Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
08 2022
08 2022
Historique:
received:
26
08
2021
accepted:
11
04
2022
revised:
07
04
2022
pubmed:
25
4
2022
medline:
22
7
2022
entrez:
24
4
2022
Statut:
ppublish
Résumé
Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down control by predators, particularly protists. However, little is known regarding the impact of microbiome predators on plant health-influencing microbes and the interactive links to plant health. Here, we aimed to decipher the importance of predator-prey interactions in influencing plant health. To achieve this goal, we investigated soil and root-associated microbiomes (bacteria, fungi and protists) over nine years of banana planting under conventional and organic fertilization regimes differing in Fusarium wilt disease incidence. We found that the reduced disease incidence and improved yield associated with organic fertilization could be best explained by higher abundances of protists and pathogen-suppressive bacteria (e.g. Bacillus spp.). The pathogen-suppressive actions of predatory protists and Bacillus spp. were mainly determined by their interactions that increased the relative abundance of secondary metabolite Q genes (e.g. nonribosomal peptide synthetase gene) within the microbiome. In a subsequent microcosm assay, we tested the interactions between predatory protists and pathogen-suppressive Bacillus spp. that showed strong improvements in plant defense. Our study shows how protistan predators stimulate disease-suppressive bacteria in the plant microbiome, ultimately enhancing plant health and yield. Thus, we suggest a new biological model useful for improving sustainable agricultural practices that is based on complex interactions between different domains of life.
Identifiants
pubmed: 35461357
doi: 10.1038/s41396-022-01244-5
pii: 10.1038/s41396-022-01244-5
pmc: PMC9296445
doi:
Substances chimiques
Soil
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1932-1943Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 42090065
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 32102475
Organisme : China Postdoctoral Science Foundation
ID : 2021TQ0156
Organisme : National Natural Science Foundation of China
ID : 31972509
Organisme : National Natural Science Foundation of China
ID : 41867006
Organisme : National Natural Science Foundation of China
ID : 32102475
Organisme : China Postdoctoral Science Foundation
ID : 2021M691613
Informations de copyright
© 2022. The Author(s), under exclusive licence to International Society for Microbial Ecology.
Références
Amundson R, Berhe AA, Hopmans JW, Olson C, Sztein AE, Sparks DL. Soil and human security in the 21st century. Science. 2015;348:1261071.
pubmed: 25954014
doi: 10.1126/science.1261071
Borrelli P, Robinson DA, Fleischer LR, Lugato E, Ballabio C, Alewell C, et al. An assessment of the global impact of 21st century land use change on soil erosion. Nat Commun. 2017;8:2013.
pubmed: 29222506
pmcid: 5722879
doi: 10.1038/s41467-017-02142-7
Carvalho FP. Pesticides, environment, and food safety. Food Energy Secur. 2017;6:48–60.
doi: 10.1002/fes3.108
Santos VB, Araújo ASF, Leite LFC, Nunes LAPL, Melo WJ. Soil microbial biomass and organic matter fractions during transition from conventional to organic farming systems. Geoderma. 2012;170:227–31.
doi: 10.1016/j.geoderma.2011.11.007
Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, et al. Forecasting agriculturally driven global environmental change. Science. 2001;292:281–4.
pubmed: 11303102
doi: 10.1126/science.1057544
Tu C, Louws FJ, Creamer NG, Paul Mueller J, Brownie C, Fager K, et al. Responses of soil microbial biomass and N availability to transition strategies from conventional to organic farming systems. Agric Ecosyst Environ. 2006;113:206–15.
doi: 10.1016/j.agee.2005.09.013
Blundell R, Schmidt JE, Igwe A, Cheung AL, Vannette RL, Gaudin ACM, et al. Organic management promotes natural pest control through altered plant resistance to insects. Nat Plants. 2020;6:483–91.
pubmed: 32415295
doi: 10.1038/s41477-020-0656-9
Verbruggen E, Röling WFM, Gamper HA, Kowalchuk GA, Verhoef HA, van der Heijden MGA. Positive effects of organic farming on below-ground mutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils. N. Phytol. 2010;186:968–79.
doi: 10.1111/j.1469-8137.2010.03230.x
Lupatini M, Korthals GW, de Hollander M, Janssens TKS, Kuramae EE. Soil microbiome is more heterogeneous in organic than in conventional farming system. Front Microbiol. 2017;7:2064.
pubmed: 28101080
pmcid: 5209367
doi: 10.3389/fmicb.2016.02064
Cheng H, Zhang D, Ren L, Song Z, Li Q, Wu J, et al. Bio-activation of soil with beneficial microbes after soil fumigation reduces soil-borne pathogens and increases tomato yield. Environ Pollut. 2021;283:117160.
pubmed: 33878684
doi: 10.1016/j.envpol.2021.117160
Shahi DK, Kachhap S, Kumar A, Agarwal BK. Organic agriculture for plant disease management. In: Singh KP, Jahagirdar S, Sarma BK. (eds). Emerging Trends in Plant Pathology. 2021. Springer, Singapore, pp 643–62.
Francioli D, Schulz E, Lentendu G, Wubet T, Buscot F, Reitz T. Mineral vs organic amendments: microbial community structure, activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies. Front Microbiol. 2016;7:1446.
pubmed: 27683576
pmcid: 5022044
doi: 10.3389/fmicb.2016.01446
Sanchez-Barrios A, Sahib MR, DeBolt S. “I’ve got the magic in me”: the microbiome of conventional vs organic production systems. In: Singh DP, Singh HB, Prabha R. (eds). Plant-Microbe Interactions in Agro-Ecological Perspectives: Volume 1: Fundamental Mechanisms, Methods and Functions. 2017. Springer, Singapore, pp 85–95.
Chowdhury SP, Babin D, Sandmann M, Jacquiod S, Sommermann L, Sørensen SJ, et al. Effect of long-term organic and mineral fertilization strategies on rhizosphere microbiota assemblage and performance of lettuce. Environ Microbiol. 2019;21:2426–39.
doi: 10.1111/1462-2920.14631
Weller DM. Pseudomonas biocontrol agents of soilborne pathogens: Looking back over 30 years. Phytopathology 2007;97:250–6.
pubmed: 18944383
doi: 10.1094/PHYTO-97-2-0250
Tao C, Li R, Xiong W, Shen Z, Liu S, Wang B, et al. Bio-organic fertilizers stimulate indigenous soil Pseudomonas populations to enhance plant disease suppression. Microbiome 2020;8:137.
pubmed: 32962766
pmcid: 7510105
doi: 10.1186/s40168-020-00892-z
Mazurier S, Corberand T, Lemanceau P, Raaijmakers JM. Phenazine antibiotics produced by fluorescent Pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME J. 2009;3:977–91.
pubmed: 19369971
doi: 10.1038/ismej.2009.33
Yuan J, Zhao M, Li R, Huang Q, Rensing C, Shen Q. Lipopeptides produced by B. amyloliquefaciens NJN-6 altered the soil fungal community and non-ribosomal peptides genes harboring microbial community. Appl Soil Ecol. 2017;117–8:96–105.
doi: 10.1016/j.apsoil.2017.05.002
Kiesewalter HT, Lozano-Andrade CN, Strube ML, Kovács ÁT. Secondary metabolites of Bacillus subtilis impact the assembly of soil-derived semisynthetic bacterial communities. Beilstein J Org Chem. 2020;16:2983–98.
pubmed: 33335606
pmcid: 7722629
doi: 10.3762/bjoc.16.248
Banerjee S, Schlaeppi K, van der Heijden MGA. Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol. 2018;16:567–76.
pubmed: 29789680
doi: 10.1038/s41579-018-0024-1
Zhang Z, Han X, Yan J, Zou W, Wang E, Lu X, et al. Keystone microbiomes revealed by 14 years of field restoration of the degraded agricultural soil under distinct vegetation scenarios. Front Microbiol. 2020;11:1915.
pubmed: 33013730
pmcid: 7461875
doi: 10.3389/fmicb.2020.01915
Shang X, Cai X, Zhou Y, Han X, Zhang C-S, Ilyas N, et al. Pseudomonas inoculation stimulates endophytic Azospira population and induces systemic resistance to bacterial wilt. Front Plant Sci. 2021;12:1964.
doi: 10.3389/fpls.2021.738611
Tyc O, Song C, Dickschat JS, Vos M, Garbeva P. The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol. 2017;25:280–92.
pubmed: 28038926
doi: 10.1016/j.tim.2016.12.002
Cornforth DM, Foster KR. Competition sensing: the social side of bacterial stress responses. Nat Rev Microbiol. 2013;11:285–93.
pubmed: 23456045
doi: 10.1038/nrmicro2977
Berg G, Mahnert A, Moissl-Eichinger C. Beneficial effects of plant-associated microbes on indoor microbiomes and human health? Front Microbiol. 2014;5:15.
pubmed: 24523719
pmcid: 3905206
doi: 10.3389/fmicb.2014.00015
Straight PD, Willey JM, Kolter R. Interactions between Streptomyces coelicolor and Bacillus subtilis: Role of surfactants in raising aerial structures. J Bacteriol. 2006;188:4918–25.
pubmed: 16788200
pmcid: 1483000
doi: 10.1128/JB.00162-06
González O, Ortíz-Castro R, Díaz-Pérez C, Díaz-Pérez AL, Magaña-Dueñas V, López-Bucio J, et al. Non-ribosomal peptide synthases from Pseudomonas aeruginosa play a role in cyclodipeptide biosynthesis, quorum-sensing regulation, and root development in a plant host. Micro Ecol. 2017;73:616–29.
doi: 10.1007/s00248-016-0896-4
Zhao M, Yuan J, Zhang R, Dong M, Deng X, Zhu C, et al. Microflora that harbor the NRPS gene are responsible for Fusarium wilt disease-suppressive soil. Appl Soil Ecol. 2018;132:83–90.
doi: 10.1016/j.apsoil.2018.08.022
Caulier S, Nannan C, Gillis A, Licciardi F, Bragard C, Mahillon J. Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Front Microbiol. 2019;10:302.
pubmed: 30873135
pmcid: 6401651
doi: 10.3389/fmicb.2019.00302
Tambadou F, Lanneluc I, Sablé S, Klein GL, Doghri I, Sopéna V, et al. Novel nonribosomal peptide synthetase (NRPS) genes sequenced from intertidal mudflat bacteria. FEMS Microbiol Lett. 2014;357:123–30.
pubmed: 25039651
Prieto C. Characterization of nonribosomal peptide synthetases with NRPSsp. In: Evans BS. (ed). Nonribosomal Peptide and Polyketide Biosynthesis: Methods and Protocols. 2016. Springer, New York, NY, pp 273–8.
Yuan J, Ruan Y, Wang B, Zhang J, Waseem R, Huang Q, et al. Plant growth-promoting rhizobacteria strain Bacillus amyloliquefaciens NJN-6-enriched bio-organic fertilizer suppressed Fusarium wilt and promoted the growth of banana plants. J Agric Food Chem. 2013;61:3774–80.
pubmed: 23541032
doi: 10.1021/jf400038z
Yuan J, Li B, Zhang N, Waseem R, Shen Q, Huang Q. Production of bacillomycin- and macrolactin-type antibiotics by Bacillus amyloliquefaciens NJN-6 for suppressing soilborne plant pathogens. J Agric Food Chem. 2012;60:2976–81.
pubmed: 22385216
doi: 10.1021/jf204868z
Xiong W, Song Y, Yang K, Gu Y, Wei Z, Kowalchuk GA, et al. Rhizosphere protists are key determinants of plant health. Microbiome. 2020;8:27.
pubmed: 32127034
pmcid: 7055055
doi: 10.1186/s40168-020-00799-9
Thakur MP, Geisen S. Trophic regulations of the soil microbiome. Trends Microbiol. 2019;27:771–80.
pubmed: 31138481
doi: 10.1016/j.tim.2019.04.008
Müller MS, Scheu S, Jousset A. Protozoa drive the dynamics of culturable biocontrol bacterial communities. PLOS ONE. 2013;8:e66200.
pubmed: 23840423
pmcid: 3694078
doi: 10.1371/journal.pone.0066200
Geisen S, Mitchell EAD, Adl S, Bonkowski M, Dunthorn M, Ekelund F, et al. Soil protists: A fertile frontier in soil biology research. FEMS Microbiol Rev. 2018;42:293–323.
pubmed: 29447350
doi: 10.1093/femsre/fuy006
Gao Z, Karlsson I, Geisen S, Kowalchuk G, Jousset A. Protists: puppet masters of the rhizosphere microbiome. Trends Plant Sci. 2019;24:165–76.
pubmed: 30446306
doi: 10.1016/j.tplants.2018.10.011
Jousset A, Lara E, Wall LG, Valverde C. Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing. Appl Environ Microbiol. 2006;72:7083–90.
pubmed: 17088380
pmcid: 1636139
doi: 10.1128/AEM.00557-06
Liu H, Xiong W, Zhang R, Hang X, Wang D, Li R, et al. Continuous application of different organic additives can suppress tomato disease by inducing the healthy rhizospheric microbiota through alterations to the bulk soil microflora. Plant Soil. 2018;423:229–40.
doi: 10.1007/s11104-017-3504-6
Chen D, Wang X, Zhang W, Zhou Z, Ding C, Liao Y, et al. Persistent organic fertilization reinforces soil-borne disease suppressiveness of rhizosphere bacterial community. Plant Soil. 2020;452:313–28.
doi: 10.1007/s11104-020-04576-3
Müller JP, Hauzy C, Hulot FD. Ingredients for protist coexistence: Competition, endosymbiosis and a pinch of biochemical interactions. J Anim Ecol. 2012;81:222–32.
pubmed: 21831194
doi: 10.1111/j.1365-2656.2011.01894.x
Guo S, Xiong W, Hang X, Gao Z, Jiao Z, Liu H, et al. Protists as main indicators and determinants of plant performance. Microbiome. 2021;9:64.
pubmed: 33743825
pmcid: 7981826
doi: 10.1186/s40168-021-01025-w
Ren F, Sun N, Xu M, Zhang X, Wu L, Xu M. Changes in soil microbial biomass with manure application in cropping systems: a meta-analysis. Soil Tillage Res. 2019;194:104291.
doi: 10.1016/j.still.2019.06.008
Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17:478–86.
pubmed: 22564542
doi: 10.1016/j.tplants.2012.04.001
Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y. The rhizosphere: A playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil. 2009;321:341–61.
doi: 10.1007/s11104-008-9568-6
Compant S, Cambon MC, Vacher C, Mitter B, Samad A, Sessitsch A. The plant endosphere world – bacterial life within plants. Environ Microbiol. 2021;23:1812–29.
pubmed: 32955144
doi: 10.1111/1462-2920.15240
Oliverio AM, Geisen S, Delgado-Baquerizo M, Maestre FT, Turner BL, Fierer N. The global-scale distributions of soil protists and their contributions to belowground systems. Sci Adv. 2020;6:eaax8787.
pubmed: 32042898
pmcid: 6981079
doi: 10.1126/sciadv.aax8787
Dumack K, Fiore-Donno AM, Bass D, Bonkowski M. Making sense of environmental sequencing data: ecologically important functional traits of the protistan groups Cercozoa and Endomyxa (Rhizaria). Mol Ecol Resour. 2020;20:398–403.
pubmed: 31677344
doi: 10.1111/1755-0998.13112
Romdhane S, Spor A, Banerjee S, Breuil M-C, Bru D, Chabbi A, et al. Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity. Environ Microbiome. 2022;17:1.
pubmed: 34991714
pmcid: 8740439
doi: 10.1186/s40793-021-00396-9
Jousset A, Rochat L, Péchy-Tarr M, Keel C, Scheu S, Bonkowski M. Predators promote defence of rhizosphere bacterial populations by selective feeding on non-toxic cheaters. ISME J. 2009;3:666–74.
pubmed: 19322247
doi: 10.1038/ismej.2009.26
Yu GY, Sinclair JB, Hartman GL, Bertagnolli BL. Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol Biochem. 2002;34:955–63.
doi: 10.1016/S0038-0717(02)00027-5
Romero D, de Vicente A, Rakotoaly RH, Dufour SE, Veening J-W, Arrebola E, et al. The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant Microbe Interact. 2007;20:430–40.
pubmed: 17427813
doi: 10.1094/MPMI-20-4-0430
Xu Z, Mandic-Mulec I, Zhang H, Liu Y, Sun X, Feng H, et al. Antibiotic bacillomycin D affects iron acquisition and biofilm formation in Bacillus velezensis through a Btr-mediated FeuABC-dependent pathway. Cell Rep. 2019;29:1192–1202.e5.
pubmed: 31665633
doi: 10.1016/j.celrep.2019.09.061
Huang J, Wei Z, Tan S, Mei X, Shen Q, Xu Y. Suppression of bacterial wilt of tomato by bioorganic fertilizer made from the antibacterial compound producing strain Bacillus amyloliquefaciens HR62. J Agric Food Chem. 2014;62:10708–16.
pubmed: 25322261
doi: 10.1021/jf503136a
Wang B, Shen Z, Zhang F, Raza W, Yuan J, Huang R, et al. Bacillus amyloliquefaciens strain W19 can promote growth and yield and suppress Fusarium wilt in banana under greenhouse and field conditions. Pedosphere. 2016;26:733–44.
doi: 10.1016/S1002-0160(15)60083-2
Shen Z, Ruan Y, Chao X, Zhang J, Li R, Shen Q. Rhizosphere microbial community manipulated by 2 years of consecutive biofertilizer application associated with banana Fusarium wilt disease suppression. Biol Fertil Soils. 2015;51:553–62.
doi: 10.1007/s00374-015-1002-7
Jeger MJ, Eden-Green S, Thresh JM, Johanson A, Waller JM, Brown AE. Banana diseases. In: Gowen S. (ed). Bananas and Plantains. 1995. Springer Netherlands, Dordrecht, pp 317–81.
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci. 2015;112:E911–20.
pubmed: 25605935
pmcid: 4345613
doi: 10.1073/pnas.1414592112
Fierer N, Jackson JA, Vilgalys R, Jackson RB. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol. 2005;71:4117–20.
pubmed: 16000830
pmcid: 1169028
doi: 10.1128/AEM.71.7.4117-4120.2005
Jiménez-Fernández D, Montes-Borrego M, Navas-Cortés JA, Jiménez-Díaz RM, Landa BB. Identification and quantification of Fusarium oxysporum in planta and soil by means of an improved specific and quantitative PCR assay. Appl Soil Ecol. 2010;46:372–82.
doi: 10.1016/j.apsoil.2010.10.001
Mori K, Iriye R, Hirata M, Takamizawa K. Quantification of Bacillus species in a wastewater treatment system by the molecular analyses. Biotechnol Bioprocess Eng. 2004;9:482–9.
doi: 10.1007/BF02933490
Ayuso-Sacido A, Genilloud O. New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Micro Ecol. 2005;49:10–24.
doi: 10.1007/s00248-004-0249-6
Fu L, Penton CR, Ruan Y, Shen Z, Xue C, Li R, et al. Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biol Biochem. 2017;104:39–48.
doi: 10.1016/j.soilbio.2016.10.008
Claesson MJ, O’Sullivan O, Wang Q, Nikkilä J, Marchesi JR, Smidt H, et al. Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLOS ONE. 2009;4:e6669.
pubmed: 19693277
pmcid: 2725325
doi: 10.1371/journal.pone.0006669
White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ. (eds). PCR Protocols. 1990. Academic Press, San Diego, pp 315–22.
Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2:113–8.
pubmed: 8180733
doi: 10.1111/j.1365-294X.1993.tb00005.x
Bass D, Silberman JD, Brown MW, Pearce RA, Tice AK, Jousset A, et al. Coprophilic amoebae and flagellates, including Guttulinopsis, Rosculus and Helkesimastix, characterise a divergent and diverse rhizarian radiation and contribute to a large diversity of faecal-associated protists. Environ Microbiol. 2016;18:1604–19.
pubmed: 26914587
doi: 10.1111/1462-2920.13235
Geisen S, Vaulot D, Mahé F, Lara E, Vargas C de, Bass D. A user guide to environmental protistology: primers, metabarcoding, sequencing, and analyses. BioRxiv 2019;850610:1–34.
Xiong W, Jousset A, Li R, Delgado-Baquerizo M, Bahram M, Logares R, et al. A global overview of the trophic structure within microbiomes across ecosystems. Environ Int. 2021;151:106438.
pubmed: 33621916
doi: 10.1016/j.envint.2021.106438
Xiong W, Li R, Ren Y, Liu C, Zhao Q, Wu H, et al. Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biol Biochem. 2017;107:198–207.
doi: 10.1016/j.soilbio.2017.01.010
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–200.
pubmed: 21700674
pmcid: 3150044
doi: 10.1093/bioinformatics/btr381
Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.
pubmed: 17586664
pmcid: 1950982
doi: 10.1128/AEM.00062-07
Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al. The Protist Ribosomal Reference database (PR2): A catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2013;41:D597–D604.
pubmed: 23193267
doi: 10.1093/nar/gks1160
Xiong W, Li R, Guo S, Karlsson I, Jiao Z, Xun W, et al. Microbial amendments alter protist communities within the soil microbiome. Soil Biol Biochem. 2019;135:379–82.
doi: 10.1016/j.soilbio.2019.05.025
Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, et al. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 2016;44:D286–93.
pubmed: 26582926
doi: 10.1093/nar/gkv1248
Revelle W, Revelle MW. Package ‘psych’. Compr R Arch Netw. 2015;337:338.
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995;57:289–300.
Bargabus RL, Zidack NK, Sherwood JE, Jacobsen BJ. Characterisation of systemic resistance in sugar beet elicited by a non-pathogenic, phyllosphere-colonizing Bacillus mycoides, biological control agent. Physiol Mol Plant Pathol. 2002;61:289–98.
doi: 10.1006/pmpp.2003.0443
Bais HP, Fall R, Vivanco JM. Biocontrol of Bacillus subtilis against infection of arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol. 2004;134:307–19.
pubmed: 14684838
pmcid: 316310
doi: 10.1104/pp.103.028712
Cazorla FM, Romero D, Pérez-García A, Lugtenberg BJJ, Vicente Ade, Bloemberg G. Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. J Appl Microbiol. 2007;103:1950–9.
pubmed: 17953605
doi: 10.1111/j.1365-2672.2007.03433.x
Aneja KR. Experiments in microbiology, plant pathology and biotechnology. 2007. New Age International, New Delhi.
Mela F, Fritsche K, de Boer W, van Veen JA, de Graaff LH, van den Berg M, et al. Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger. ISME J. 2011;5:1494–504.
pubmed: 21614084
pmcid: 3160687
doi: 10.1038/ismej.2011.29
Gao Z. Soil protists: From traits to ecological functions. 2020. Utrecht University.
Anderson MJ. Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef: Statistics Reference Online. 2017. American Cancer Society, pp 1–15.
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, et al. Package ‘vegan’. Community Ecol Package Version. 2013;2:1–295.
Breiman L. Random forests. Mach Learn. 2001;45:5–32.
doi: 10.1023/A:1010933404324
Liaw A, Wiener M. Classification and regression by randomForest. R N. 2002;23:18–22.
Archer E. rfPermute: Estimate permutation p-values for random forest importance metrics. R Package Version 20 2016.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.
pubmed: 21702898
pmcid: 3218848
doi: 10.1186/gb-2011-12-6-r60
Oguntunde PG, Fosu M, Ajayi AE, van de Giesen N. Effects of charcoal production on maize yield, chemical properties and texture of soil. Biol Fertil Soils. 2004;39:295–9.
doi: 10.1007/s00374-003-0707-1
Mcdonald JH. Handbook of biological statistics. 2009. Baltimore: sparky house publishing, Baltimore.