Abstract
Soil disinfestation is an important agricultural practice to conquer soil-borne diseases and thereby ensure crop productivity. Reductive soil disinfestation (RSD) had been developed as an environmentally friendly alternative to chemical soil disinfestation (CSD). However, the differences between CSD and RSD on soil-borne pathogen suppression and fungal community structure remain poorly understood. In this work, five treatments, i.e., untreated soil (CK), CSD with 0.5 t ha−1 dazomet (DZ), RSD with 10 t ha−1 ethanol (ET), 15 t ha−1 sugarcane bagasse (SB), and 15 t ha−1 bean dregs (BD), were performed to investigate their influences on disinfestation efficiency, fungal abundance, diversity, and community structure via quantitative PCR and high-throughput sequencing. RSD-related treatments, especially the BD treatment, effectively alleviated soil acidification and salinization. The fungal abundance and microbial activity considerably increased in the BD treatment and significantly declined in the DZ treatment as compared to the CK treatment. Moreover, both CSD and RSD-related treatments significantly inhibited the population of Fusarium oxysporum and the relative abundance of genus Fusarium. Fungal community structure was notably altered by CSD and RSD practices. Furthermore, both CSD and RSD harbored a distinct unique microbiome, with the DZ treatment dominated by the genus Mortierella and BD treatment predominated by the genera Zopfiella, Chaetomium, and Penicillium. Taken together, these results indicate that the BD treatment could considerably alleviate the soil deterioration, improve soil microbial activity, and reassemble a non-pathogen unique microbiome that have more disease-suppressive agents and thus might be a promising disinfestation practice to control soil-borne disease in monoculture system.





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References
Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J (2014) The placenta harbors a unique microbiome. Sci Transl Med 6(237):237ra65
Adam G, Duncan H (2001) Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biol Biochem 33(7):943–951
Anderson MJ (2005) Permutational multivariate analysis of variance. Department of Statistics, University of Auckland, Auckland 26:32–46
Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62(1):245–253
Blok WJ, Lamers JG, Termorshuizen AJ, Bollen GJ (2000) Control of soilborne plant pathogens by incorporating fresh organic amendments followed by tarping. Phytopathology 90(3):253–259
Burgin AJ, Hamilton SK (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ 5(2):89–96
Butler D (2013) Fungus threatens top banana. Nature 504(7479):195–196
Butler DM, Rosskopf EN, Kokalis-Burelle N, Albano JP, Muramoto J, Shennan C (2012) Exploring warm-season cover crop as carbon sources for anaerobic soil disinfestation (ASD). Plant Soil 355:149–165
Cai F, Chen W, Wei Z, Pang G, Li R, Ran W, Shen Q (2015) Colonization of Trichoderma harzianum strain SQR-T037 on tomato roots and its relationship to plant growth, nutrient availability and soil microflora. Plant Soil 388(1–2):337–350
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336
Cebolla V, Busto J, Ferrer A, Miguel A, Maroto V (2000) Methyl bromide alternatives on horticultural crops. Acta Hortic (532):237–242
Chávez R, Bull P, Eyzaguirre J (2006) The xylanolytic enzyme system from the genus Penicillium. J Biotechnol 123(4):413–433
Domínguez-Mendoza CA, Bello-López JM, Navarro-Noya YE, de León-Lorenzana AS, Delgado-Balbuena L, Gómez-Acata S, Ruíz-Valdiviezo VM, Ramirez-Villanueva DA, Luna-Guido M, Dendooven L (2014) Bacterial community structure in fumigated soil. Soil Biol Biochem 73:122–129
Dutta BK (1981) Studies on some fungi isolated from the rhizosphere of tomato plants and the consequent prospect for the control of Verticillium wilt. Plant Soil 63(2):209–216
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200
Eo J, Park K-C (2014) Effects of dazomet on soil organisms and recolonisation of fumigated soil. Pedobiologia 57(3):147–154
Fravel DR, Deahl KL, Stommel JR (2005) Compatibility of the biocontrol fungus Fusarium oxysporum strain CS-20 with selected fungicides. Biol Control 34(2):165–169
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118
Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KWT, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327(5968):1008–1010
Hanson CA, Allison SD, Bradford MA, Wallenstein MD, Treseder KK (2008) Fungal taxa target different carbon sources in forest soil. Ecosystems 11(7):1157–1167
Hewavitharana SS, Ruddell D, Mazzola M (2014) Carbon source-dependent antifungal and nematicidal volatiles derived during anaerobic soil disinfestation. Eur J Plant Pathol 140(1):39–52
Huang X, Liu L, Wen T, Zhu R, Zhang J, Cai Z (2015a) Illumina MiSeq investigations on the changes of microbial community in the Fusarium oxysporum f. sp. cubense infected soil during and after reductive soil disinfestation. Microbiol Res 181:33–42
Huang X, Wen T, Zhang J, Meng L, Zhu T, Cai Z (2015b) Toxic organic acids produced in biological soil disinfestation mainly caused the suppression of Fusarium oxysporum f. sp. cubense. BioControl 60(1):113–124
Huang X, Wen T, Zhang J, Meng L, Zhu T, Liu L, Cai Z (2015c) Control of soil-borne pathogen Fusarium oxysporum by biological soil disinfestation with incorporation of various organic matters. Eur J Plant Pathol 143(2):223–235
Huang X, Liu L, Wen T, Zhang J, Shen Q, Cai Z (2016a) Reductive soil disinfestations combined or not with Trichoderma for the treatment of a degraded and Rhizoctonia solani infested greenhouse soil. Sci Hortic 206:51–61
Huang X, Liu L, Wen T, Zhang J, Wang F, Cai Z (2016b) Changes in the soil microbial community after reductive soil disinfestation and cucumber seedling cultivation. Appl Microbiol Biotechnol 100(12):5581–5593
Ibekwe AM, Papiernik SK, Gan J, Yates SR, Yang C-H, Crowley DE (2001) Impact of fumigants on soil microbial communities. Appl Environ Microbiol 67(7):3245–3257
Klein E, Ofek M, Katan J, Minz D, Gamliel A (2013) Soil suppressiveness to Fusarium disease: shifts in root microbiome associated with reduction of pathogen root colonization. Phytopathology 103(1):23–33
Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22(21):5271–5277
Li R, Shen Z, Sun L, Zhang R, Fu L, Deng X, Shen Q (2016) Novel soil fumigation method for suppressing cucumber Fusarium wilt disease associated with soil microflora alterations. Appl Soil Ecol 101:28–36
Lievens B, Brouwer M, Vanachter ACRC, Lévesque CA, Cammue B, Thomma BPHJ (2005) Quantitative assessment of phytopathogenic fungi in various substrates using a DNA macroarray. Environ Microbiol 7(11):1698–1710
Liu L, Kong J, Cui H, Zhang J, Wang F, Cai Z, Huang X (2016) Relationships of decomposability and C/N ratio in different types of organic matter with suppression of Fusarium oxysporum and microbial communities during reductive soil disinfestation. Biol Control 101:103–113
Longoni P, Rodolfi M, Pantaleoni L, Doria E, Concia L, Picco AM, Cella R (2012) Functional analysis of the degradation of cellulosic substrates by a Chaetomium globosum endophytic isolate. Appl Environ Microbiol 78(10):3693–3705
Mao LG, Wang QX, Yan DD, Xie HW, Li Y, Guo MX, Cao AC (2012) Evaluation of the combination of 1, 3-dichloropropene and dazomet as an efficient alternative to methyl bromide for cucumber production in China. Pest Manag Sci 68(4):602–609
Momma N, Kobara Y, Momma M (2011) Fe2+ and Mn2+, potential agents to induce suppression of Fusarium oxysporum for biological soil disinfestation. J Gen Plant Pathol 77(6):331–335
Momma N, Kobara Y, Uematsu S, Kita N, Shinmura A (2013) Development of biological soil disinfestations in Japan. Appl Microbiol Biotechnol 97(9):3801–3809
Mowlick S, Inoue T, Takehara T, Kaku N, Ueki K, Ueki A (2013) Changes and recovery of soil bacterial communities influenced by biological soil disinfestation as compared with chloropicrin-treatment. AMB Express 3(1):46
Nannipieri P, Ascher J, Ceccherini M, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54(4):655–670
Nicola L, Turco E, Albanese D, Donati C, Thalheimer M, Pindo M, Insam H, Cavalieri D, Pertot I (2017) Fumigation with dazomet modifies soil microbiota in apple orchards affected by replant disease. Appl Soil Ecol 113:71–79
Ohr HD, Sims JJ, Grech NM, Becker JO, McGiffen Jr ME (1996) Methyl iodide, an ozone-safe alternative to methyl bromide as a soil fumigant. Plant Dis 80(7):731–735
Omirou M, Rousidou C, Bekris F, Papadopoulou KK, Menkissoglou-Spiroudi U, Ehaliotis C, Karpouzas DG (2011) The impact of biofumigation and chemical fumigation methods on the structure and function of the soil microbial community. Microb Ecol 61(1):201–213
Park J-H, Choi GJ, Jang KS, Lim HK, Kim HT, Cho KY, Kim J-C (2005) Antifungal activity against plant pathogenic fungi of chaetoviridins isolated from Chaetomium globosum. FEMS Microbiol Lett 252(2):309–313
Qiao K, Wang Z, Wei M, Wang H, Wang Y, Wang K (2015) Evaluation of chemical alternatives to methyl bromide in tomato crops in China. Crop Prot 67:223–227
R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna ISBN 3-900051-07-0
Raupach GS, Kloepper JW (2000) Biocontrol of cucumber diseases in the field by plant growth-promoting rhizobacteria with and without methyl bromide fumigation. Plant Dis 84(10):1073–1075
Ren L, Su S, Yang X, Xu Y, Huang Q, Shen Q (2008) Intercropping with aerobic rice suppressed fusarium wilt in watermelon. Soil Biol Biochem 40(3):834–844
Roberts DW (2007) labdsv: ordination and multivariate analysis for ecology. R package version 1(1)
Rousk J, Bååth E (2007) Fungal and bacterial growth in soil with plant materials of different C/N ratios. FEMS Microbiol Ecol 62(3):258–267
Samtani JB, Gilbert C, Weber JB, Subbarao KV, Goodhue RE, Fennimore SA (2012) Effect of steam and solarization treatments on pest control, strawberry yield, and economic returns relative to methyl bromide fumigation. HortSci 47(1):64–70
Shade A, Handelsman J (2012) Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol 14(1):4–12
Shi W-M, Yao J, Yan F (2009) Vegetable cultivation under greenhouse conditions leads to rapid accumulation of nutrients, acidification and salinity of soils and groundwater contamination in south-eastern China. Nutr Cycl Agroecosyst 83(1):73–84
Shinmura A (2000) Causal agent and control of root rot of welsh onion. PSJ Soil-borne Dis Workshop Rep 20:133–143
Ślusarski C, Pietr SJ (2009) Combined application of dazomet and Trichoderma asperellum as an efficient alternative to methyl bromide in controlling the soil-borne disease complex of bell pepper. Crop Prot 28(8):668–674
Sun R, Dsouza M, Gilbert JA, Guo X, Wang D, Guo Z, Ni Y, Chu H (2016) Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter. Environ Microbiol 18(12):5137–5150
Tenuta M, Lazarovits G (2002) Ammonia and nitrous acid from nitrogenous amendments kill the microsclerotia of Verticillium dahliae. Phytopathology 92(3):255–264
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172(8):4238–4246
Walther D, Gindrat D (1988) Biological control of damping-off of sugar-beet and cotton with Chaetomium globosum or a fluorescent Pseudomonas sp. Can J Microbiol 34(5):631–637
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267
Wang Q, Ma Y, Yang H, Chang Z (2014) Effect of biofumigation and chemical fumigation on soil microbial community structure and control of pepper Phytophthora blight. World J Microbiol Biotechnol 30(2):507–518
Wei Z, Yang X, Yin S, Shen Q, Ran W, Xu Y (2011) Efficacy of Bacillus-fortified organic fertiliser in controlling bacterial wilt of tomato in the field. Appl Soil Ecol 48(2):152–159
Xiong W, Li R, Ren Y, Liu C, Zhao Q, Wu H, Jousset A, Shen Q (2017) Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biol Biochem 107:198–207
Xu L, Ravnskov S, Larsen J, Nilsson RH, Nicolaisen M (2012) Soil fungal community structure along a soil health gradient in pea fields examined using deep amplicon sequencing. Soil Biol Biochem 46:26–32
Zhao J, Ni T, Li Y, Xiong W, Ran W, Shen B, Shen Q, Zhang R (2014) Responses of bacterial communities in arable soils in a rice-wheat cropping system to different fertilizer regimes and sampling times. PLoS One 9(1):e85301
Zhao J, Ni T, Li J, Lu Q, Fang Z, Huang Q, Zhang R, Li R, Shen B, Shen Q (2016) Effects of organic–inorganic compound fertilizer with reduced chemical fertilizer application on crop yields, soil biological activity and bacterial community structure in a rice–wheat cropping system. Appl Soil Ecol 99:1–12
Zhao J, Mei Z, Zhang X, Xue C, Zhang C, Ma T, Zhang S (2017a) Suppression of Fusarium wilt of cucumber by ammonia gas fumigation via reduction of Fusarium population in the field. Sci Rep 7:43103
Zhao J, Ni T, Xun W, Huang X, Huang Q, Ran W, Shen B, Zhang R, Shen Q (2017b) Influence of straw incorporation with and without straw decomposer on soil bacterial community structure and function in a rice-wheat cropping system. Appl Microbiol Biotechnol 101(11):4761–4773
Zhu T, Zhang J, Yang W, Cai Z (2013) Effects of organic material amendment and water content on NO, N2O, and N2 emissions in a nitrate-rich vegetable soil. Biol Fertil Soils 49(2):153–163
Funding
This study was financially supported by the National Natural Science Foundation of China (Grant Nos. 41701277, 41771281), the National Key Research and Development Program of China (2017YFD0200600), the Startup Funds of Nanjing Normal University (Grant No. 184080H202B136), the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions, and the Key Subjects of Jiangsu Province (Ecology).
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Zhao, J., Zhou, X., Jiang, A. et al. Distinct impacts of reductive soil disinfestation and chemical soil disinfestation on soil fungal communities and memberships. Appl Microbiol Biotechnol 102, 7623–7634 (2018). https://doi.org/10.1007/s00253-018-9107-1
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DOI: https://doi.org/10.1007/s00253-018-9107-1


