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Changes in bulk soil affect the disease-suppressive rhizosphere microbiome against Fusarium wilt disease |
Lin FU1,2, Wu XIONG3, Francisco DINI-ANDREOTE4,5, Beibei WANG6, Chengyuan TAO1, Yunze RUAN6, Zongzhuan SHEN1, Rong LI1(), Qirong SHEN1 |
1. Jiangsu Provincial Key Laboratory of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Education Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, China 2. School of Life Sciences, Liaoning University, Shenyang 110036, China 3. Ecology and Biodiversity Group, Department of Biology, Institute of Environmental Biology, Utrecht University, Utrecht, 3584 CH, The Netherlands 4. Department of Plant Science, The Pennsylvania State University, University Park, PA 16802, USA 5. Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA 6. Hainan Key Laboratory for Sustainable Utilization of Tropical Bio-Resources, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou 570228, China |
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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.
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Keywords
agricultural practice
bulk soil
disease suppression
rhizosphere ecology
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Corresponding Author(s):
Rong LI
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Just Accepted Date: 02 April 2020
Online First Date: 27 April 2020
Issue Date: 28 July 2020
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1 |
H Toju, K G Peay, M Yamamichi, K Narisawa, K Hiruma, K Naito, S Fukuda, M Ushio, S Nakaoka, Y Onoda, K Yoshida, K Schlaeppi, Y Bai, R Sugiura, Y Ichihashi, K Minamisawa, E T Kiers. Core microbiomes for sustainable agroecosystems. Nature Plants, 2018, 4(5): 247–257
https://doi.org/10.1038/s41477-018-0139-4
pmid: 29725101
|
2 |
J M Raaijmakers, M Mazzola. Soil immune responses. Science, 2016, 352(6292): 1392–1393
https://doi.org/10.1126/science.aaf3252
pmid: 27313024
|
3 |
P A Matson, W J Parton, A G Power, M J Swift. Agricultural intensification and ecosystem properties. Science, 1997, 277(5325): 504–509
https://doi.org/10.1126/science.277.5325.504
pmid: 20662149
|
4 |
L Fu, C R Penton, Y Z Ruan, Z Z Shen, C Xue, R Li, Q R Shen. Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biology & Biochemistry, 2017, 104: 39–48
https://doi.org/10.1016/j.soilbio.2016.10.008
|
5 |
H J Liu, W Xiong, R F Zhang, X N Hang, D S Wang, R Li, Q R Shen. 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
https://doi.org/10.1007/s11104-017-3504-6
|
6 |
E Klein, J Katan, A Gamliel. Soil suppressiveness by organic amendment to Fusarium disease in cucumber: effect on pathogen and host. Phytoparasitica, 2016, 44(2): 239–249
https://doi.org/10.1007/s12600-016-0512-7
|
7 |
L Fu, Y Ruan, C Tao, R Li, Q Shen. Continous application of bioorganic fertilizer induced resilient culturable bacteria community associated with banana Fusarium wilt suppression. Scientific Reports, 2016, 6(1): 27731
https://doi.org/10.1038/srep27731
pmid: 27306096
|
8 |
J M Raaijmakers, T C Paulitz, C Steinberg, C Alabouvette, Y Moënne-Loccoz. The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant and Soil, 2009, 321(1–2): 341–361
https://doi.org/10.1007/s11104-008-9568-6
|
9 |
G Bonanomi, V Antignani, M Capodilupo, F Scala. Identifying the characteristics of organic soil amendments that suppress soilborne plant diseases. Soil Biology & Biochemistry, 2010, 42(2): 136–144
https://doi.org/10.1016/j.soilbio.2009.10.012
|
10 |
Z Z Shen, Y Z Ruan, C Xue, J Zhang, R Li, Q R Shen. 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
https://doi.org/10.1007/s00374-015-1002-7
|
11 |
Z Z Shen, Y Z Ruan, B B Wang, S T Zhong, L X Su, R Li, Q R Shen. 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
https://doi.org/10.1016/j.apsoil.2015.04.013
|
12 |
L W Mendes, E E Kuramae, A A Navarrete, J A van Veen, S M Tsai. Taxonomical and functional microbial community selection in soybean rhizosphere. ISME Journal, 2014, 8(8): 1577–1587
https://doi.org/10.1038/ismej.2014.17
pmid: 24553468
|
13 |
D Butler. Fungus threatens top banana. Nature, 2013, 504(7479): 195–196
https://doi.org/10.1038/504195a
pmid: 24336262
|
14 |
J F Wang, A Stein, B B Gao, Y Ge. A review of spatial sampling. Spatial Statistics, 2012, 2(1): 1–14
https://doi.org/10.1016/j.spasta.2012.08.001
|
15 |
N Fierer, J A Jackson, R Vilgalys, R B Jackson. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Applied and Environmental Microbiology, 2005, 71(7): 4117–4120
https://doi.org/10.1128/AEM.71.7.4117-4120.2005
pmid: 16000830
|
16 |
D Jiménez-Fernández, M Montes-Borrego, J A Navas-Cortés, R M Jiménez-Díaz , B B Landa. 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
https://doi.org/10.1016/j.apsoil.2010.10.001
|
17 |
L Bergmark, P H B Poulsen, W A Al-Soud, A Norman, L H Hansen, S J Sørensen. 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
https://doi.org/10.1111/j.1574-6968.2012.02601.x
pmid: 22639954
|
18 |
J G Caporaso, C L Lauber, W A Walters, D Berg-Lyons, C A Lozupone, P J Turnbaugh, N Fierer, R Knight. 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
https://doi.org/10.1073/pnas.1000080107
pmid: 20534432
|
19 |
K L McGuire, S G Payne, M I Palmer, C M Gillikin, D Keefe, S J Kim, S M Gedallovich, J Discenza, R Rangamannar, J A Koshner, A L Massmann, G Orazi, A Essene, J W Leff, N Fierer. Digging the New York City Skyline: soil fungal communities in green roofs and city parks. PLoS One, 2013, 8(3): e58020
https://doi.org/10.1371/journal.pone.0058020
pmid: 23469260
|
20 |
J G Caporaso, J Kuczynski, J Stombaugh, K Bittinger, F D Bushman, E K Costello, N Fierer, A G Peña, J K Goodrich, J I Gordon, G A Huttley, S T Kelley, D Knights, J E Koenig, R E Ley, C A Lozupone, D McDonald, B D Muegge, M Pirrung, J Reeder, J R Sevinsky, P J Turnbaugh, W A Walters, J Widmann, T Yatsunenko, J Zaneveld, R Knight. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 2010, 7(5): 335–336
https://doi.org/10.1038/nmeth.f.303
pmid: 20383131
|
21 |
R C Edgar. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 2013, 10(10): 996–998
https://doi.org/10.1038/nmeth.2604
pmid: 23955772
|
22 |
Q Wang, G M Garrity, J M Tiedje, J R Cole. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 2007, 73(16): 5261–5267
https://doi.org/10.1128/AEM.00062-07
pmid: 17586664
|
23 |
U Kõljalg, R H Nilsson, K Abarenkov, L Tedersoo, A F S Taylor, M Bahram, S T Bates, T D Bruns, J Bengtsson-Palme, T M Callaghan, B Douglas, T Drenkhan, U Eberhardt, M Dueñas, T Grebenc, G W Griffith, M Hartmann, P M Kirk, P Kohout, E Larsson, B D Lindahl, R Lücking, M P Martín, P B Matheny, N H Nguyen, T Niskanen, J Oja, K G Peay, U Peintner, M Peterson, K Põldmaa, L Saag, I Saar, A Schüßler, J A Scott, C Senés, M E Smith, A Suija, D L Taylor, M T Telleria, M Weiss, K H Larsson. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology, 2013, 22(21): 5271–5277
https://doi.org/10.1111/mec.12481
pmid: 24112409
|
24 |
The R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 2018
|
25 |
P D Schloss, S L Westcott, T Ryabin, J R Hall, M Hartmann, E B Hollister, R A Lesniewski, B B Oakley, D H Parks, C J Robinson, J W Sahl, B Stres, G G Thallinger, D J Van Horn, C F Weber. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 2009, 75(23): 7537–7541
https://doi.org/10.1128/AEM.01541-09
pmid: 19801464
|
26 |
K R Clarke. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 1993, 18(1): 117–143
|
27 |
D H Parks, G W Tyson, P Hugenholtz, R G Beiko. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics, 2014, 30(21): 3123–3124
https://doi.org/10.1093/bioinformatics/btu494
pmid: 25061070
|
28 |
P Garbeva, J Postma, J A van Veen, J D van Elsas. 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
https://doi.org/10.1111/j.1462-2920.2005.00888.x
pmid: 16423012
|
29 |
J D van Elsas, M Chiurazzi, C A Mallon, D Elhottovā, V Krištůfek, J F Salles. 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
https://doi.org/10.1073/pnas.1109326109
pmid: 22232669
|
30 |
T Whitman, C Pepe-Ranney, A Enders, C Koechli, A Campbell, D H Buckley, J Lehmann. 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
https://doi.org/10.1038/ismej.2016.68
pmid: 27128990
|
31 |
A S Ridder-Duine, G A Kowalchuk, P J A K Gunnewiek, W Smant, J A van Veen, W Boer. 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
https://doi.org/10.1016/j.soilbio.2004.08.005
|
32 |
M G Bakker, J M Chaparro, D K Manter, J M Vivanco. Impacts of bulk soil microbial community structure on rhizosphere microbiomes of Zea mays. Plant and Soil, 2015, 392(1–2): 115–126
https://doi.org/10.1007/s11104-015-2446-0
|
33 |
M Hartmann, B Frey, J Mayer, P Mäder, F Widmer. Distinct soil microbial diversity under long-term organic and conventional farming. ISME Journal, 2015, 9(5): 1177–1194
https://doi.org/10.1038/ismej.2014.210
pmid: 25350160
|
34 |
W Xiong, S Guo, A Jousset, Q Y Zhao, H S Wu, R Li, G A Kowalchuk, Q R Shen. Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome. Soil Biology & Biochemistry, 2017, 114: 238–247
https://doi.org/10.1016/j.soilbio.2017.07.016
|
35 |
J M Raaijmakers, D M Weller. 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
https://doi.org/10.1128/AEM.67.6.2545-2554.2001
pmid: 11375162
|
36 |
E M M Fishal, S Meon, W M Yun. 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
https://doi.org/10.1016/S1671-2927(09)60201-7
|
37 |
F S Haack, A Poehlein, C Kröger, C A Voigt, M Piepenbring, H B Bode, R Daniel, W Schäfer, W R Streit. Molecular keys to the Janthinobacterium and Duganella spp. interaction with the plant pathogen Fusarium graminearum. Frontiers in Microbiology, 2016, 7: 1668
https://doi.org/10.3389/fmicb.2016.01668
pmid: 27833590
|
38 |
K Fujiwara, Y Iida, N Someya, M Takano, J Ohnishi, F Terami, M Shinohara. 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
https://doi.org/10.1111/jph.12504
|
39 |
M F Kreutzer, M Nett. Genomics-driven discovery of taiwachelin, a lipopeptide siderophore from Cupriavidus taiwanensis. Organic & Biomolecular Chemistry, 2012, 10(47): 9338–9343
https://doi.org/10.1039/c2ob26296g
pmid: 22972004
|
40 |
J B Neilands, S A Leong. Siderophores in relation to plant growth and disease. Annual Review of Plant Physiology, 1986, 37(1): 187–208
https://doi.org/10.1146/annurev.pp.37.060186.001155
|
41 |
Y Ou, C R Penton, S Geisen, Z Shen, Y Sun, N Lv, B Wang, Y Ruan, W Xiong, R Li, Q Shen. Deciphering underlying drivers of disease suppressiveness against pathogenic Fusarium oxysporum. Frontiers in Microbiology, 2019, 10: 2535
https://doi.org/10.3389/fmicb.2019.02535
pmid: 31781059
|
42 |
H Reichenbach. 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 |
N Rosenzweig, J M Tiedje, J F Quensen 3rd, Q Meng, J J Hao. Microbial communities associated with potato common scab-suppressive. Plant Disease, 2012, 96(5): 718–725
https://doi.org/10.1094/PDIS-07-11-0571
pmid: 30727523
|
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