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Reductive soil disinfestation incorporated with organic residue combination significantly improves soil microbial activity and functional diversity than sole residue incorporation

  • Environmental biotechnology
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Abstract

Reductive soil disinfestation (RSD) is an effective agricultural practice to eliminate soil-borne pathogens that heavily relies on the organic substrate used. However, the influences of combined application of organic residues on disinfestation efficiency, soil microbiomes, and their associated functional characteristics are still not well-characterized. In this work, four treatments, i.e., untreated soil (CK), RSD with 15 t ha−1 sugarcane bagasse (SB), bean dregs (BD), and their combinations (1:1, SB+BD), were conducted to investigate their influence on disinfestation efficiency, microbial functional diversity, community diversity, and composition using Biolog analysis, real-time PCR, and high-throughput sequencing. The SB+BD treatment had synergetic effects on soil microbial activity, metabolic activity, and functional diversity with similar efficacy in pathogen elimination and soil salinization alleviation, as compared to the SB and BD treatments. Moreover, the SB+BD treatment distinctly altered the structure and composition of bacterial and fungal communities, especially enriched the core microbiomes associated with soil general functions such as organic decomposition and nitrate removal. The SB+BD treatment also strengthened the soil specific functions including disease suppression through the regulation of unique microbiomes. In addition, the microbial richness, diversity, and evenness were significantly higher in the SB+BD-treated soil as compared to the SB- and BD-treated soils. Taken together, RSD incorporated with organic residue combination not only efficiently restore the degraded soils, but also considerably improve soil functions, which may benefit to the health for the future plant generations.

Key points

• Organic residue combination effectively declines pathogen density.

• Organic residue combination improves soil microbial activity and functional diversity.

• The enriched core microbiome is responsible for soil general functions.

• The induced unique microbiome is important for soil specific functions.

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References

  • 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

    CAS  Google Scholar 

  • Anderson T-H (2003) Microbial eco-physiological indicators to asses soil quality. Agric Ecosyst Environ 98(1):285–293

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Bonanomi G, Antignani V, Capodilupo M, Scala F (2010) Identifying the characteristics of organic soil amendments that suppress soilborne plant diseases. Soil Biol Biochem 42(2):136–144

    CAS  Google Scholar 

  • Butler D (2013) Fungus threatens top banana. Nature 504(7479):195–196

    CAS  PubMed  Google Scholar 

  • Butler DM, Kokalis-Burelle N, Muramoto J, Shennan C, McCollum TG, Rosskopf EN (2012a) Impact of anaerobic soil disinfestation combined with soil solarization on plant–parasitic nematodes and introduced inoculum of soilborne plant pathogens in raised-bed vegetable production. Crop Prot 39(8):33–40

    CAS  Google Scholar 

  • Butler DM, Rosskopf EN, Kokalis-Burelle N, Albano JP, Muramoto J, Shennan C (2012b) Exploring warm-season cover crops as carbon sources for anaerobic soil disinfestation (ASD). Plant Soil 355(1-2):149–165

    CAS  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cavers PB (1995) Seed banks: memory in soil. Can J Soil Sci 75(1):11–13

    Google Scholar 

  • Cebolla V, Busto J, Ferrer A, Miguel A, Maroto V (2000) Methyl bromide alternatives on horticultural crops. Acta Hortic 532:237–242

    Google Scholar 

  • Coventry E, Noble R, Mead A, Whipps JM (2005) Suppression of Allium white rot (Sclerotium cepivorum) in different soils using vegetable wastes. Eur J Plant Pathol 111(2):101–112

    Google Scholar 

  • Ebben MH, Gandy DG, Spencer DM (2010) Toxicity of methyl bromide to soil-borne fungi. Plant Pathol 32(4):429–433

    Google Scholar 

  • Ebihara Y, Uematsu S, Nomiya S (2010) Control of Verticillium dahliae at a strawberry nursery by paddy-upland rotation. J Gen Plant Pathol 76(1):7–20

    Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461

    CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fisk MC, Ruether KF, Yavitt JB (2003) Microbial activity and functional composition among northern peatland ecosystems. Soil Biol Biochem 35(4):591–602

    CAS  Google Scholar 

  • Garland JL (1996) Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biol Biochem 28(2):213–221

    CAS  Google Scholar 

  • 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  Google Scholar 

  • Gullino ML, Minuto A, Gilardi G, Garibaldi A, Ajwa H, Duafala T (2002) Efficacy of preplant soil fumigation with chloropicrin for tomato production in Italy. Crop Prot 21(9):741–749

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Huang G, Huang Y, Hu H, Liu F, Zhang Y, Deng R (2015a) Remediation of nitrate–nitrogen contaminated groundwater using a pilot-scale two-layer heterotrophic–autotrophic denitrification permeable reactive barrier with spongy iron/pine bark. Chemosphere 130:8–16

    CAS  PubMed  Google Scholar 

  • Huang X, Liu L, Wen T, Zhu R, Zhang J, Cai Z (2015b) 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

    CAS  PubMed  Google Scholar 

  • Huang X, Wen T, Zhang J, Meng L, Zhu T, Cai Z (2015c) Toxic organic acids produced in biological soil disinfestation mainly caused the suppression of Fusarium oxysporum f. sp. cubense. BioControl 60(1):113–124

    CAS  Google Scholar 

  • Huang X, Wen T, Zhang J, Meng L, Zhu T, Liu L (2015d) Control of soil-borne pathogen Fusarium oxysporum by biological soil disinfestation with incorporation of various organic matters. Eu J Plant Pathol 143(2):223–235

    CAS  Google Scholar 

  • 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(12):5581–5593

    CAS  PubMed  Google Scholar 

  • Huang X, Zhao J, Zhou X, Han Y, Zhang J, Cai Z (2019) How green alternatives to chemical pesticides are environmentally friendly and more efficient. Eur J Soil Sci 70(3):518–529

    CAS  Google Scholar 

  • Kennedy AC, Smith KL (1995) Soil microbial diversity and the sustainability of agricultural soils. Plant Soil 170(1):75–86

    CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79(17):5112–5120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li B, Li Q, Xu Z, Zhang N, Shen Q, Zhang R (2014) Responses of beneficial Bacillus amyloliquefaciens SQR9 to different soilborne fungal pathogens through the alteration of antifungal compounds production. Front Microbiol 5:636

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Li Y, Wang B, Chang Y, Yang Y, Yao C, Huang X, Zhang J, Cai Z, Zhao J (2019) Reductive soil disinfestation effectively alleviates the replant failure of Sanqi ginseng through allelochemical degradation and pathogen suppression. Appl Microbiol Biotechnol 103(8):3581–3595

    CAS  PubMed  Google Scholar 

  • Liu F, Huang G, Fallowfield H, Guan H, Zhu L, Hu H (2013) Study on heterotrophic-autotrophic denitrification permeable reactive barriers (HAD PRBs) for in situ groundwater remediation. Springer, Heidelberg

    Google Scholar 

  • Liu X, Zhang J, Gu T, Zhang W, Shen Q, Yin S, Qiu H (2014) Microbial community diversities and taxa abundances in soils along a seven-year gradient of potato monoculture using high throughput pyrosequencing approach. PLoS One 9(1):e86610

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Mazzola M, Granatstein DM, Elfving DC, Mullinix K (2001) Suppression of specific apple root pathogens by Brassica napus seed meal amendment regardless of glucosinolate content. Phytopathology 91(7):673–679

    CAS  PubMed  Google Scholar 

  • McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6(3):610–618

    CAS  PubMed  Google Scholar 

  • Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Neveinas M, Anned VD, Marcel W, Alexanderr VB, Jaapd J, Trudiegc C, Aadj T, Arienahc VB, Wimj B (2007) Biological Soil Disinfestation (BSD), a new control method for potato brown rot, caused by Ralstonia solanacearum race 3 biovar 2. Eur J Plant Pathol 117(4):403–415

    Google Scholar 

  • Palaniyandi SA, Yang SH, Zhang L, Suh J-W (2013) Effects of actinobacteria on plant disease suppression and growth promotion. Appl Microbiol Biotechnol 97(22):9621–9636

    CAS  PubMed  Google Scholar 

  • Potin O, Rafin C, Veignie E (2004) Bioremediation of an aged polycyclic aromatic hydrocarbons (PAHs)-contaminated soil by filamentous fungi isolated from the soil. Int Biodeterior Biodegradation 54(1):45–52

    CAS  Google Scholar 

  • Prosser JI (2002) Molecular and functional diversity in soil micro-organisms. Plant Soil 244(1/2):9–17

    CAS  Google Scholar 

  • Shade A, Handelsman J (2012) Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol 14(1):4–12

    CAS  PubMed  Google Scholar 

  • Shen Z, Ruan Y, Xue C, Zhong S, Li R, Shen Q (2015) Soils naturally suppressive to banana Fusarium wilt disease harbor unique bacterial communities. Plant Soil 393(1-2):21–33

    CAS  Google Scholar 

  • Shennan C, Muramoto J, Koike ST, Daugovish O (2009) Optimizing anaerobic soil disinfestation for non-fumigated strawberry production in California. In: Obenauf GL (ed) Proceedings of the 16th Annual International Research Conference on Methyl Bromide Alternatives and Emissions Reductions. San Diego, CA. p. 23-1–23-4

  • Shennan C, Muramoto J, Koike S, Baird G, Fennimore S, Samtani J, Bolda M, Dara S, Daugovish O, Lazarovits G (2018) Anaerobic soil disinfestation is an alternative to soil fumigation for control of some soilborne pathogens in strawberry production. Plant Pathol 67:51–66

    CAS  Google Scholar 

  • Shi WM, 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

    CAS  Google Scholar 

  • Shinmura A (2000) Causal agent and control of root rot of welsh onion. PSJ Soilborne Dis Workshop Rep 20:133–143

    Google Scholar 

  • Shrestha U, Augé RM, Butler DM (2016) A meta-analysis of the impact of anaerobic soil disinfestation on pest suppression and yield of horticultural crops. Front Plant Sci 7:1254

    PubMed  PubMed Central  Google Scholar 

  • Sonku Y, Kita K (1979) A study on disease control by water. VII. Effect of organic amendment and tarping on soil Eh and disease incidence of Fusarium wilt of tomato. Jap J Phytopathol 45:524–525

    Google Scholar 

  • Szczech MM (1999) Suppressiveness of vermicompost against Fusarium wilt of tomato. J Phytopathol 147(3):155–161

    CAS  Google Scholar 

  • Tilston EL, Pitt D, Groenhof AC (2002) Composted recycled organic matter suppresses soil-borne diseases of field crops. New Phytol 154(3):731–740

    CAS  PubMed  Google Scholar 

  • Uchida T, Asari S, Ashizawa T (1981) Control of tomato Verticillium wilt by rotation with paddy field. J Gen Plant Pathol 28-48

  • Ueki A, Kaku N, Ueki K (2018) Role of anaerobic bacteria in biological soil disinfestation for elimination of soil-borne plant pathogens in agriculture. Appl Microbiol Biotechnol 102(15):6309–6318

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe B (1973) Effect of flooding on Rhizoctonia solani. Jap J Phytopathol 39:200

    Google Scholar 

  • 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

    Google Scholar 

  • Wen T, Huang X, Zhang J, Cai Z (2016) Effects of biological soil disinfestation and water regime on suppressing Artemisia selengensis root rot pathogens. J Soils Sediments 16(1):215–225

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Xun W, Huang T, Zhao J, Ran W, Wang B, Shen Q, Zhang R (2015) Environmental conditions rather than microbial inoculum composition determine the bacterial composition, microbial biomass and enzymatic activity of reconstructed soil microbial communities. Soil Biol Biochem 90:10–18

    CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Zhao J, Mei Z, Zhang X, Xue C, Zhang C, Ma T, Zhang S (2017) Suppression of Fusarium wilt of cucumber by ammonia gas fumigation via reduction of Fusarium population in the field. Sci Rep 7:43103

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Zhou X, Jiang A, Fan J, Lan T, Zhang J, Cai Z (2018) Distinct impacts of reductive soil disinfestation and chemical soil disinfestation on soil fungal communities and memberships. Appl Microbiol Biotechnol 102(17):7623–7634

    CAS  PubMed  Google Scholar 

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Funding

This study was financially supported by the National Natural Science Foundation of China (41701277, 41977032), the National Key Research and Development Program of China (2017YFD0200600), the China Postdoctoral Science Foundation (2018M630573, 2019T120442), the Startup Funds of Nanjing Normal University (184080H202B136), and the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions and the Key Subjects of Jiangsu Province (Ecology).

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Authors and Affiliations

  1. School of Geography, Nanjing Normal University, Nanjing, 210023, China

    Jun Zhao, Shuzhe Liu, Xing Zhou, Qing Xia, Xian Liu, Shuran Zhang, Jinbo Zhang, Zucong Cai & Xinqi Huang

  2. Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and Application, Nanjing, 210023, China

    Jun Zhao, Jinbo Zhang, Zucong Cai & Xinqi Huang

  3. Key Laboratory of Virtual Geographical Environment (Nanjing Normal University), Ministry of Education, Nanjing, 210023, China

    Jun Zhao & Jinbo Zhang

  4. Jiangsu Provincial Key Laboratory of Materials Cycling and Pollution Control, Nanjing Normal University, Nanjing, 210023, China

    Zucong Cai

  5. State Key Laboratory Cultivation Base of Geographical Environment Evolution, Nanjing, Jiangsu Province, 210023, China

    Xinqi Huang

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  1. Jun Zhao
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  2. Shuzhe Liu
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  3. Xing Zhou
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  4. Qing Xia
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  5. Xian Liu
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  9. Xinqi Huang
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Contributions

JZ, XQH, JBZ, and ZCC conceived and designed research. JZ, SZL, XZ, QX, XL, and SRZ conducted experiments. JZ and XZ analyzed data. JZ wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Xinqi Huang.

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Zhao, J., Liu, S., Zhou, X. et al. Reductive soil disinfestation incorporated with organic residue combination significantly improves soil microbial activity and functional diversity than sole residue incorporation. Appl Microbiol Biotechnol 104, 7573–7588 (2020). https://doi.org/10.1007/s00253-020-10778-7

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