DE, Cid FP, Mora ML, Jorquera MA (2014) Bacterial community structures in rhizosphere microsites of ryegrass (Lolium perenne var. Nui) as revealed by pyrosequencing. Biol Fertil Soils 50:1253–1266. CrossRefGoogle Scholar
  43. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Li JG, Wang CD, Tang ZH, Guo YQ, Zheng TC, Li YZ, You ZQ (2017) The gut bacterial community composition of wild cervus albirostris (white-lipped deer) detected by the 16S ribosomal RNA gene sequencing. Curr Microbiol 74:1100–1107. CrossRefPubMedGoogle Scholar
  45. Liu S, Meng J, Jiang L, Yang X, Lan Y, Cheng X, Chen W (2017) Rice husk biochar impacts soil phosphorous availability, phosphatase activities and bacterial community characteristics in three different soil types. Appl Soil Ecol 116:12–22. CrossRefGoogle Scholar
  46. Liu J, Zhang X, Wang H, Hui X, Wang Z, Qiu W (2018) Long-term nitrogen fertilization impacts soil fungal and bacterial community structures in a dryland soil of Loess Plateau in China. J Soils Sediments 18:1632–1640. CrossRefGoogle Scholar
  47. Lu L, Yin S, Liu X, Zhang W, Gu T, Shen Q, Qiu H (2013) Fungal networks in yield-invigorating and -debilitating soils induced by prolonged potato monoculture. Soil Biol Biochem 65:186–194. CrossRefGoogle Scholar
  48. Luo G, Ling N, Nannipieri P, Chen H, Raza W, Wang M, Guo S, Shen Q (2017) Long-term fertilisation regimes affect the composition of the alkaline phosphomonoesterase encoding microbial community of a vertisol and its derivative soil fractions. Biol Fertil Soils 53:375–388. CrossRefGoogle Scholar
  49. Lupatini M, Suleiman AKA, Jacques RJS, Antoniolli ZI, Kuramae EE, de Oliveira Camargo FA, Wurdig Roesch LF (2013) Soil-borne bacterial structure and diversity does not reflect community activity in pampa biome. PLoS One 8:e76465. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Ma A, Zhuang X, Wu J, Cui M, Lv D, Liu C, Zhuang G (2013) Ascomycota members dominate fungal communities during straw residue decomposition in arable soil. PLoS One 8:e66146. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Manevski K, Børgesen CD, Andersen MN, Kristensen IS (2014) Reduced nitrogen leaching by intercropping maize with red fescue on sandy soils in North Europe: a combined field and modeling study. Plant Soil 388:67–85. CrossRefGoogle Scholar
  53. Manici LM, Caputo F (2010) Soil fungal communities as indicators for replanting new peach orchards in intensively cultivated areas. Eur J Agron 33:188–196. CrossRefGoogle Scholar
  54. Martin González AM, Dalsgaard B, Olesen JM (2010) Centrality measures and the importance of generalist species in pollination networks. Ecol Complex 7:36–43. CrossRefGoogle Scholar
  55. Miao CP, Mi QL, Qiao XG, Zheng YK, Chen YW, Xu LH, Guan HL, Zhao LX (2016) Rhizospheric fungi of Panax notoginseng: diversity and antagonism to host phytopathogens. J Ginseng Res 40:127–134. CrossRefPubMedGoogle Scholar
  56. Mille-Lindblom C, Fischer H, Tranvik LJ (2006) Antagonism between bacteria and fungi: substrate competition and a possible tradeoff between fungal growth and tolerance towards bacteria. OIKOS 113:233–242. CrossRefGoogle Scholar
  57. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36CrossRefGoogle Scholar
  58. Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762. CrossRefGoogle Scholar
  59. Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19. CrossRefGoogle Scholar
  60. Nelson DW, Sommers LE (1982) Total carbon, organic carbon and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, 2nd edn. America Society of Agronomy, Madison, pp 535–579Google Scholar
  61. Nunes I, Jurburg S, Jacquiod S, Brejnrod A, Salles JF, Priemé A, Sørensen SJ (2018) Soil bacteria show different tolerance ranges to an unprecedented disturbance. Biol Fertil Soils 54:189–202. CrossRefGoogle Scholar
  62. Pathan SI, Ceccherini MT, Hansen MA, Giagnoni L, Ascher J, Aremella M, Sørensen SJ, Pietramellara G, Nannipieri P, Renella G (2015) Maize lines with differing nitrogen use efficiency select bacterial communities with different β-glucosidase encoding genes and glucosidase activity in the rhizosphere. Biol Fertil Soils 51:995–1004. CrossRefGoogle Scholar
  63. Pradel E, Poeri P (2000) Influence of a grass layer on vineyard soil temperature. Aust J Grape Wine Res 6:59–67CrossRefGoogle Scholar
  64. Qi R, Li J, Lin Z, Li Z, Li Y, Yang X, Zhang J, Zhao B (2016) Temperature effects on soil organic carbon soil labile organic carbon fractions and soil enzyme activities under long-term fertilization regimes. Appl Soil Ecol 102:36–45. CrossRefGoogle Scholar
  65. Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Chang Biol 18:1918–1927. CrossRefGoogle Scholar
  66. Ravachol J, de Philip P, Borne R, Mansuelle P, Mate MJ, Perret S, Fierobe HP (2016) Mechanisms involved in xyloglucan catabolism by the cellulosome-producing bacterium Ruminiclostridium cellulolyticum. Sci Rep 6:22770. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Reith F, Brugger J, Zammit CM, Gregg AL, Goldfarb KC, Andersen GL, Desantis TZ, Piceno YM, Brodie EL, Lu Z (2012) Influence of geogenic factors on microbial communities in metallogenic Australian soils. ISME J 6:2107–2118. CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sánchez EE, Giayetto A, Cichón L, Fernández D, Aruani MC, Curetti M (2007) Cover crops influence soil properties and tree performance in an organic apple (Malus domestica Borkh) orchard in northern Patagonia. Plant Soil 292:193–203. CrossRefGoogle Scholar
  69. Schöler A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fertil Soils 53:485–489. CrossRefGoogle Scholar
  70. Scow KM (1997) Ecology in agriculture. In: Jackson LE (ed) Ecology in Agriculture. Academic Press, San Diego, CA, pp 367–413CrossRefGoogle Scholar
  71. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. CrossRefPubMedPubMedCentralGoogle Scholar
  72. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569. CrossRefGoogle Scholar
  74. Tiwari R, Kumar K, Singh S, Nain L, Shukla P (2016) Molecular detection and environment-specific diversity of glycosyl hydrolase family 1 beta-glucosidase in different habitats. Front Microbiol 7:1597. CrossRefPubMedPubMedCentralGoogle Scholar
  75. Trivedi P, Anderson I, Singh B (2013) Microbial modulators of soil carbon storage: integrating genomic and metabolic knowledge for global prediction. Trends Microbiol 21:641–651. CrossRefPubMedGoogle Scholar
  76. van der Toorn JJTK, van Gylswyk NO (1985) Xylan-digesting bacteria from the rumen of sheep fed maize straw diets. J General Microbiol 131:2601–2607Google Scholar
  77. Verzeaux J, Alahmad A, Habbib H, Nivelle E, Roger D, Lacoux J, Decocq G, Hirel B, Catterou M, Spicher F, Dubois F, Duclercq J, Tetu T (2016) Cover crops prevent the deleterious effect of nitrogen fertilisation on bacterial diversity by maintaining the carbon content of ploughed soil. Geoderma 281:49–57. CrossRefGoogle Scholar
  78. Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart—how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484. CrossRefGoogle Scholar
  79. Vick-Majors TJ, Priscu JC, Amaral-Zettler L (2014) Modular community structure suggests metabolic plasticity during the transition to polar night in ice covered Antarctic lakes. ISME J 8:778–789. CrossRefPubMedGoogle Scholar
  80. Wagai R, Kitayama K, Satomura T, Fujinuma R, Balser T (2011) Interactive influences of climate and parent material on soil microbial community structure in bornean tropical forest ecosystems. Ecol Res 26:627–636. CrossRefGoogle Scholar
  81. Walsh BD, Salmins S, Buszard DJ, MacKenzie AF (1996) Impact of soil management systems on organic dwarf apple orchards and soil aggregate stability bulk density temperature and water content. Can J Soil Sci 76:203–209. CrossRefGoogle Scholar
  82. Wang G, Wang Y, Yang P, Luo H, Huang H, Shi P, Meng K, Yao B (2010) Molecular detection and diversity of xylanase genes in alpine tundra soil. Appl Microbiol Biotechnol 87:1383–1393. CrossRefPubMedGoogle Scholar
  83. Wang J, Bao J, Su J, Li X, Chen G, Ma X (2015) Impact of inorganic nitrogen additions on microbes in biological soil crusts. Soil Biol Biochem 88:303–313. CrossRefGoogle Scholar
  84. Wang Q, Liu YR, Zhang CJ, Zhang LM, Han LL, Shen JP, He JZ (2017) Responses of soil nitrous oxide production and abundances and composition of associated microbial communities to nitrogen and water amendment. Biol Fertil Soils 53:601–611. CrossRefGoogle Scholar
  85. Wegner CE, Liesack W (2016) Microbial community dynamics during the early stages of plant polymer breakdown in paddy soil. Environ Microbiol 18:2825–2842. CrossRefPubMedGoogle Scholar
  86. Williams MA, Jangid K, Shanmugam SG, Whitman WB (2013) Bacterial communities in soil mimic patterns of vegetative succession and ecosystem climax but are resilient to change between seasons. Soil Biol Biochem 57:749–757. CrossRefGoogle Scholar
  87. Yao S, Merwin IA, Bird GW, Abawi GS, Thies JE (2005) Orchard floor management practices that maintain vegetative or biomass groundcover stimulate soil microbial activity and alter soil microbial community composition. Plant Soil 271:377–389. CrossRefGoogle Scholar
  88. Zhalnina K, Dias R, de Quadros PD, Davis-Richardson A, Camargo FA, Clark IM, McGrath SP, Hirsch PR, Triplett EW (2015) Soil pH determines microbial diversity and composition in the park grass experiment. Microb Ecol 69:395–460. CrossRefPubMedGoogle Scholar
  89. Zhang HS, Qin FF, Qin P, Pan SM (2014) Evidence that arbuscular mycorrhizal and phosphate-solubilizing fungi alleviate NaCl stress in the halophyte Kosteletzkya virginica: nutrient uptake and ion distribution within root tissues. Mycorrhiza 24:383–395. CrossRefPubMedGoogle Scholar
  90. Zhang X, Zhang R, Gao J, Wang X, Fan F, Ma X, Yin H, Zhang C, Feng K, Deng Y (2017) Thirty-one years of rice-rice-green manure rotations shape the rhizosphere microbial community and enrich beneficial bacteria. Soil Biol Biochem 104:208–217. CrossRefGoogle Scholar
  91. Zhou J, Jiang X, Zhou B, Zhao B, Ma M, Guan D, Li J, Chen S, Cao F, Shen D, Qin J (2016) Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China. Soil Biol Biochem 95:135–143. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Resources and EnvironmentNorthwest A&F UniversityYanglingChina
  2. 2.Key Laboratory of Plant Nutrition and the Agri-environment in Northwest ChinaMinistry of AgricultureYanglingChina
  3. 3.Apple Experimental Station of Northwest A&F UniversityWeinanChina

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