Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Influence of Companion Planting on Microbial Compositions and Their Symbiotic Network in Pepper Continuous Cropping Soil

  • Jingxia Gao (Institute of Soil and Water Conservation, Northwest A&F University) ;
  • Fengbao Zhang (Institute of Soil and Water Conservation, Northwest A&F University)
  • Received : 2022.11.17
  • Accepted : 2023.03.22
  • Published : 2023.06.28
Download PDF
⟨ Previous Next ⟩

Abstract

Continuous cropping obstacles have become a serious factor restricting sustainable development in modern agriculture, while companion planting is one of the most common and effective methods for solving this problem. Here, we monitored the effects of companion planting on soil fertility and the microbial community distribution pattern in pepper monoculture and companion plantings. Soil microbial communities were analyzed using high-throughput sequencing technology. Companion plants included garlic (T1), oat (T2), cabbage (T3), celery (T4), and white clover (T5). The results showed that compared with the monoculture system, companion planting significantly increased the activities of soil urease (except for T5) and sucrase, but decreased catalase activity. In addition, T2 significantly improved microbial diversity (Shannon index) while T1 resulted in a decrease of bacterial OTUs and an increase of fungal OTUs. Companion planting also significantly changed soil microbial community structures and compositions. Correlation analysis showed that soil enzyme activities were closely correlated with bacterial and fungal community structures. Moreover, the companion system weakened the complexity of microbial networks. These findings indicated that companion plants can provide nutrition to microbes and weaken the competition among them, which offers a theoretical basis and data for further research into methods for reducing continuous cropping obstacles in agriculture.

Keywords

Acknowledgement

The authors are thankful to the Ningxia Vegetable High-Quality Development Technology Center support of key technology research and development (NGSB-2021-8-05).

References

  1. Gao JX, Pei HX, Xie H. 2020. Synergistic effects of organic fertilizer and corn straw on microorganisms of pepper continuous cropping soil in China. Bioengineered 11: 1258-1268. https://doi.org/10.1080/21655979.2020.1840753
  2. Zeng JR, Liu JZ, Lu CH, Ou XH, Luo KK, Li CM, et al. 2020. Intercropping with turmeric or ginger reduce the continuous cropping obstacles that affect Pogostemon cablin (Patchouli). Front. Microbiol. 11: 579719.
  3. Ding S, Zhou DP, Wei HW, Wu SH, Xie B. 2021. Alleviating soil degradation caused by watermelon continuous cropping obstacle: application of urban waste compost. Chemosphere 262: 128387.
  4. Chen LJ, Li DJ, Shao Y, Adni J, Wang H, Liu YQ, et al. 2020. Comparative analysis of soil microbiome profiles in the companion planting of white clover and orchard grass using 16S rRNA gene sequencing data. Front. Plant Sci. 11: 538311.
  5. Acosta-Martinez V, Cotton J. 2017. Lasting effects of soil health improvements with management changes in cotton-based cropping systems in a sandy soil. Biol. Fert. Soils 53: 533-546 https://doi.org/10.1007/s00374-017-1192-2
  6. Li S, Wu FZ. 2018. Diversity and co-occurrence patterns of soil bacterial and fungal communities in seven intercropping systems. Front. Microbiol. 9: 1521.
  7. Xu WH, Liu D, Wu FZ, Liu SW. 2015. Root exudates of wheat are involved in suppression of Fusarium wilt in watermelon in watermelon-wheat companion cropping. Eur. J. Plant Pathol. 141: 209-216. https://doi.org/10.1007/s10658-014-0528-0
  8. Li L, Zhang FS, Li XL, Christie P, Sun JH, Yang SC, et al. 2003. Interspecific facilitation of nutrient uptake by intercropped maize and faba bean. Nutr. Cycl. Agroecosys 65: 61-71. https://doi.org/10.1023/A:1021885032241
  9. Xiao XM, Cheng ZH, Meng HW, Liu LH, Li HZ, Dong YX. 2013. Intercropping of green garlic (Allium sativum L.) induces nutrient concentration changes in the soil and plants in continuously cropped cucumber (Cucumis sativus L.) in a plastic tunnel. PLoS One 8: e62173.
  10. Fu XP, Li CX, Zhou XG, Liu SW, Wu FZ. 2016. Physiological response and sulfur metabolism of the V. dahliae-infected tomato plants in tomato/potato onion companion cropping. Sci. Rep. 6: 36445.
  11. Gao DM, Zhou XG, Duan YD, Fu XP, Wu FZ. 2017. Wheat cover crop promoted cucumber seedling growth through regulating soil nutrient resources or soil microbial communities? Plant Soil 418: 459-475. https://doi.org/10.1007/s11104-017-3307-9
  12. Makoi JHJR, Chimphango SBM, Dakora FD. 2010. Elevated levels of acid and alkaline phosphatase activity in roots and rhizosphere of cowpea (Vigna unguiculata L. Walp.) genotypes grown in mixed culture and at different densities with sorghum (Sorghum bicolor L.). Crop Pasture Sci. 61: 279-286. https://doi.org/10.1071/CP09212
  13. Kirk JL, Beaudette LA, Hart M, Moutoglis P, Khironomos JN, Lee H, et al. 2004. Methods of studying soil microbial diversity. J. Microbiol. Meth. 58: 169-188. https://doi.org/10.1016/j.mimet.2004.04.006
  14. Dai CC, Chen Y, Wang XX, Li PD. 2013. Effects of intercropping of peanut with the medicinal plant Atractylodes lancea on soil microecology and peanut yield in subtropical China. Agroforest. Syst. 87: 417-426. https://doi.org/10.1007/s10457-012-9563-z
  15. Zhou WJ, Zhang YZ, Wang KR, Li HS, Hao YJ, Liu X. 2009. Plant phosphorus uptake in a soybean-citrus intercropping system in the red soil hilly region of South China. Pedosphere 19: 244-250. https://doi.org/10.1016/S1002-0160(09)60114-4
  16. Finney DM, Kaye JP. 2017. Functional diversity in cover crop polycultures increases multifunctionality of an agricultural system. J. Appl. Ecol. 54: 509-517. https://doi.org/10.1111/1365-2664.12765
  17. Xiao XM, Cheng ZH, Meng HW, Khan MA, Li HZ. 2012. Intercropping with garlic alleviated continuous cropping obstacle of cucumber in plastic tunnel. Acta. Agr. Scand B-S. P. 62: 696-705. https://doi.org/10.1080/09064710.2012.697571
  18. 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: e00555.
  19. van Elsas JD, Chiurazzi M, Mallon CA, Elhottova D, Kristufek V, Salles JF. 2012. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc. Natl. Acad. Sci. USA 109: 1159-1164. https://doi.org/10.1073/pnas.1109326109
  20. Garbeva P, Postma J, van Veen JA, van Elsas JD. 2006. Effect of above-ground plant species on soil microbial community structure and its impact on suppression of Rhizoctonia solani AG3. Environ. Microbiol. 8: 233-246. https://doi.org/10.1111/j.1462-2920.2005.00888.x
  21. Jin X, Zhang JH, Shi YJ, Wu FZ, Zhou XG. 2019. Green manures of Indian mustard and wild rocket enhance cucumber resistance to Fusarium wilt through modulating rhizosphere bacterial community composition. Plant Soil 441: 283-300. https://doi.org/10.1007/s11104-019-04118-6
  22. Ren LX, Su SM, Yang XM, Xu YC, Huang QW, Shen QR. 2008. Intercropping with aerobic rice suppressed Fusarium wilt in watermelon. Soil Biol. Biochem. 40: 834-844. https://doi.org/10.1016/j.soilbio.2007.11.003
  23. Zhou XG, Yu GB, Wu FZ. 2011. Effects of intercropping cucumber with onion or garlic on soil enzyme activities, microbial communities and cucumber yield. Eur. J. Soil Biol. 47: 279-287. https://doi.org/10.1016/j.ejsobi.2011.07.001
  24. Dennis PG, Miller AJ, Hirsch PR. 2010. Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol. Ecol. 72: 313-327. https://doi.org/10.1111/j.1574-6941.2010.00860.x
  25. Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, et al. 2013. Soil enzymes in a changing environment: Current knowledge and future directions. Soil Biol. Biochem. 58: 216-234. https://doi.org/10.1016/j.soilbio.2012.11.009
  26. He Y, Ding N, Shi JC, Wu M, Liao H, Xu JM. 2013. Profiling of microbial PLFAs: Implications for interspecific interactions due to intercropping which increase phosphorus uptake in phosphorus limited acidic soils. Soil Biol. Biochem. 57: 625-634. https://doi.org/10.1016/j.soilbio.2012.07.027
  27. Song YN, Zhang FS, Marschner P, Fan FL, Gao HM, Bao XG, et al. 2007. Effect of intercropping on crop yield and chemical and microbiological properties in rhizosphere of wheat (Triticum aestivum L.), maize (Zea mays L.), and faba bean (Vicia faba L.). Biol. Fert. Soils 43: 565-574. https://doi.org/10.1007/s00374-006-0139-9
  28. Li Y, Feng H, Chen J, Lu J, Wu W, Liu X, et al. 2022. Biochar incorporation increases winter wheat (Triticum aestivum L.) production with significantly improving soil enzyme activities at jointing stage. Catena 211: 105979.
  29. Guo MJ, Wu FH, Hao GG, Qi Q, Li R, Li N, et al. 2017. Bacillus subtilis improves immunity and disease resistance in rabbits. Front. Immunol. 8: 354.
  30. Magoc T, Salzberg SL. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27: 2957-2963. https://doi.org/10.1093/bioinformatics/btr507
  31. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7: 335-336. https://doi.org/10.1038/nmeth.f.303
  32. Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998. https://doi.org/10.1038/nmeth.2604
  33. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig WG, Peplies J, et al. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35: 7188-7196. https://doi.org/10.1093/nar/gkm864
  34. Nilsson RH, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, et al. 2019. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 47: D259-D264. https://doi.org/10.1093/nar/gky1022
  35. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biol. 12: R60.
  36. Du PQ, He HR, Wu XH, Xu J, Dong FS, Liu XG, et al. 2021. Mesosulfuron-methyl influenced biodegradability potential and N transformation of soil. J. Hazard. Mater. 416: 125770.
  37. Zhang HP, Song JJ, Zhang ZH, Zhang QK, Chen SY, Mei JJ, et al. 2021. Exposure to fungicide difenoconazole reduces the soil bacterial community diversity and the co-occurrence network complexity. J. Hazard. Mater. 405: 124208.
  38. Wu CC, Wang ZN, Ma Y, Luo JY, Gao XK, Ning J, et al. 2021. Influence of the neonicotinoid insecticide thiamethoxam on soil bacterial community composition and metabolic function. J. Hazard. Mater. 405: 124275.
  39. Blaise D, Velmourougane K, Santosh S, Manikandan A. 2021. Intercrop mulch affects soil biology and microbial diversity in rainfed transgenic Bt cotton hybrids. Sci. Total Environ. 794: 148787.
  40. Yang CD, Lu SG. 2022. Straw and straw biochar differently affect phosphorus availability, enzyme activity and microbial functional genes in an Ultisol. Sci. Total Environ. 805: 150325.
  41. Hiradate S, Morita S, Furubayashi A, Fujii Y, Harada J. 2005. Plant growth inhibition by cis-cinnamoyl glucosides and cis-cinnamic acid. J. Chem. Ecol. 31: 591-601. https://doi.org/10.1007/s10886-005-2047-0
  42. Curtright AJ, Tiemann LK. 2021. Intercropping increases soil extracellular enzyme activity: a meta-analysis. Agr. Ecosyst. Environ. 319: 107284.
  43. Wang B, Shen H, Yang X, Guo T, Zhang B, Yan W. 2013. Effects of chitinase-transgenic (McChit1) tobacco on the rhizospheric microflora and enzyme activities of the purple soil. Plant Soil Environ. 59: 241-246. https://doi.org/10.17221/704/2012-PSE
  44. Sun SY, Sun H, Zhang DS, Zhang JF, Cai ZY, Qin GH, et al. 2019. Response of soil microbes to vegetation restoration in coal mining subsidence areas at Huaibei Coal Mine, China. Int. J. Environ. Res. Public Health 16: 1757.
  45. German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD. 2011. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol. Biochem. 43: 1387-1397. https://doi.org/10.1016/j.soilbio.2011.03.017
  46. Li YF, Wang YQ, Zhang WQ. 2021. Impact of simulated acid rain on the composition of soil microbial communities and soil respiration in typical subtropical forests in Southwest China. Ecotox. Environ. Safe 215: 112152.
  47. Yin YA, Yang C, Tang JR, Gu J, Li HC, Duan ML, et al. 2021. Bamboo charcoal enhances cellulase and urease activities during chicken manure composting: Roles of the bacterial community and metabolic functions. J. Environ. Sci. 108: 84-95. https://doi.org/10.1016/j.jes.2021.02.007
  48. Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, et al. 2016. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7: 10541.
  49. Wagg C, Bender SF, Widmer F, van der Heijden MGA. 2014. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc. Natl. Acad. Sci. USA 111: 5266-5270. https://doi.org/10.1073/pnas.1320054111
  50. King AE, Hofmockel KS. 2017. Diversified cropping systems support greater microbial cycling and retention of carbon and nitrogen. Agr. Ecosyst. Environ. 240: 66-76 https://doi.org/10.1016/j.agee.2017.01.040
  51. Lian TX, Mu YH, Jin J, Ma QB, Cheng YB, Cai ZD, Nian H. 2019. Impact of intercropping on the coupling between soil microbial community structure, activity, and nutrient-use efficiencies. PeeJ. 7: e6412.
  52. Li NH, Gao DM, Zhou XG, Chen SC, Li CX, Wu FZ. 2020. Intercropping with potato-onion enhanced the soil microbial diversity of tomato. Microorganisms 8: 834
  53. Park JH, Han HJ. 2019. Effect of tungsten-resistant bacteria on uptake of tungsten by lettuce and tungsten speciation in plants. J. Hazard. Mater. 379: 120825.
  54. Samad A, Trognitz F, Compant S, Antonielli L, Sessitsch A. 2017. Shared and host-specific microbiome diversity and functioning of grapevine and accompanying weed plants. Environ. Microbiol. 19: 1407-1424. https://doi.org/10.1111/1462-2920.13618
  55. Zheng W, Gong QL, Zhao ZY, Liu J, Zhai BN, Wang ZH, et al. 2018. Changes in the soil bacterial community structure and enzyme activities after intercrop mulch with cover crop for eight years in an orchard. Eur. J. Soil Biol. 86: 34-41. https://doi.org/10.1016/j.ejsobi.2018.01.009
  56. Deng JJ, Bai XJ, Zhou YB, Zhu WX, Yin Y. 2020. Variations of soil microbial communities accompanied by different vegetation restoration in an open-cut iron mining area. Sci. Total Environ. 704: 135243.
  57. Wu T, Qin Y, Li M. 2021. Intercropping of tea (Camellia sinensis L.) and chinese chestnut: variation in the structure of rhizosphere bacterial communities. J. Soil Sci. Plant Nut. 21: 2178-2190. https://doi.org/10.1007/s42729-021-00513-0
  58. Bian FY, Zhong ZK, Li CZ, Zhang XP, Gu LJ, Huang ZC, et al. 2021. Intercropping improves heavy metal phytoremediation efficiency through changing properties of rhizosphere soil in bamboo plantation. J. Hazard. Mater. 416: 125898.
  59. Jiang B, Adebayo A, Jia JL, Xing Y, Deng SQ, Guo LM, et al. 2019. Impacts of heavy metals and soil properties at a Nigerian e-waste site on soil microbial community. J. Hazard. Mater. 362: 187-195. https://doi.org/10.1016/j.jhazmat.2018.08.060
  60. Perez-Izquierdo L, Zabal-Aguirre M, Gonzalez-Martinez SC, Buee M, Verdu M, Rincon A, et al. 2019. Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome. J. Ecol. 107: 1594-1605 https://doi.org/10.1111/1365-2745.13202
  61. Devos DP. 2021. Reconciling asgardarchaeota phylogenetic proximity to Eukaryotes and Planctomycetes cellular features in the evolution of life. Mol. Biol. Evol. 38: 3531-3542. https://doi.org/10.1093/molbev/msab186
  62. Boedeker C, Schuler M, Reintjes G, Jeske O, van Teeseling MCF, Jogler M, et al. 2017. Determining the bacterial cell biology of Planctomycetes. Nat. Commun. 8: 14853.
  63. Lin YB, Ye YM, Hu YM, Shi HK. 2019. The variation in microbial community structure under different heavy metal contamination levels in paddy soils. Ecotox. Environ. Safe 180: 557-564. https://doi.org/10.1016/j.ecoenv.2019.05.057
  64. Al-Sadi AM, Al-Khatri B, Nasehi A, Al-Shihi M, Al-Mahmooli IH, Maharachchikumbura SSN. 2017. High fungal diversity and dominance by Ascomycota in dam reservoir soils of arid climates. Int. J. Agric. Biol. 19: 682-688. https://doi.org/10.17957/IJAB/15.0328
  65. Saldanha AV, Gontijo LM, Carvalho RMR, Vasconcelos CJ, Correa AS, Gandra RLR. 2019. Companion planting enhances pest suppression despite reducing parasitoid emergence. Basic Appl. Ecol. 41: 45-55. https://doi.org/10.1016/j.baae.2019.10.002
  66. Zheng W, Zhao ZY, Gong QL, Zhai BN, Li ZY. 2018. Responses of fungal-bacterial community and network to organic inputs vary among different spatial habitats in soil. Soil Biol. Biochem. 125: 54-63. https://doi.org/10.1016/j.soilbio.2018.06.029
  67. Pivato B, Semblat A, Guegan T, Jacquiod S, Martin J, Deau F, et al. 2021. Rhizosphere bacterial networks, but not diversity, are impacted by pea-wheat intercropping. Front. Microbiol. 12: 674556.
  68. Chen XD, Jiang N, Condron LM, Dunfield KE, Chen ZH, Wang JK, et al. 2019. Impact of long-term phosphorus fertilizer inputs on bacterial phoD gene community in a maize field, Northeast China. Sci. Total Environ. 669: 1011-1018. https://doi.org/10.1016/j.scitotenv.2019.03.172
  69. Liu JS, Ma Q, Hui XL, Ran JY, Ma QX, Wang XS, et al. 2020. Long-term high-P fertilizer input decreased the total bacterial diversity but not phoD-harboring bacteria in wheat rhizosphere soil with available-P deficiency. Soil Biol. Biochem. 149: 107918.