Sugars altered fungal community composition and caused high network complexity in a Fusarium wilt pathogen-infested soil

  • Gaidi Ren
  • Tianzhu Meng
  • Yan MaEmail author
Original Paper


Despite the quantitative dominance of sugars within root exudates and their ecological importance in regulating plant disease development, it is not well understood how specific sugars influence the fate of fungal pathogens, the fungal community composition and, in particular, the fungal interactions in soil. In this study, a microcosm incubation experiment was conducted by adding four low-molecular-weight sugars to a Fusarium wilt pathogen-infested natural soil (i.e., Low-FO soil) and the soil further receiving Fusarium wilt pathogen inocula (i.e., High-FO soil) to understand the changes in fungal community composition and fungal interactions. Despite living in soils where multiple microbes coexist, after the addition of sugar, Fusarium wilt pathogen was selectively enriched, and sugar allowed it to sustain its dominance over time. Concurrently, the fungal richness became lower, and the fungal community composition was altered throughout 42 days of incubation. The Humicola-affiliated OTU600 showed a more rapid biomass increase than this pathogen after the addition of sugars in the Low-FO soil at some time points, and also increased over time in the High-FO soil. The community network in sugar-added soils was more complex and connected than in those without added sugar, indicating greater fungal interactions and niche-sharing. The Fusarium wilt pathogen formed positive or no connections with the keystone taxa in sugar-spiked networks in almost all cases. This suggests that the keystone taxa may have promoted or not constrained the wilt pathogen, representing a potential mechanism enabling this pathogen to vigorously proliferate after the addition of sugar.


Root exudate Sugar Fusarium wilt pathogen Fungal community Microbial network Keystone species 



We thank Prof. Xiangzhen Li and Dr. Jiabao Li from Chengdu Institute of Biology, Chinese Academy of Sciences, Dr. Ruibo Sun from Institute of Genetic and Development Biology, Chinese Academy of Sciences, and Yuntao Li, Kaoping Zhang, Kunkun Fan, Zhiying Guo, Teng Yang, and Dr. Xiaomi Wang from Institute of Soil Science, Chinese Academy of Sciences for their help in the statistical analysis. We thank Prof. Zhongjun Jia from Institute of Soil Science, Chinese Academy of Sciences for his suggestions on experimental design. We thank Dr. Qiujun Wang from Institute of Agricultural Sciences and Environments, Jiangsu Academy of Agricultural Sciences for his help in sample collection.

Funding information

This work was supported by the National Science Foundation for Young Scientists of China (No. 41601266), Special Fund of China Postdoctoral Science Foundation (No. 2017 T100340), China Postdoctoral Science Foundation (No. 2016 M600387), Jiangsu Postdoctoral Science Foundation, China (No.1601061B), National Science Foundation for Young Scientists of China (No. 41701304), Ministry of Science and Technology 973 project (No. 2015CB150500), Agricultural Science and Technology Innovation Fund of Jiangsu Province of China (No. CX(16)1002) and the 5th Phase of "Project 333" of Jiangsu Province of China (No. BRA2019313).

Supplementary material

374_2019_1424_MOESM1_ESM.doc (4 mb)
ESM 1 (DOC 4127 kb)


  1. Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105:11512–11519. CrossRefPubMedGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. CrossRefGoogle Scholar
  3. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681. CrossRefPubMedGoogle Scholar
  4. Bai G-H, Desjardins AE, Plattner RD (2002) Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause diseasespread in wheat spikes. Mycopathologia 153:91–98. CrossRefGoogle Scholar
  5. Banerjee S, Kirkby CA, Schmutter D, Bissett A, Kirkegaard JA, Richardson AE (2016) 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
  6. Banerjee S, Schlaeppi K, van der Heijden MGA (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16:567–576. CrossRefPubMedGoogle Scholar
  7. Bani M, Cimmino A, Evidente A, Rubiales D, Rispail N (2018) Pisatin involvement in the variation of inhibition of Fusarium oxysporum f. sp. pisi spore germination by root exudates of Pisum spp. germplasm. Plant Pathol 67:1046–1054. CrossRefGoogle Scholar
  8. Baudoin E, Benizri E, Guckert A (2003) Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol Biochem 35:1183–1192. CrossRefGoogle Scholar
  9. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bremer E, Kuikman P (1994) Microbial utilization of 14C[U]glucose in soil is affected by the amount and timing of glucose additions. Soil Biol Biochem 26:511–517. CrossRefGoogle Scholar
  11. Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. CrossRefPubMedGoogle Scholar
  12. Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803. CrossRefPubMedGoogle Scholar
  13. Chen SC, Zhou XG, Yu HJ, Wu FZ (2018) Root exudates of potato onion are involved in the suppression of clubroot in a Chinese cabbage-potato onion-Chinese cabbage crop rotation. Eur J Plant Pathol 150:765–777. CrossRefGoogle Scholar
  14. Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. CrossRefGoogle Scholar
  15. Costa R, Götz M, Mrotzek N, Lottmann J, Berg G, Smalla K (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbio Ecol 56:236–249. CrossRefGoogle Scholar
  16. Cuthbert A, Jeffries P (1984) Mycoparasitism by Piptocephalis unispora within the Mortierellaceae. Transactions of the British Mycological Society 83:700–702. CrossRefGoogle Scholar
  17. de Cárcer AD, Denman SE, McSweeney C, Morrison M (2011) Evaluation of subsampling-based normalization strategies for tagged high-throughput sequencing data sets from gut microbiomes. Appl Environ Microb 77:8795–8798. CrossRefGoogle Scholar
  18. Deng Y, Jiang Y-H, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinformatics 13:113. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Eilers KG, Lauber CL, Knight R, Fierer N (2010) Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42:896–903. CrossRefGoogle Scholar
  21. Fierer N, Lennon JT (2011) The generation and maintenance of diversity in microbial communities. Am J Bot 98:439–448. CrossRefPubMedGoogle Scholar
  22. Foster EA, Franks DW, Morrell LJ, Balcomb KC, Parsons KM, van Ginneken A, Croft DP (2012) Social network correlates of food availability in an endangered population of killer whales, Orcinus orca. Anim Beha 83:731–736. CrossRefGoogle Scholar
  23. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes ‐ application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Green JL, Bohannan BJM, Whitaker RJ (2008) Microbial biogeography: from taxonomy to traits. Science 320:1039–1043. CrossRefPubMedGoogle Scholar
  25. Haichar FE, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80. CrossRefGoogle Scholar
  26. Hanson CA, Allison SD, Bradford MA, Wallenstein MD, Treseder KK (2008) Fungal taxa target different carbon sources in forest soil. Ecosystems 11:1157–1167. CrossRefGoogle Scholar
  27. Hao WY, Ren LX, Ran W, Shen QR (2010) Allelopathic effects of root exudates from watermelon and rice plants on Fusarium oxysporum f.sp. niveum. Plant Soil 336:485–497. CrossRefGoogle Scholar
  28. Henzi SP, Lusseau D, Weingrill T, van Schaik CP, Barrett L (2009) Cyclicity in the structure of female baboon social networks. Behav Ecol Sociobiol 63:1015–1021. CrossRefGoogle Scholar
  29. Kraffczyk I, Trolldenier G, Beringer H (1984) Soluble root exudates of maize: influence of potassium supply and rhizosphere microorganisms. Soil Biol Biochem 16:315–322CrossRefGoogle Scholar
  30. LaMondia JA (2015) Fusarium wilt of tobacco. Crop Prot 73:73–77. CrossRefGoogle Scholar
  31. Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399–1410.[1399:cotnan];2 CrossRefPubMedGoogle Scholar
  32. Li X, Rui J, Mao Y, Yannarell A, Mackie R (2014a) Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar. Soil Biol Biochem 68:392–401. CrossRefGoogle Scholar
  33. Li XG, Ding CF, Hua K, Zhang TL, Zhang YN, Zhao L, Yang YR, Liu JG, Wang XX (2014b) Soil sickness of peanuts is attributable to modifications in soil microbes induced by peanut root exudates rather than to direct allelopathy. Soil Biol Biochem 78:149–159. CrossRefGoogle Scholar
  34. Lievens B, Brouwer M, Vanachter ACRC, Lévesque CA, Cammue BPA, Thomma BPHJ (2005) Quantitative assessment of phytopathogenic fungi in various substrates using a DNA macroarray. Environ Microbiol 7:1698–1710. CrossRefGoogle Scholar
  35. Ling N, Zhang WW, Wang DS, Mao JG, Huang QW, Guo SW, Shen QR (2013) Root exudates from grafted-root watermelon showed a certain contribution in inhibiting Fusarium oxysporum f. sp. niveum. Plos One 8:e63383. CrossRefGoogle Scholar
  36. Liu YX, Li X, Cai K, Cai LT, Lu N, Shi JX (2015) Identification of benzoic acid and 3-phenylpropanoic acid in tobacco root exudates and their role in the growth of rhizosphere microorganisms. Appl Soil Ecol 93:78–87. CrossRefGoogle Scholar
  37. 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
  38. Lupatini M, Suleiman AKA, Jacques RJS, Antoniolli ZI, de Siqueira FA, Kuramae EE, Roesch LFW (2014) Network topology reveals high connectance levels and few key microbial genera within soils. Frontiers in Environmental Science 2:10. CrossRefGoogle Scholar
  39. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10. CrossRefGoogle Scholar
  40. May LA, Smiley B, Schmidt MG (2001) Comparative denaturing gradient gel electrophoresis analysis of fungal communities associated with whole plant corn silage. Can J Microbiol 47:829–841. CrossRefPubMedGoogle Scholar
  41. McCune B, Grace JB (2002) Analysis of ecological communities. MjM Software Design, Gleneden Beach, Oregon, USAGoogle Scholar
  42. Mielke PW, Berry KJ (2001) Permutation methods: a distance function approach. Springer, New YorkCrossRefGoogle Scholar
  43. Miyatake K, Saito T, Negoro S, Yamaguchi H, Nunome T, Ohyama A, Fukuoka H (2016) Detailed mapping of a resistance locus against Fusarium wilt in cultivated eggplant (Solanum melongena). Theor App Genet 129:357–367. CrossRefGoogle Scholar
  44. Petkovits T et al (2011) Data partitions, Bayesian analysis and phylogeny of the zygomycetous fungal family Mortierellaceae, inferred from nuclear ribosomal DNA sequences. Plos One 6:e27507. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Posas MB, Toyota K, Islam TMD (2007) Inhibition of bacterial wilt of tomato caused by Ralstonia solanacearum by sugars and amino acids. Microbes Environ 22:290–296. CrossRefGoogle Scholar
  46. Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, Daily G, Castilla JC, Lubchenco J, Paine RT (1996) Challenges in the quest for keystones. Bioscience 46:609–620. CrossRefGoogle Scholar
  47. 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
  48. 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
  49. Shi SJ, Nuccio E, Herman DJ, Rijkers R, Estera K, Li JB, Da Rocha UN, He ZL, Pett-Ridge J, Brodie EL, Zhou JZ, Firestone M (2015) Successional trajectories of rhizosphere bacterial communities over consecutive seasons. mBio 6:e00746-00715. CrossRefGoogle Scholar
  50. Shi L, Du NS, Yuan YH, Shu S, Sun J, Guo SR (2016a) Vinegar residue compost as a growth substrate enhances cucumber resistance against the Fusarium wilt pathogen Fusarium oxysporum by regulating physiological and biochemical responses. Environ Sci Pollut R 23:18277–18287. CrossRefGoogle Scholar
  51. Shi SJ, Nuccio EE, Shi ZJ, He ZL, Zhou JZ, Firestone MK (2016b) The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages. Ecol Lett 19:926–936. CrossRefPubMedGoogle Scholar
  52. Steinkellner S, Mammerler R, Vierheilig H (2005) Microconidia germination of the tomato pathogen Fusarium oxysporum in the presence of root exudates. J Plant Interact 1:23–30. CrossRefGoogle Scholar
  53. Tipton L, Muller CL, Kurtz ZD, Huang L, Kleerup E, Morris A, Bonneau R, Ghedin E (2018) Fungi stabilize connectivity in the lung and skin microbial ecosystems. Microbiome 6:12. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Torsvik V, Ovreas L, Thingstad TF (2002) Prokaryotic diversity - Magnitude, dynamics, and controlling factors. Science 296:1064–1066. CrossRefPubMedGoogle Scholar
  55. Uroz S, Buée M, Murat C, Frey-Klett P, Martin F (2010) Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Env Microbiol Rep 2:281–288. CrossRefGoogle Scholar
  56. 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
  57. Whalley WM, Taylor GS (1973) Influence of pea‐root exudates on germination of conidia and chlamydospores of physiologic races of Fusarium oxysporum f. pisi. Ann Appl Biol 73:269–276CrossRefGoogle Scholar
  58. Wu H-S, Luo J, Raza W, Liu Y-X, Gu M, Chen G, Hu X-F, Wang J-H, Mao Z-S, Shen Q-R (2010) Effect of exogenously added ferulic acid on in vitro Fusarium oxysporum f. sp. niveum. Scientia Horticulturae 124:448–453. CrossRefGoogle Scholar
  59. Xue C, Ryan Penton C, 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 54:95–106. CrossRefGoogle Scholar
  60. Yang RX, Gao ZG, Liu X, Yao Y, Cheng Y, Huang J, McDermott MI (2015) Effects of phenolic compounds of muskmelon root exudates on growth and pathogenic gene expression of Fusarium oxysporum f. sp melonis. Allelopathy J 35:175–185Google Scholar
  61. Yu XM, Ai CX, Xin L, Zhou GF (2011) The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. Eur J Soil Biol 47:138–145. CrossRefGoogle Scholar
  62. Zhalnina K, Louie KB, Hao Z, Mansoori N, da Rocha UN, Shi SJ, Cho HJ, Karaoz U, Loque D, Bowen BP, Firestone MK, Northen TR, Brodie EL (2018) Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3:470–480. CrossRefGoogle Scholar
  63. Zhao S, Liu DY, Ling N, Chen FD, Fang WM, Shen QR (2014) Bio-organic fertilizer application significantly reduces the Fusarium oxysporum population and alters the composition of fungi communities of watermelon Fusarium wilt rhizosphere soil. Biol Fert Soils 50:765–774. CrossRefGoogle Scholar
  64. Zhou J, Deng Y, Luo F, He Z, Tu Q, Zhi X (2010) Functional molecular ecological networks. mBio 1:e00169-00110.
  65. Zhou J, Deng Y, Luo F, He Z, Yang Y (2011) Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. mBio 2:e00122-00111. CrossRefGoogle Scholar
  66. Zhou JZ, Xue K, Xie JP, Deng Y, Wu LY, Cheng XL, Fei SF, Deng SP, He ZL, Van Nostrand JD, Luo YQ (2012) Microbial mediation of carbon-cycle feedbacks to climate warming. Nat Clim Change 2:106–110. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Institute of Agricultural Sciences and EnvironmentsJiangsu Academy of Agricultural SciencesNanjingPeople’s Republic of China
  2. 2.Key Laboratory of Agro-Environment in Downstream of Yangtze PlainMinistry of AgricultureNanjingPeople’s Republic of China
  3. 3.School of the Environment and Safety Engineering, Jiangsu UniversityNanjingPeople’s Republic of China

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