Changes in bulk soil affect the disease-suppressive rhizosphere microbiome against Fusarium wilt disease

Abstract

Harnessing disease-suppressive microbiomes constitutes a promising strategy for optimizing plant growth. However, relatively little information is available about the relationship between bulk and rhizosphere soil microbiomes. Here, the assembly of banana bulk soil and rhizosphere microbiomes was investigated in a monoculture system consisting of bio-organic (BIO) and organic management practices. Applying BIO practice in newly reclaimed fields resulted in a high-efficiency biocontrol rate, thus providing a promising strategy for pre-control of Fusarium wilt disease. The soil microbiota was further characterized by MiSeq sequencing and quantitative PCR. The results indicate that disease suppression was mediated by the structure of a suppressive rhizosphere microbiome with respect to distinct community composition, diversity and abundance. Overall microbiome suppressiveness was primarily related to a particular set of enriched bacterial taxa affiliated with Pseudomonas, Terrimonas, Cupriavidus, Gp6, Ohtaekwangia and Duganella. Finally, structural equation modeling was used to show that the changes in bulk soil bacterial community determined its induced rhizosphere bacterial community, which serves as an important and direct factor in restraining the pathogen. Collectively, this study provides an integrative approach to disentangle the biological basis of disease-suppressive microbiomes in the context of agricultural practice and soil management.

Keywords

agricultural practice / bulk soil / disease suppression / rhizosphere ecology

References

[1] Toju H, Peay K G, Yamamichi M, Narisawa K, Hiruma K, Naito K, Fukuda S, Ushio M, Nakaoka S, Onoda Y, Yoshida K, Schlaeppi K, Bai Y, Sugiura R, Ichihashi Y, Minamisawa K, Kiers E T. Core microbiomes for sustainable agroecosystems. Nature Plants, 2018, 4(5): 247–257

[2] Raaijmakers J M, Mazzola M. Soil immune responses. Science, 2016, 352(6292): 1392–1393

[3] Matson P A, Parton W J, Power A G, Swift M J. Agricultural intensification and ecosystem properties. Science, 1997, 277(5325): 504–509

[4] Fu L, Penton C R, Ruan Y Z, Shen Z Z, Xue C, Li R, Shen Q R. Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biology & Biochemistry, 2017, 104: 39–48

[5] Liu H J, Xiong W, Zhang R F, Hang X N, Wang D S, Li R, Shen Q R. Continuous application of different organic additives can suppress tomato disease by inducing the healthy rhizospheric microbiota through alterations to the bulk soil microflora. Plant and Soil, 2018, 423(1–2): 229–240

[6] Klein E, Katan J, Gamliel A. Soil suppressiveness by organic amendment to Fusarium disease in cucumber: effect on pathogen and host. Phytoparasitica, 2016, 44(2): 239–249

[7] Fu L, Ruan Y, Tao C, Li R, Shen Q. Continous application of bioorganic fertilizer induced resilient culturable bacteria community associated with banana Fusarium wilt suppression. Scientific Reports, 2016, 6(1): 27731

[8] Raaijmakers J M, Paulitz T C, Steinberg C, Alabouvette C, Moënne-Loccoz Y. The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant and Soil, 2009, 321(1–2): 341–361

[9] Bonanomi G, Antignani V, Capodilupo M, Scala F. Identifying the characteristics of organic soil amendments that suppress soilborne plant diseases. Soil Biology & Biochemistry, 2010, 42(2): 136–144

[10] Shen Z Z, Ruan Y Z, Xue C, Zhang J, Li R, Shen Q R. Rhizosphere microbial community manipulated by 2 years of consecutive biofertilizer application associated with banana Fusarium wilt disease suppression. Biology and Fertility of Soils, 2015, 51(5): 553–562

[11] Shen Z Z, Ruan Y Z, Wang B B, Zhong S T, Su L X, Li R, Shen Q R. Effect of biofertilizer for suppressing Fusarium wilt disease of banana as well as enhancing microbial and chemical properties of soil under greenhouse trial. Applied Soil Ecology, 2015, 93: 111–119

[12] Mendes L W, Kuramae E E, Navarrete A A, van Veen J A, Tsai S M. Taxonomical and functional microbial community selection in soybean rhizosphere. ISME Journal, 2014, 8(8): 1577–1587

[13] Butler D. Fungus threatens top banana. Nature, 2013, 504(7479): 195–196

[14] Wang J F, Stein A, Gao B B, Ge Y. A review of spatial sampling. Spatial Statistics, 2012, 2(1): 1–14

[15] Fierer N, Jackson J A, Vilgalys R, Jackson R B. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Applied and Environmental Microbiology, 2005, 71(7): 4117–4120

[16] Jiménez-Fernández D, Montes-Borrego M, Navas-Cortés J A, Jiménez-Díaz R M, Landa B B. Identification and quantification of Fusarium oxysporum in planta and soil by means of an improved specific and quantitative PCR assay. Applied Soil Ecology, 2010, 46(3): 372–382

[17] Bergmark L, Poulsen P H B, Al-Soud W A, Norman A, Hansen L H, Sørensen S J. Assessment of the specificity of Burkholderia and Pseudomonas qPCR assays for detection of these genera in soil using 454 pyrosequencing. FEMS Microbiology Letters, 2012, 333(1): 77–84

[18] Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Lozupone C A, Turnbaugh P J, Fierer N, Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(Suppl 1): 4516–4522

[19] McGuire K L, Payne S G, Palmer M I, Gillikin C M, Keefe D, Kim S J, Gedallovich S M, Discenza J, Rangamannar R, Koshner J A, Massmann A L, Orazi G, Essene A, Leff J W, Fierer N. Digging the New York City Skyline: soil fungal communities in green roofs and city parks. PLoS One, 2013, 8(3): e58020

[20] Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, Fierer N, Peña A G, Goodrich J K, Gordon J I, Huttley G A, Kelley S T, Knights D, Koenig J E, Ley R E, Lozupone C A, McDonald D, Muegge B D, Pirrung M, Reeder J, Sevinsky J R, Turnbaugh P J, Walters W A, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 2010, 7(5): 335–336

[21] Edgar R C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 2013, 10(10): 996–998

[22] Wang Q, Garrity G M, Tiedje J M, Cole J R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 2007, 73(16): 5261–5267

[23] Kõljalg U, Nilsson R H, Abarenkov K, Tedersoo L, Taylor A F S, Bahram M, Bates S T, Bruns T D, Bengtsson-Palme J, Callaghan T M, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith G W, Hartmann M, Kirk P M, Kohout P, Larsson E, Lindahl B D, Lücking R, Martín M P, Matheny P B, Nguyen N H, Niskanen T, Oja J, Peay K G, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott J A, Senés C, Smith M E, Suija A, Taylor D L, Telleria M T, Weiss M, Larsson K H. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology, 2013, 22(21): 5271–5277

[24] The R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 2018

[25] Schloss P D, Westcott S L, Ryabin T, Hall J R, Hartmann M, Hollister E B, Lesniewski R A, Oakley B B, Parks D H, Robinson C J, Sahl J W, Stres B, Thallinger G G, Van Horn D J, Weber C F. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 2009, 75(23): 7537–7541

[26] Clarke K R. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 1993, 18(1): 117–143

[27] Parks D H, Tyson G W, Hugenholtz P, Beiko R G. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics, 2014, 30(21): 3123–3124

[28] Garbeva P, Postma J, van Veen J A, van Elsas J D. Effect of above-ground plant species on soil microbial community structure and its impact on suppression of Rhizoctonia solani AG3. Environmental Microbiology, 2006, 8(2): 233–246

[29] van Elsas J D, Chiurazzi M, Mallon C A, Elhottovā D, Krištůfek V, Salles J F. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(4): 1159–1164

[30] Whitman T, Pepe-Ranney C, Enders A, Koechli C, Campbell A, Buckley D H, Lehmann J. Dynamics of microbial community composition and soil organic carbon mineralization in soil following addition of pyrogenic and fresh organic matter. ISME Journal, 2016, 10(12): 2918–2930

[31] Ridder-Duine A S, Kowalchuk G A, Gunnewiek P J A K, Smant W, van Veen J A, Boer W. Rhizosphere bacterial community composition in natural stands of Carex arenaria (sand sedge) is determined by bulk soil community composition. Soil Biology & Biochemistry, 2005, 37(2): 349–357

[32] Bakker M G, Chaparro J M, Manter D K, Vivanco J M. Impacts of bulk soil microbial community structure on rhizosphere microbiomes of Zea mays. Plant and Soil, 2015, 392(1–2): 115–126

[33] Hartmann M, Frey B, Mayer J, Mäder P, Widmer F. Distinct soil microbial diversity under long-term organic and conventional farming. ISME Journal, 2015, 9(5): 1177–1194

[34] Xiong W, Guo S, Jousset A, Zhao Q Y, Wu H S, Li R, Kowalchuk G A, Shen Q R. Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome. Soil Biology & Biochemistry, 2017, 114: 238–247

[35] Raaijmakers J M, Weller D M. Exploiting genotypic diversity of 2,4-diacetylphloroglucinol-producing Pseudomonas spp.: characterization of superior root-colonizing P. fluorescens strain Q8r1-96. Applied and Environmental Microbiology, 2001, 67(6): 2545–2554

[36] Fishal E M M, Meon S, Yun W M. Induction of tolerance to Fusarium Wilt and defense-related mechanisms in the plantlets of susceptible berangan banana pre-inoculated with Pseudomonas sp. (UPMP3) and Burkholderia sp. (UPMB3). Agricultural Sciences in China, 2010, 9(8): 1140–1149

[37] Haack F S, Poehlein A, Kröger C, Voigt C A, Piepenbring M, Bode H B, Daniel R, Schäfer W, Streit W R. Molecular keys to the Janthinobacterium and Duganella spp. interaction with the plant pathogen Fusarium graminearum. Frontiers in Microbiology, 2016, 7: 1668

[38] Fujiwara K, Iida Y, Someya N, Takano M, Ohnishi J, Terami F, Shinohara M. Emergence of antagonism against the pathogenic fungus Fusarium oxysporum by interplay among non-antagonistic bacteria in a hydroponics using multiple parallel mineralization. Journal of Phytopathology, 2016, 164(11–12): 853–862

[39] Kreutzer M F, Nett M. Genomics-driven discovery of taiwachelin, a lipopeptide siderophore from Cupriavidus taiwanensis. Organic & Biomolecular Chemistry, 2012, 10(47): 9338–9343

[40] Neilands J B, Leong S A. Siderophores in relation to plant growth and disease. Annual Review of Plant Physiology, 1986, 37(1): 187–208

[41] Ou Y, Penton C R, Geisen S, Shen Z, Sun Y, Lv N, Wang B, Ruan Y, Xiong W, Li R, Shen Q. Deciphering underlying drivers of disease suppressiveness against pathogenic Fusarium oxysporum. Frontiers in Microbiology, 2019, 10: 2535

[42] Reichenbach H. The order cytophagales. In: Balows A, Trüper H G, Dworkin M, Harder W, Schleifer K, eds. The prokaryotes. New York: Springer, 2006, 549–590

[43] Rosenzweig N, Tiedje J M, Quensen J F 3rd, Meng Q, Hao J J. Microbial communities associated with potato common scab-suppressive. Plant Disease, 2012, 96(5): 718–725

Supplementary materials

The online version of this article at https://doi.org/10.15302/J-FASE-2020328 contains supplementary materials (Figs. S1–S4; Tables S1–S3).

Acknowledgements

This research was funded by the National Key Research and Development Program (2017YFD0202101), the National Natural Science Foundation of China (31672239 and 31972509), the 111 project (B12009), the Priority Academic Program Development of the Jiangsu Higher Education Institutions (PAPD), and the Innovative Research Team Development Plan of the Ministry of Education of China (IRT_17R56).

Compliance with ethics guidelines

Lin Fu, Wu Xiong, Francisco Dini-Andreote, Beibei Wang, Chengyuan Tao, Yunze Ruan, Zongzhuan Shen, Rong Li, and Qirong Shen declare that they have no conflicts of interest or financial conflicts to disclose.

This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2020. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)