Abstract
Soil microbial communities are key players responsible for imparting suppressive potential to the soil against soil-borne phytopathogens. Fungi have an immense potential to inhibit soil-borne phytopathogens, but the fungal counterpart has been less explored in this context. We assessed the composition of fungal communities in soil under long-term organic and conventional farming practice, and control soil. The disease-suppressive potential of organic field was already established. A comparative analysis of the disease suppressiveness contributed by the fungal component of soil from conventional and organic farms was assessed using dual culture assays. The quantification of biocontrol markers and total fungi was done; the characterization of fungal community was carried out using ITS-based amplicon sequencing. Soil from organic field exhibited higher disease-suppressive potential than that from conventional farming, against the pathogens selected for the study. Higher levels of hydrolytic enzymes such as chitinase and cellulase, and siderophore production were observed in soil from the organic field compared to the conventional field. Differences in community composition were observed under conventional and organic farming, with soil from organic field exhibiting specific enrichment of key biocontrol fungal genera. The fungal alpha diversity was lower in soil from the organic field compared to the conventional field. Our results highlight the role of fungi in contributing to general disease-suppressive ability of the soil against phytopathogens. The identification of fungal taxa specifically associated with organic farming can aid in understanding the mechanism of disease suppression under such a practice, and can be exploited to induce general disease suppressiveness in otherwise conducive soil.
Similar content being viewed by others
Data and Materials Availability
Data on the ITS sequences analyzed in this study is available in the NCBI SRA database under BioProject ID: PRJNA901449.
References
Toyota K (2021) Studies on ecology, diagnosis, and control of soilborne plant pathogens and plant parasitic nematodes: a synthesis. Soil Sci Plant Nutr 67:18–25
Chen G, Cao L, Cao C, Zhao P, Li F, Xu B, Huang Q (2021) Effective and sustained control of soil-borne plant diseases by biodegradable polyhydroxybutyrate mulch films embedded with fungicide of prothioconazole. Molecules 26:762
Du S, Trivedi P, Wei Z, Feng J, Hu HW, Bi L, Huang Q, Liu YR (2022) The proportion of soil-borne fungal pathogens increases with elevated organic carbon in agricultural soils. Msystems 7:e01337-e1421
Zhang W (2018) Global pesticide use: profile, trend, cost/benefit and more. Proc Int Acad Ecol Environ Sci 8:1
Wang Y, Zhu Y, Zhang S, Wang Y (2018) What could promote farmers to replace chemical fertilizers with organic fertilizers? J Clean Prod 199:882–890
Ge G, Li Z, Fan F, Chu G, Hou Z, Liang Y (2010) Soil biological activity and their seasonal variations in response to long-term application of organic and inorganic fertilizers. Plant Soil 326:31–44
Lin W, Lin M, Zhou H, Wu H, Li Z, Lin W (2019) The effects of chemical and organic fertilizer usage on rhizosphere soil in tea orchards. PLoS One 14:e0217018
Gu S, Hu Q, Cheng Y, Bai L, Liu Z, Xiao W, Gong Z, Wu Y, Feng K, Deng Y, Tan L (2019) Application of organic fertilizer improves microbial community diversity and alters microbial network structure in tea (Camellia sinensis) plantation soils. Soil Till Res 195:104356
Khatri S, Dubey S, Shivay YS, Jelsbak L, Sharma S (2023) Organic farming induces changes in bacterial community and disease suppressiveness against fungal phytopathogens. Appl Soil Ecol 181:104658
Khatri S, Sazinas P, Strube ML, Ding L, Dubey S, Shivay S, Jelsbak L, Sharma S (2023) Pseudomonas is a key player in conferring disease suppressiveness in organic farming. In press, Plant and Soil
Li H, Cai X, Gong J, Xu T, Ding GC, Li J (2019) Long-term organic farming manipulated rhizospheric microbiome and Bacillus antagonism against pepper blight (Phytophthora capsici). Front Microbiol 10:342
de Corato U (2020) Soil microbiota manipulation and its role in suppressing soil-borne plant pathogens in organic farming systems under the light of microbiome-assisted strategies. Chem Biol Technol Agric 7:1–26
Löbmann MT, Vetukuri RR, de Zinger L, Alsanius BW, Grenville-Briggs LJ, Walter AJ (2016) The occurrence of pathogen suppressive soils in Sweden in relation to soil biota, soil properties, and farming practices. Appl Soil Ecol 107:57–65
Penton CR, Gupta VVSR, Tiedje JM, Neate SM, Ophel-Keller K, Gillings M, Harvey P, Pham A, Roget DK (2014) Fungal community structure in disease suppressive soils assessed by 28S LSU gene sequencing. PLoS One 9:e93893
Shi W, Li M, Wei G, Tian R, Li C, Wang B, Lin R, Shi C, Chi X, Zhou B, Gao Z (2019) The occurrence of potato common scab correlates with the community composition and function of the geocaulosphere soil microbiome. Microbiome 7:1–18
Jayaraman S, Naorem AK, Lal R, Dalal RC, Sinha NK, Patra AK, Chaudhari SK (2021) Disease-suppressive soils—beyond food production: a critical review. J Soil Sci Plant Nutr 21:1437–1465
Schlatter D, Kinkel L, Thomashow L, Weller D, Paulitz T (2017) Disease suppressive soils: new insights from the soil microbiome. Phytopathology 107:1284–1297
Weller DM, LeTourneau M, Yang M (2022) Classification, discovery, and microbial basis of disease‐suppressive soils. Good Microbes Med, Food Prod, Biotechnol, Bioremed Agric 457–465.
Chen D, Wang X, Zhang W, Zhou Z, Ding C, Liao Y, Li X (2020) Persistent organic fertilization reinforces soil-borne disease suppressiveness of rhizosphere bacterial community. Plant Soil 452:313–328
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
Hernández-Lara LA, Ros M, Cuartero J, Bustamante MÁ, Moral R, Andreu-Rodríguez FJ, Pascual JA (2022) Bacterial and fungal community dynamics during different stages of agro-industrial waste composting and its relationship with compost suppressiveness. Sci Total Environ 805:150330
Siegel-Hertz K, Edel-Hermann V, Chapelle E, Terrat S, Raaijmakers JM, Steinberg C (2018) Comparative microbiome analysis of a Fusarium wilt suppressive soil and a Fusarium wilt conducive soil from the Châteaurenard region. Front Microbiol 9:568
Rodriguez-Kabana R, Godoy G, Morgan-Jones G, Shelby RA (1983) The determination of soil chitinase activity: conditions for assay and ecological studies. Plant Soil 75:95–106
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analyt Chem 31:426–428
Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56
Chowdappa S, Jagannath S, Konappa N, Udayashankar AC, Jogaiah S (2020) Detection and characterization of antibacterial siderophores secreted by endophytic fungi from Cymbidium aloifolium. Biomolecules 10:1412
Rinttilä T, Kassinen A, Malinen E, Krogius L, Palva A (2004) Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 97:1166–1177
Boyle SA, Yarwood RR, Bottomley PJ, Myrold DD (2008) Bacterial and fungal contributions to soil nitrogen cycling under Douglas fir and red alder at two sites in Oregon. Soil Biol Biochem 40:443–451
Fang X, Wang H, Zhao L, Wang M, Sun M (2022) Diversity and structure of the rhizosphere microbial communities of wild and cultivated ginseng. BMC Microbiol 22:1–12
Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research. John Wiley & Sons
Gu Z, Eils R, Schlesner M (2016) Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32:2847–2849
Edel-Hermann V, Lecomte C (2019) Current status of Fusarium oxysporum formae speciales and races. Phytopathology 109:512–530
Yu H, Zhou Q, Hwang SF, Ho AJ, Chang KF, Strelkov SE, He Y, Conner RL, Harding MW (2021) Pathogenicity, anastomosis groups, host range, and genetic diversity of Rhizoctonia species isolated from soybean, pea, and other crops in Alberta and Manitoba, Canada. Can J Plant Sci 102:301–315
Tang L, Xia Y, Fan C, Kou J, Wu F, Li W, Pan K (2020) Control of Fusarium wilt by wheat straw is associated with microbial network changes in watermelon rhizosphere. Sci Rep 10:12736
Behera HT, Mojumdar A, Behera SS, Das S, Ray L (2022) Biocontrol of wilt disease of rice seedlings incited by Fusarium oxysporum through soil application of Streptomyces chilikensis RC1830. Lett in Appl Microbiol 75:1366–1382
Pfenning LH, de Melo MP, Costa MM, Reis A, Cabral CS, Lima CS, Costa SS (2019) Fusarium udum revisited: a common, but poorly understood member of the Fusarium fujikuroi species complex. Mycol Prog 18:107–117
Hartl L, Zach S, Seidl-Seiboth V (2012) Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Appl Microbiol Biotechnol 93:533–543
Hjort K, Presti I, Elväng A, Marinelli F, Sjöling S (2014) Bacterial chitinase with phytopathogen control capacity from suppressive soil revealed by functional metagenomics. Appl Microbiol Biotechnol 98:2819–2828
Berini F, Presti I, Beltrametti F, Pedroli M, Vårum KM, Pollegioni L, Sjoling S, Marinelli F (2017) Production and characterization of a novel antifungal chitinase identified by functional screening of a suppressive-soil metagenome. Microb Cell Factories 16:1–15
Phitsuwan P, Laohakunjit N, Kerdchoechuen O, Kyu KL, Ratanakhanokchai K (2013) Present and potential applications of cellulases in agriculture, biotechnology, and bioenergy. Folia Microbiol 58:163–176
Rasmussen PH, Knudsen IM, Elmholt S, Jensen DF (2002) Relationship between soil cellulolytic activity and suppression of seedling blight of barley in arable soils. Appl Soil Ecol 19:91–96
Sadeghi A, Koobaz P, Azimi H, Karimi E, Akbari AR (2017) Plant growth promotion and suppression of Phytophthora drechsleri damping-off in cucumber by cellulase-producing Streptomyces. Biocontrol 62:805–819
Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959
Saraf M, Pandya U, Thakkar A (2014) Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol Res 169:18–29
Ahmed E, Holmström SJ (2014) Siderophores in environmental research: roles and applications. Microb Biotechnol 7:196–208
Ghosh SK, Banerjee S, Sengupta C (2017) Bioassay, characterization and estimation of siderophores from some important antagonistic fungi. J Biopestic 10:105–112
Wong PTW, Baker R (1984) Suppression of wheat take-all and Ophiobolus patch by fluorescent pseudomonads from a Fusarium-suppressive soil. Soil Biol Biochem 16:397–403
Carrión VJ, Cordovez V, Tyc O, Etalo DW, de Bruijn I, de Jager VC, Medema MH, Eberl L, Raaijmakers JM (2018) Involvement of Burkholderiaceae and sulfurous volatiles in disease-suppressive soils. ISME J 12:2307–2321
Tracanna V, Ossowicki A, Petrus ML, Overduin S, Terlouw BR, Lund G, Robinson SL, Warris S, Schijlen EGWM, van Wezel GP, Raiijmakers JM, Garbeva P, Medema MH (2021) Dissecting disease-suppressive rhizosphere microbiomes by functional amplicon sequencing and 10× metagenomics. MSystems 6:e01116-e1120
Baldrian P, Větrovský T, Cajthaml T, Dobiášová P, Petránková M, Šnajdr J, Eichlerová I (2013) Estimation of fungal biomass in forest litter and soil. Fungal Ecol 6:1–11
Vanegas J, Munoz-Garcia A, Pérez-Parra KA, Figueroa-Galvis I, Mestanza O, Polanía J (2019) Effect of salinity on fungal diversity in the rhizosphere of the halophyte Avicennia germinans from a semi-arid mangrove. Fungal Ecol 42:100855
Mbareche H, Veillette M, Bilodeau G, Duchaine C (2020) Comparison of the performance of ITS1 and ITS2 as barcodes in amplicon-based sequencing of bioaerosols. PeerJ 8:e8523
Zhong W, Gu T, Wang W, Zhang B, Lin X, Huang Q, Shen W (2010) The effects of mineral fertilizer and organic manure on soil microbial community and diversity. Plant Soil 326:511–522
Wang, J, Song Y, Ma T, Raza W, Li J, Howland JG, ... Shen Q (2017) Impacts of inorganic and organic fertilization treatments on bacterial and fungal communities in a paddy soil. Appl Soil Ecol112:42-50.
Klapec T, Cholewa G, Cholewa A, Dutkiewicz J, Wójcik-Fatla A (2018) Fungal diversity of root vegetables and soil rhizosphere collected from organic and conventional farms in Eastern Poland. Ann Agric Environ Medicine 25:374–381
Sharma-Poudyal D, Schlatter D, Yin C, Hulbert S, Paulitz T (2017) Long-term no-till: a major driver of fungal communities in dryland wheat cropping systems. PLoS One 12:e0184611
Sun R, Li W, Dong W, Tian Y, Hu C, Liu B (2018) Tillage changes vertical distribution of soil bacterial and fungal communities. Front Microbiol 9:699
Liu X, Zhang Y (2021) Exploring the communities of bacteria, fungi and ammonia oxidizers in rhizosphere of Fusarium-diseased greenhouse cucumber. Appl Soil Ecol 161:103832
Wang Q, Zhou L, Jin H, Cong B, Yang H, Wang S (2022) Investigating the responses of microbial communities to banana Fusarium wilt in suppressive and conducive soils based on soil particle-size differentiation. Agronomy 12:229
Ali A, Ghani MI, Haiyan D, Iqbal M, Cheng Z, Cai Z (2020) Garlic substrate induces cucumber growth development and decreases Fusarium wilt through regulation of soil microbial community structure and diversity in replanted disturbed soil. Int J Mol Sci 21:6008
Shen Z, Ruan Y, Chao X, Zhang J, Li R, Shen Q (2015) Rhizosphere microbial community manipulated by 2 years of consecutive biofertilizer application associated with banana Fusarium wilt disease suppression. Biol Fertil Soils 51:553–562
Wang B, Sun M, Yang J, Shen Z, Ou Y, Fu L, Zhao Y, Li R, Ruan Y, Shen Q (2022) Inducing banana Fusarium wilt disease suppression through soil microbiome reshaping by pineapple–banana rotation combined with biofertilizer application. Soil 8:17–29
Lu SW, Kroken S, Lee BN, Robbertse B, Churchill AC, Yoder OC, Turgeon BG (2003) A novel class of gene controlling virulence in plant pathogenic ascomycete fungi. Proc Nat Acad Sci 100:5980–5985
Lang J, Hu J, Ran W, Xu Y, Shen Q (2012) Control of cotton Verticillium wilt and fungal diversity of rhizosphere soils by bio-organic fertilizer. Biol Fertil Soils 48:191–203
Sasan RK, Bidochka MJ (2013) Antagonism of the endophytic insect pathogenic fungus Metarhizium robertsii against the bean plant pathogen Fusarium solani f. sp. phaseoli. Can J Plant Path 35:288–293
Zhang G, Wang F, Qin J, Wang D, Zhang J, Zhang Y, Zhang S, Pan H (2013) Efficacy assessment of antifungal metabolites from Chaetomium globosum no. 05, a new biocontrol agent, against Setosphaeria turcica. Biol Control 64:90–98
Zhao SS, Zhang YY, Yan W, Cao LL, Xiao Y, Ye YH (2017) Chaetomium globosum CDW7, a potential biological control strain and its antifungal metabolites. Microbiol Lett 364:fnw287
Sarven MS, Hao Q, Deng J, Yang F, Wang G, Xiao Y, Xiao X (2020) Biological control of tomato gray mold caused by Botrytis cinerea with the entomopathogenic fungus Metarhizium anisopliae. Pathogens 9:213
Nakasaki K, Saito M, Suzuki N (2007) Coprinellus curtus (Hitoyo-take) prevents diseases of vegetables caused by pathogenic fungi. FEMS Microbiol Lett 275:286–291
Zhang H, Wang L, Ma L, Dong Y, Jiang S, Xu B, Zheng X (2009) Biocontrol of major postharvest pathogens on apple using Rhodotorula glutinis and its effects on postharvest quality parameters. Biol Control 48:79–83
Bautista-Rosales PU, Calderon-Santoyo M, Servín-Villegas R, Ochoa-Álvarez NA, Vázquez-Juárez R, Ragazzo-Sánchez JA (2014) Biocontrol action mechanisms of Cryptococcus laurentii on Colletotrichum gloeosporioides of mango. Crop Prot 65:194–201
Qin GZ, Tian SP (2004) Biocontrol of postharvest diseases of jujube fruit by Cryptococcus laurentii combined with a low dosage of fungicides under different storage conditions. Plant Dis 88:497–501
Durán P, Viscardi S, Acuña JJ, Cornejo P, Azcón R, Mora MDLL (2018) Endophytic selenobacteria and arbuscular mycorrhizal fungus for selenium biofortification and Gaeumannomyces graminis biocontrol. J Soil Sci Plant Nutr 18:1021–1035
Pánek M, Hanáček A, Wenzlová J, Maňasová M, Zouhar M (2021) A comparison of the ability of some commercially produced biological control agents to protect strawberry plants against the plant pathogen Phytophthora cactorum. Agriculture 11:1086
Ravnskov S, Cabral C, Larsen J (2020) Mycorrhiza induced tolerance in Cucumis sativus against root rot caused by Pythium ultimum depends on fungal species in the arbuscular mycorrhizal symbiosis. Biol Control 14:104133
Ros M, Raut I, Santisima-Trinidad AB, Pascual JA (2017) Relationship of microbial communities and suppressiveness of Trichoderma fortified composts for pepper seedlings infected by Phytophthora nicotianae. PLoS One 12:e0174069
Khan FI, Bisetty K, Singh S, Permaul K, Hassan M (2015) Chitinase from Thermomyces lanuginosus SSBP and its biotechnological applications. Extremophiles 19:1055–1066
Zhang D, Yan D, Cheng H, Fang W, Huang B, Wang X, Yan Y, Oyuyang C, Li Y, Wang Q, Cao A (2020) Effects of multi-year biofumigation on soil bacterial and fungal communities and strawberry yield. Environ Pollut 256:113415
Ali A, Elrys AS, Liu L, Xia Q, Wang B, Li Y, Dan X, Iqbal M, Zhao J, Huang X, Cai Z (2022) Deciphering the synergies of reductive soil disinfestation combined with biochar and antagonistic microbial inoculation in cucumber fusarium wilt suppression through rhizosphere microbiota structure. Microbial Ecol, In Press,. https://doi.org/10.1007/s00248-022-02097-3
Hartmann M, Frey B, Mayer J, Mäder P, Widmer F (2015) Distinct soil microbial diversity under long-term organic and conventional farming. ISME J 9:1177–1194
Schneider S, Hartmann M, Enkerli J, Widmer F (2010) Fungal community structure in soils of conventional and organic farming systems. Fung Ecol 3:215–224
Zhang H, Zheng X, Bai N, Li S, Zhang J, Lv W (2019) Responses of soil bacterial and fungal communities to organic and conventional farming systems in East China. J Microbial Biotechnol 29:441–453
Esmaeilzadeh-Salestani K, Bahram M, Seraj RGM, Gohar D, Tohidfar M, Eremeev V, Talgre L, Khaleghdoust B, Mirmajlessi SM, Luik A, Loit E (2021) Cropping systems with higher organic carbon promote soil microbial diversity. Agric Ecosys Environ 319:107521
Funding
To support this study, funding was received from the M-FIRP scheme of IIT Delhi and ICAR (MI02024) and IIT Delhi and TU Delft (MI02535). SK received a fellowship from University Grants Commission, India, to support her Ph.D. PC acknowledges the fellowship received from University of Queensland–Indian Institute of Technology Delhi Academy of Research (UQIDAR).
Author information
Authors and Affiliations
Contributions
SK: methodology, investigation, formal analysis, writing—original draft preparation, PC: investigation, writing—review and editing, YS: investigation, project administration, funding acquisition, writing—review and editing, SS: conceptualization, project administration, funding acquisition, supervision, writing—review and editing.
Corresponding author
Ethics declarations
Competing Interests
The authors declare no competing interests.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Khatri, S., Chaudhary, P., Shivay, Y.S. et al. Role of Fungi in Imparting General Disease Suppressiveness in Soil from Organic Field. Microb Ecol 86, 2047–2059 (2023). https://doi.org/10.1007/s00248-023-02211-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-023-02211-z