Nitrogen application and intercropping change microbial community diversity and physicochemical characteristics in mulberry and alfalfa rhizosphere soil

Abstract

Intercropping of mulberry (Morus alba L.) and alfalfa (Medicago sativa L.) is a new forestry-grass compound model in China, which can provide high forage yields with high protein. Nitrogen application is one of the important factors determining the production and quality of this system. To elucidate the advantages of intercropping and nitrogen application, we analyzed the changes of physicochemical properties, enzyme activities, and microbial communities in the rhizosphere soil. We used principal components analysis (PCA) and redundancy discriminators analysis to clarify the relationships among treatments and between treatments and environmental factors, respectively. The results showed that nitrogen application significantly increased pH value, available nitrogen content, soil water content (SWC), and urea (URE) activity in rhizosphere soil of monoculture mulberry. In contrast, intercropping and intercropping + N significantly decreased pH and SWC in mulberry treatments. Nitrogen, intercropping and intercropping + N sharply reduced soil organic matter content and SWC in alfalfa treatments. Nitrogen, intercropping, and intercropping + N increased the values of McIntosh diversity (U), Simpson diversity (D), and Shannon–Weaver diversity (H′) in mulberry treatments. However, PCA scatter plots showed clustering of monoculture mulberry with nitrogen (MNE) and intercropping mulberry without nitrogen (M0). Intercropping reduced both H′ and D but nitrogen application showed no effect on diversity of microbial communities in alfalfa. There were obvious differences in using the six types of carbon sources between mulberry and alfalfa treatments. Nitrogen and intercropping increased the numbers of sole carbon substrate in mulberry treatments where the relative use rate exceeded 4%. While the numbers declined in alfalfa with nitrogen and intercropping. RDA indicated that URE was positive when intercropping mulberry was treated with nitrogen, but was negative in monoculture alfalfa treated with nitrogen. Soil pH and SWC were positive with mulberry treatments but were negative with alfalfa treatments. Intercropping with alfalfa benefited mulberry in the absence of nitrogen application. Intercropping with alfalfa and nitrogen application could improve the microbial community function and diversity in rhizosphere soil of mulberry. The microbial community in rhizosphere soil of mulberry and alfalfa is strategically complementary in terms of using carbon sources.

This is a preview of subscription content, access via your institution.

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

References

  1. Amador JA, Gorres JH (2007) Microbiological characterization of the structures built by earthworms and ants in an agricultural field. Soil Biol Biochem 39(8):2070–2077

    CAS  Article  Google Scholar 

  2. Ashworth AJ, West CP, Allen FL, Keyser PD, Weiss SA, Tyler DD, Taylor AM, Warwick KL, Beamer KP (2015) Biologically fixed nitrogen in legume intercropped systems: comparison of nitrogen-difference and nitrogen-15 enrichment techniques. Agron J 107(6):2419–2430

    CAS  Article  Google Scholar 

  3. Bandick AK, Dick RP (1999) Field management effects on soil enzyme activities. Soil Biol Biochem 31(11):1471–1479

    CAS  Article  Google Scholar 

  4. Baslam M, Antolín M, Gogorcena Y, Muñoz F, Goicoechea N (2014) Changes in alfalfa forage quality and stem carbohydrates induced by arbuscular mycorrhizal fungi and elevated atmospheric CO2. Annal Appl Biol 164(2):190–199

    CAS  Article  Google Scholar 

  5. Chalk P (1998) Dynamics of biologically fixed N in legume-cereal rotations: a review. Aust J Agric Res 49(3):303–316

    CAS  Article  Google Scholar 

  6. Chu H, Grogan P (2010) Soil microbial biomass, nutrient availability and nitrogen mineralization potential among vegetation-types in a low arctic tundra landscape. Plant Soil 329(1):411–420

    CAS  Article  Google Scholar 

  7. Classen AT, Boyle SI, Haskins KE, Overby S, Hart SC (2003) Community-level physiological profiles of bacteria and fungi: plate type and incubation temperature influences on contrasting soils. FEMS Microbiol Ecol 44(3):319–328

    CAS  PubMed  Article  Google Scholar 

  8. Condron LM, Stark C, O’Callaghan M, Clinton P, Huang Z (2010) The role of microbial communities in the formation and decomposition of soil organic matter. In: Dixon GR, Tilston EL (eds) Soil microbiology and sustainable crop production. Springer, Netherlands, pp 81–118

    Google Scholar 

  9. Davis JHC, Woolley JN (1993) Genotypic requirement for intercropping. Field Crops Res 34:407–430

    Article  Google Scholar 

  10. Delgadoâ Baquerizo M, Brajesh KS, Jasmine G, Peter BR (2016) Relative importance of soil properties and microbial community for soil functionality: insights from a microbial swap experiment. Funct Ecol 30(11):1862–1873

    Article  Google Scholar 

  11. Deveryshetty J, Suvekbala V, Varadamshetty G, Phale P (2007) Metabolism of 2-, 3- and 4-hydroxybenzoates by soil isolates Alcaligenes sp. strain PPH and Pseudomonas sp. strain PPD. FEMS Microbiol Lett 268:59–66

    CAS  PubMed  Article  Google Scholar 

  12. Fog K (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63(3):433–462

    Article  Google Scholar 

  13. Garau G, Silvetti M, Deiana S, Deiana P, Castaldi P (2011) Long-term influence of red mud on As mobility and soil physico-chemical and microbial parameters in a polluted sub-acidic soil. J Hazard Mater 185(2–3):1241–1248

    CAS  PubMed  Article  Google Scholar 

  14. Garland, (1997) Analysis and interpretation of community-level physiological profiles in microbial ecology. FEMS Microbiol Ecol 24(4):289–300

    CAS  Article  Google Scholar 

  15. Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57(8):2351–2359

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. Giller KE, Witter E, Mcgrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a Review. Soil Biol Biochem 30(10–11):1389–1414

    CAS  Article  Google Scholar 

  17. Hauggaard-Nielsen H, Jensen ES (2001) Evaluating pea and barley cultivars for complementarity in intercropping at different levels of soil N availability. Field Crops Res 72(3):185–196

    Article  Google Scholar 

  18. Hector S (1999) Plant diversity and productivity in European grasslands. Science 286(5442):1123–1127

    CAS  PubMed  Article  Google Scholar 

  19. Heichel G, Vance CP (1979) Nitrate-N and rhizobium srain roles in alfalfa seedling nodulation and growth1. Crop Sci 19(4):512–518

    CAS  Article  Google Scholar 

  20. Huang N, Wang WX, Yao Y, Zhu F, Wang WX, Chang X (2017) The influence of different concentrations of bio-organic fertilizer on cucumber Fusarium wilt and soil microflora alterations. PLoS ONE 12:e0171490

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  21. Janzen H (1987) Soil organic matter characteristics after long-term cropping to various spring wheat rotations. Can J Soil Sci 67(4):845–856

    Article  Google Scholar 

  22. Jenkinson D (1968) Chemical tests for potentially available nitrogen in soil. J Sci Food Agric 19(3):160–168

    CAS  PubMed  Article  Google Scholar 

  23. Kitahara N, Shibata S, Nishida T (2002) Management and utilisation of mulberry for forage in Japan 1. Productivity of mulberry-pasture association system and nutritive value of mulberry. Phys Chem Chem Phys 15(23):9335–42

    Google Scholar 

  24. Ladygina N, Hedlund K (2010) Plant species influence microbial diversity and carbon allocation in the rhizosphere. Soil Biol Biochem 42(2):162–168

    CAS  Article  Google Scholar 

  25. Latati M, Blavet D, Alkama N, Laoufi H, Drevon JJ, Gérard F, Pansu M, Ounane SM (2014) The intercropping cowpea-maize improves soil phosphorus availability and maize yields in an alkaline soil. Plant Soil 385(1):181–191

    CAS  Article  Google Scholar 

  26. Li Z, Wu X, Chen B (2007) Changes in transformation of soil organic C and functional diversity of soil microbial community under different land uses. Agric Sci China 6(10):1235–1245

    CAS  Article  Google Scholar 

  27. Liu Y, Delgado-Baquerizo M, Wang J, Hu H, Yang ZH, He J (2018) New insights into the role of microbial community composition in driving soil respiration rates. Soil Biol Biochem 118:35–41

    CAS  Article  Google Scholar 

  28. Machii KA, Yamanouchi H (2001) A list of morphological and agronomical traits of mulberry genetic resources. Miscellaneous Publ Natl Inst Seric Entomol Sci 18(6):433–442

    Google Scholar 

  29. Mao L, Zhang L, Li W, Van der Werf W, Sun J, Spiertz H, Li L (2012) Yield advantage and water saving in maize/pea intercrop. Field Crops Res 138:11–20

    Article  Google Scholar 

  30. Motavalli P, Palm C, Parton W, Elliott E, Frey S (1995) Soil pH and organic C dynamics in tropical forest soils: evidence from laboratory and simulation studies. Biol Biochem 27(12):1589–1599

    CAS  Article  Google Scholar 

  31. Narita Y (1983) Soil microorganisms in continuous and rotated cropping in gleyic ordinary andosols in abashiri district : (iii) fungi on roots of several crops in continuous and rotated. Japanese J Soil Sci Plant Nutr 54(1):15–24

    Google Scholar 

  32. Rodríguez-Kábana R, Truelove B (1982) Effects of crop rotation and fertilization on catalase activity in a soil of the southeastern United States. Plant Soil 69(1):97–104

    Article  Google Scholar 

  33. Saiya-Cork KR, Sinsabaugh R, Zak D (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34(9):1309–1315

    CAS  Article  Google Scholar 

  34. Sánchez M (2000) Mulberry: an exceptional forage available almost worldwide. World Animal Rev 93(1):1–21

    Google Scholar 

  35. Sánchez MD (2002) Mulberry for animal production: mulberry, an exceptional forage available almost worldwide. Roma: Food and Agriculture Organization (FAO) of United Nations, pp 271–285

  36. Simpson EH (1949) The measurement of diversity. Nature 163(4148):688–688

    Article  Google Scholar 

  37. Stefanowicz A (2006) The biolog plates technique as a tool in ecological studies of microbial communities. Polish J Environ Stud 15(5):669–676

    CAS  Google Scholar 

  38. Strong WL (2016) Biased richness and evenness relationships within Shannon-Wiener index values. Ecol Ind 67:703–713

    Article  Google Scholar 

  39. Su C, Evans L (1996) Soil solution chemistry and alfalfa response to CaCO3 and MgCO3 on an acidic Gleysol. Can J Soil Sci 76(1):41–47

    CAS  Article  Google Scholar 

  40. Sun YH, Yang ZH, Zhao JJ, Li Q (2012) Functional diversity of microbial communities in sludge-amended soils. Physics Procedia 33(1):726–731

    Article  Google Scholar 

  41. Tang X, Bernard L, Brauman A, Daufresne T, Deleporte P, Desclaux D, Souche G, Placella S, Hinsinger P (2014) Increase in microbial biomass and phosphorus availability in the rhizosphere of intercropped cereal and legumes under field conditions. Soil Biol Biochem 75:86–93

    CAS  Article  Google Scholar 

  42. Teuber LR, Levin RP, Sweeney TC, Phillips DA (1984) Selection for N concentration and forage yield in alfalfa. Crop Sci 24(3):553–558

    Article  Google Scholar 

  43. Tomm GO, Walley FL, Kessel CV, Slinkard AE (1995) Nitrogen cycling in an alfalfa and bromegrass sward via litterfall and harvest losses. Agron J 87(6):1078–1085

    Article  Google Scholar 

  44. Trasar-Cepeda C, Camiña F, Leirós MC, Gil-Sotres F (1999) An improved method to measure catalase activity in soils. Soil Biol Biochem 31(3):483–485

    CAS  Article  Google Scholar 

  45. Van Der Heijden MGA, Bakker R, Verwaal J, Scheublin TR, Rutten M, Van Logtestijn R, Staehelin C (2006) Symbiotic bacteria as a determinant of plant community structure and plant productivity in dune grassland. FEMS Microbiol Ecol 56(2):178–187

    PubMed  Article  CAS  Google Scholar 

  46. Wang WX, Yang HJ, Bo YK, Ding S, Cao BH (2012) Nutrient composition, polyphenolic contents, and in situ protein degradation kinetics of leaves from three mulberry species. Livestock Sci 146(2–3):203–206

    Article  Google Scholar 

  47. Wei J, Gao J, Wang N, Liu Y, Wang Y, Bai Z, Zhuang X, Zhuang G (2019) Differences in soil microbial response to anthropogenic disturbances in Sanjiang and Momoge Wetlands. China FEMS Microbiol Ecol 95(8):1–14

    Google Scholar 

  48. Willey RW (1979) Intercropping: its importance and research needs.part 2, agronomy and research approaches. Field Crop Abstracts 32:73–85

    Google Scholar 

  49. Wu F, Wang X (2007) Effect of monocropping and rotation on soil microbial community diversity and cucumber yield and quality under protected cultivation. Acta Hort 76:555–561

    Article  Google Scholar 

  50. Xu HJ, Li S, Su JQ, Sa N, Gibson V, Li H, Zhu YG (2014) Does urbanization shape bacterial community composition in urban park soils? A case study in 16 representative Chinese cities based on the pyrosequencing method. FEMS Microbiol Ecol 87(1):182–192

    CAS  PubMed  Article  Google Scholar 

  51. Yao H, Jiao X, Wu F (2006) Effects of continuous cucumber cropping and alternative rotations under protected cultivation on soil microbial community diversity. Plant Soil 284(1):195–203

    CAS  Article  Google Scholar 

  52. Zhang MM, AO H, Li X, Zhang JY, Wang N, Ju CM, Wang J, Cai DJ, Sun GY(2015) Effects of intercropping between mulberry and alfalfa on soil enzyme activities and microbial community diversity in rhizophere. Acta Agrestia Sinica 23(2):84–91 (Abstract in English)

  53. Zhang MM, Wang N, Hu YB, Sun GY (2018) Changes in soil physicochemical properties and soil bacterial community in mulberry (Morus alba L.)/alfalfa (Medicago sativa L.) intercropping system. Microbiologyopen 7(2):e555

    Article  CAS  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Fanjuan Meng or Guangyu Sun.

Additional information

Publisher's Note

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

Project funding: This work was financially supported by the Heilongjiang Province Science Foundation for Youths (Grant No. QC2016018), the National Natural Science Foundation of China (Grant No. 31600508), the Fundamental Research Funds for the Central University (2572017CA21), the Application Technology Research and Development Projects of Heilongjiang Province (Grant No. WB13B104), and the Science and Technology Project of Heilongjiang Farms & Land Reclamation Administration (Grant No. HNK135-01-056).

The online version is available at http://www.springerlink.com.

Corresponding editor: Yanbo Hu.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhang, X., Teng, Z., Zhang, H. et al. Nitrogen application and intercropping change microbial community diversity and physicochemical characteristics in mulberry and alfalfa rhizosphere soil. J. For. Res. (2021). https://doi.org/10.1007/s11676-020-01271-y

Download citation

Keywords

  • Mulberry intercropped with alfalfa
  • Nitrogen application
  • Principal components analysis
  • Redundancy discriminators analysis
  • Rhizosphere soil