Abstract
Soil weakness across consecutive cropping fields can be partially explained by the changes in microbial community diversity and structure. Succession patterns and co-occurrence mechanisms of bacteria and fungi, especially beneficial or pathogenic memberships in continuous cropping strawberry fields and their response to edaphic factors remained unclear. In this study, Illumina sequencing of bacterial 16S ribosomal RNA and fungal internal transcribed spacer genes was applied in three time-course (1, 5, and 10 years) fields across spring and winter. Results showed that the richness and diversity of bacterial and fungal communities increased significantly (p < 0.05) in 1-year field and decreased afterwards across two seasons. Network analysis revealed beneficial bacterial and fungal genus (Bacillus and Trichoderma) dominated under 1-year field whereas Fusarium accumulated under 10-year field at either season. Moreover, Trichoderma harzianum and Bacillus subtilis that have been reported to effectively control Fusarium wilt in strawberries accumulated significantly under 1-year field. Canonical correspondence analysis showed that beneficial bacterial Rhodospirillales and Rhizobiales and fungal Glomerales accumulated in 1-year field and their distributions were significantly affected by soil pH, microbial biomass C (MBC), and moisture. On the contrary, fungal pathogenic species Fusarium oxysporum strongly increased under 10-year field at the winter sample and the abundance was positively (p < 0.01) correlated with soil moisture. Our study suggested that the potential of microcosm under 1-year field stimulates the whole microbial diversity and favors different beneficial taxa across two seasons. Soil pH, moisture, and MBC were the most important edaphic factors leading to contrasting beneficial and pathogenic memberships across consecutive strawberry cropping fields.
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References
Banerjee S, Kirky 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. https://doi.org/10.1016/j.soilbio.2016.03.017
Baroncelli R, Zapparata A, Sarrocco S, Sukno SA, Lane CR, Thon MR, Vannacci G, Holub E, Sreenivasaprasad S (2015) Molecular diversity of anthracnose pathogen populations associated with UK strawberry production suggests multiple introductions of three different Colletotrichum species. PLoS One 10:e0129140. https://doi.org/10.1371/journal.pone.0129140
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Stat 57:289–300 http://www.jstor.org/stable/2346101
Chase JM, Kraft NJ, Smith KG, Vellend M, Inouye BD (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:art24. https://doi.org/10.1890/ES10-00117.1
Chen MN, Li X, Yang QL, Chi XY, Pan LJ, Chen N, Yang Z, Wang T, Wang M, Yu SL (2012) Soil eukaryotic microorganism succession as affected by continuous cropping of peanut—pathogenic and beneficial fungi were selected. PLoS One 7:e40659
Chen MN, Li X, Yang QL, Chi XY, Pan LJ, Chen N, Yang Z, Wang T, Wang M, Yu SL (2014) Dynamic succession of soil bacterial community during continuous cropping of peanut (Arachis hypogaea L). PLoS One 9:e101355
de Boer W, Knowalchuk GA (2001) Nitrification in acid soils: microorganisms and mechanisms. Soil Biol Biochem 33:853–866. https://doi.org/10.1016/S0038-0717(00)00247-9
Dos Santos CP, Fang Z, Mason SW, Setubal JC, Dixon R (2012) Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics 13:62. https://doi.org/10.1186/1471-2164-13-162
Fang XL, You MP, Barbetti MJ (2012) Reduced severity and impact of Fusarium wilt on strawberry by manipulation of soil pH, soil organic amendments and crop rotation. Eur J Plant Pathol 134:619–629. https://doi.org/10.1007/s10658-012-0042-1
Freedman Z, Zak DR (2015) Soil bacterial communities are shaped by temporal and environmental filtering: evidence from a long term chronosequence. Environ Microbiol 17:3208–3218. https://doi.org/10.1111/1462-2920.12762
Freeman S, Minz D, Kolesnik I, Barbul O, Zveibil A, Maymon M, Nitzani Y, Kirshner B, Rav-David D, Bilu A, Dag A, Shafir S, Elad Y (2004) Trichoderma biocontrol of Colletotrichum acutatum and Botrytis cinerea and survival in strawberry. Eur J Plant Pathol 110:361–370. https://doi.org/10.1023/B:EJPP.0000021057.93305.d9
Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. Forest Ecol Manag 196:159–171. https://doi.org/10.1016/j.foreco.2004.03.018
Hartmann M, Niklaus PA, Zimmermann S, Schmutz S, Kremer J, Abarenkov K, Luscher P, Widmer F, Fery B (2014) Resistance and resilience of the forest soil microbiome to logging-associated compaction. ISME J 8:226–244. https://doi.org/10.1038/ismej.2013.141
Henry PM, Kirkpatrick SC, Islas CM, Pastrana AM, Yoshisato JA (2017) The population of Fusarium oxysporum f sp fragariae, cause of fusarium wilt of strawberry, in California. Plant Dis 101:550–556. https://doi.org/10.1094/PDIS-07-16-1058-RE
Huang Y, Li YY, Yao HY (2014) Nitrate enhances N2O emission more than ammonium in a highly acidic soil. J Soils Sediments 14:146–154. https://doi.org/10.1007/s11368-013-0785-0
Huang Y, Long XE, Chapman SJ, Yao HY (2015) Acidophilic denitrifiers dominate the N2O production in a 100-year-old tea orchard soil. Environ Sci Pollut R 22:4173–4182. https://doi.org/10.1007/s11356-014-3653-6
Jayasekhaer M, Manonmani K, Justin CGL (2008) Development of integrated biocontrol strategy for the management of stem rot disease (Fusarium oxysporum f sp Vanillae) of Vanilla. Agric Sci Dig 28:109–111
Joergensen RG, Wichern F (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol Biochem 40:2977–2991. https://doi.org/10.1016/j.soilbio.2008.08.017
Jones D, Keddie RM (2006) The genus Arthrobacter. The prokaryotes 3:945–960. https://doi.org/10.1007/0-387-30743-5_36
Koike S, Gordon TR (2015) Management of Fusarium wilt of strawberry. Crop Prot 73:67–72. https://doi.org/10.1016/j.cropro.2015.02.003
Kong AYY, Scow KM, Córdova-Kreylos AL, Holmes WE, Six J (2011) Microbial community composition and carbon cycling within soil microenvironments of conventional, low input, and organic cropping systems. Soil Biol Biochem 43:20–30. https://doi.org/10.1016/j.soilbio.2010.09.005
Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415. https://doi.org/10.1016/j.soilbio.2008.05.021
Li XY, Lewis EE, Liu QZ, Li HQ, Bai CQ, Wang YZ (2016) Effects of long-term continuous cropping on soil nematode community and soil condition associated with replant problem in strawberry habitat. Sci Rep 6:30466. https://doi.org/10.1038/srep30466
Liu X, Zhang JL, Gu TY, Zhang WM, Shen QR, Yin SX, Qiu HZ (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:e86610. https://doi.org/10.1371/journal.pone.0086610
Liu WX, Wang QL, Wang BZ, Wang XB, Franks AE, Teng Y, Li ZG, Luo YM (2015) Changes in the abundance and structure of bacterial communities under long-term fertilization treatments in a peanut monocropping system. Plant Soil 395:415–427. https://doi.org/10.1007/s11104-015-2569-3
Lozupone C, Hamady M, Knight R (2006) UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinf 7:371. https://doi.org/10.1186/1471-2105-7-371
Maas JL, Galleta GJ (1996) Recent progress in strawberry disease research. ISHS Acta Hortic. https://doi.org/10.17660/ActaHortic1997439128
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. https://doi.org/10.1126/science.1203980
Mo AS, Qiu ZQ, He Q, Wu HY, Zhou XB (2016) Effect of continuous monocropping of tomato on soil microorganism and microbial biomass carbon. Commun Soil Sci Plan 47:1069–1077. https://doi.org/10.1080/00103624.2016.1165832
Moon BJ, Chung HS, Park HC (1995) Studies on antagonism of Trichoderma species to Fusarium oxysporum f.sp. fragariae. V. Biological control of Fusarium wilt of strawberry by a mycoparasite, Trichoderma harzianum. Korean J Plant Pathol 11:298–303
Nam HM, Park MS, Kim HG, Yoo SJ (2009) Biological control of strawberry Fusarium wilt caused by Fusarium oxysporum f sp fragariae using Bacillus velezensis BS87 and RK1 formulation. J Microbiol Biotechnol 19:520–524. https://doi.org/10.4014/jmb.0805.333
Oksanen J, Blanchet G, Kindt R, Legendre P, O’Hara RG, Simpson GL, Solymos P, Stevens MHH, Wagner H (2010) Vegan: community ecology package. R package version 1.17-1. http://CRANR-project.org/package=vegan. Accessed 10 May 2012
Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124. https://doi.org/10.1093/bioinformatics/btu494
Romanowicz KJ, Freedman ZB, Upchurch RA, Argiroff WA, Zak DR (2016) Active microorganisms in forest soils differ from the total community yet are shaped by the same environmental factors: the influence of pH and soil moisture. FEMS Microbiol Ecol 92:fiw149. https://doi.org/10.1093/femsec/fiw149
Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. https://doi.org/10.1038/ismej.2010.58
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
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. https://doi.org/10.1101/gr.1239303
Shukla SK, Lal M, Singh SK (2013) Improving bud sprouting, growth and yield of winter initiated sugarcane ratoon through tillage cum organic mediated rhizospheric modulation in Udic ustochrept under subtropical Indian condition. Soil Till Res 126:50–59. https://doi.org/10.1016/j.still.2012.07.016
Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils—methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395. https://doi.org/10.1016/j.soilbio.2010.05.007
Treude N, Rosencrantz D, Liesack W, Schnell S (2003) Strain FAc12, a dissimilarity iron-reducing member of the Anaeromyxobacter subgroup of Myxococcales. FEMS Microbiol Ecol 44:261–269. https://doi.org/10.1016/S0168-6496(03)00048-5
Turner S, Pryer KM, Miao VP, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338. https://doi.org/10.1111/j.1550-7408.1999.tb04612.x
Wang Y, Zhao X, Yin B, Zhen W, Guo J (2015) Biochemical defenses induced by mycorrhizae fungi Glomus mosseae in controlling strawberry Fusarium wilt. Open Biomed Eng J 9:301–304. https://doi.org/10.2174/1874120701509010301
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and amplications. Academic Press, Inc, New York, pp 315–322
Xiong W, Zhao QY, Zhao J, Xun WB, Li R, Zhang RF, Wu HS, Shen QR (2015) Different continuous cropping spans significantly affect microbial community membership and structure in a vanilla-grown soil as revealed by deep pyrosequencing. Microbiol Ecol 70:209–218. https://doi.org/10.1007/s00248-014-0516-0
Xu HJ, Wang XH, Li H, Yao HY, Su JQ, Zhu YG (2014) Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape. Environ Sci Technol 48:9391–9399. https://doi.org/10.1021/es5021058
Xu GL, Schleppi P, Li MH, Fu SL (2009) Negative responses of collembola in a forest soil (Alptal, Switzerland) under experimentally increased N deposition. Environ Pollut 157:2030–2036. https://doi.org/10.1016/j.envpol.2009.02.026
Yuan SF, Wang LL, Wu K, Shi JX, Wang MS, Yang XM, Shen QR, Shen B (2014) Evaluation of Bacillus-fortified organic fertilizer for controlling tobacco bacterial wilt in greenhouse and field experiments. Appl Soil Ecol 75:86–94. https://doi.org/10.1016/j.apsoil.2013.11.004
Zhang S, Raza W, Yang X, Hu J, Huang YC, Liu XH, Ran W, Shen QR (2008) Control of Fusarium wilt disease of cucumber plants with the application of a bioorganic fertilizer. Biol Fert Soils 44:1073–1080. https://doi.org/10.1007/s00374-008-0296-0
Zhang N, Wu K, He X, Li SQ, Zhang ZH, Shen B, Yang XM, Zhang RF, Huang QW (2011) A new bioorganic fertilizer can effectively control banana wilt by strong colonization with Bacillus subtilis N11. Plant Soil 344:87–97. https://doi.org/10.1007/s11104-011-0729-7
Zhang XX, Wang F, Li L, Li CS (2016) Main problems and development countermeasures during the strawberry production in China. Forest By-Product Speciality in China 2:92–96. https://doi.org/10.13268/j.cnki.fbsic.2016.02.038
Zhao J, Zhang R, Xue C, Xun WB, Sun L, Xu YC, Shen QR (2014) Pyrosequencing reveals contrasting soil bacterial diversity and community structure of two main winter wheat cropping systems in China. Microbial Ecol 67:443–453. https://doi.org/10.1007/s00248-013-0322-0
Zhou XG, Wu FZ (2012) Dynamics of the diversity of fungal and Fusarium communities during continuous cropping of cucumber in the greenhouse. FEMS Microbiol Ecol 80:469–478. https://doi.org/10.1111/fem.2012.80.issue-2
Acknowledgments
The authors gratefully acknowledge Professor Li Huixin from the Nanjing Agricultural University for providing molecular system (qPCR) for analyzing gene abundance. We thank Professor Yao Huaiying from Key Lab of Urban Environment and Health, Institute of Urban Environment for providing incubation system for analyzing gas kinetics.
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This research is supported by the National Natural Science Foundation of China (41501333) and General Financial Grant from the China Postdoctoral Science Foundation (2017M621666).
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Huang, Y., Xiao, X., Huang, H. et al. Contrasting beneficial and pathogenic microbial communities across consecutive cropping fields of greenhouse strawberry. Appl Microbiol Biotechnol 102, 5717–5729 (2018). https://doi.org/10.1007/s00253-018-9013-6
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DOI: https://doi.org/10.1007/s00253-018-9013-6