Small changes in rhizosphere microbiome composition predict disease outcomes earlier than pathogen density variations.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
received:
18
01
2022
accepted:
06
07
2022
revised:
04
07
2022
pubmed:
23
7
2022
medline:
20
9
2022
entrez:
22
7
2022
Statut:
ppublish
Résumé
Even in homogeneous conditions, plants facing a soilborne pathogen tend to show a binary outcome with individuals either remaining fully healthy or developing severe to lethal disease symptoms. As the rhizosphere microbiome is a major determinant of plant health, we postulated that such a binary outcome may result from an early divergence in the rhizosphere microbiome assembly that may further cascade into varying disease suppression abilities. We tested this hypothesis by setting up a longitudinal study of tomato plants growing in a natural but homogenized soil infested with the soilborne bacterial pathogen Ralstonia solanacearum. Starting from an originally identical species pool, individual rhizosphere microbiome compositions rapidly diverged into multiple configurations during the plant vegetative growth. This variation in community composition was strongly associated with later disease development during the later fruiting state. Most interestingly, these patterns also significantly predicted disease outcomes 2 weeks before any difference in pathogen density became apparent between the healthy and diseased groups. In this system, a total of 135 bacterial OTUs were associated with persistent healthy plants. Five of these enriched OTUs (Lysinibacillus, Pseudarthrobacter, Bordetella, Bacillus, and Chryseobacterium) were isolated and shown to reduce disease severity by 30.4-100% when co-introduced with the pathogen. Overall, our results demonstrated that an initially homogenized soil can rapidly diverge into rhizosphere microbiomes varying in their ability to promote plant protection. This suggests that early life interventions may have significant effects on later microbiome states, and highlights an exciting opportunity for microbiome diagnostics and plant disease prevention.
Identifiants
pubmed: 35869387
doi: 10.1038/s41396-022-01290-z
pii: 10.1038/s41396-022-01290-z
pmc: PMC9478146
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
2448-2456Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 42090060
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 41922053
Informations de copyright
© 2022. The Author(s).
Références
Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, et al. The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol. 2012;13:414–30.
pubmed: 22471698
pmcid: 6638784
doi: 10.1111/j.1364-3703.2011.00783.x
Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol. 2012;13:614–29.
pubmed: 22672649
pmcid: 6638704
doi: 10.1111/j.1364-3703.2012.00804.x
Campbell CL, Noe JP. The spatial analysis of soilborne pathogens and root diseases. Annu Rev Phytopathol. 1985;23:129–48.
doi: 10.1146/annurev.py.23.090185.001021
Genin S, Denny TP. Pathogenomics of the Ralstonia solanacearum species complex. Annu Rev Phytopathol. 2012;50:67–89.
pubmed: 22559068
doi: 10.1146/annurev-phyto-081211-173000
Kwak MJ, Kong HG, Choi K, Kwon SK, Song JY, Lee J, et al. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat Biotechnol. 2018;36:1100–9.
doi: 10.1038/nbt.4232
Wei Z, Gu Y, Friman V-P, Kowalchuk GA, Xu Y, Shen Q, et al. Initial soil microbiome composition and functioning predetermine future plant health. Sci Adv. 2019;5:eaaw0759.
pubmed: 31579818
pmcid: 6760924
doi: 10.1126/sciadv.aaw0759
Lee SM, Kong HG, Song GC, Ryu CM. Disruption of Firmicutes and Actinobacteria abundance in tomato rhizosphere causes the incidence of bacterial wilt disease. ISME J 2021;15:330–47.
pubmed: 33028974
doi: 10.1038/s41396-020-00785-x
Berendsen RL, Pieterse CM, Bakker PA. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17:478–86.
pubmed: 22564542
doi: 10.1016/j.tplants.2012.04.001
Hu J, Wei Z, Kowalchuk GA, Xu Y, Shen Q, Jousset A. Rhizosphere microbiome functional diversity and pathogen invasion resistance build up during plant development. Environ Microbiol. 2020;22:5005–18.
pubmed: 32458448
doi: 10.1111/1462-2920.15097
Faust K, Lahti L, Gonze D, de Vos WM, Raes J. Metagenomics meets time series analysis: unraveling microbial community dynamics. Curr Opin Microbiol. 2015;25:56–66.
pubmed: 26005845
doi: 10.1016/j.mib.2015.04.004
Fuentes-Chust C, Parolo C, Rosati G, Rivas L, Perez-Toralla K, Simon S, et al. The microbiome meets nanotechnology: opportunities and challenges in developing new diagnostic devices. Adv Mater. 2021;33:e2006104.
pubmed: 33719117
doi: 10.1002/adma.202006104
Schlaberg R. Microbiome diagnostics. Clin Chem. 2020;66:68–76.
pubmed: 31843867
doi: 10.1373/clinchem.2019.303248
Xiao Y, Yang C, Yu L, Tian F, Wu Y, Zhao J, et al. Human gut-derived B. longum subsp. longum strains protect against aging in a D-galactose-induced aging mouse model. Microbiome. 2021;9:180.
pubmed: 34470652
pmcid: 8411540
doi: 10.1186/s40168-021-01108-8
Petrova MI, Lievens E, Malik S, Imholz N, Lebeer S. Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health. Front Physiol. 2015;6:81.
pubmed: 25859220
pmcid: 4373506
doi: 10.3389/fphys.2015.00081
Wei Z, Hu J, Gu Y, Yin S, Xu Y, Jousset A, et al. Ralstonia solanacearum pathogen disrupts bacterial rhizosphere microbiome during an invasion. Soil Biol Biochem. 2018;118:8–17.
doi: 10.1016/j.soilbio.2017.11.012
Gu S, Wei Z, Shao Z, Friman V-P, Cao K, Yang T, et al. Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat Microbiol. 2020;5:1002–10.
pubmed: 32393858
pmcid: 7116525
doi: 10.1038/s41564-020-0719-8
Wei Z, Yang T, Friman V-P, Xu Y, Shen Q, Jousset A. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat Commun. 2015;6:8413.
pubmed: 26400552
doi: 10.1038/ncomms9413
Li M, Pommier T, Yin Y, Wang J, Gu S, Jousset A, et al. Indirect reduction of Ralstonia solanacearum via pathogen helper inhibition. ISME J 2022;16:868–75.
pubmed: 34671104
doi: 10.1038/s41396-021-01126-2
Dubinkina V, Fridman Y, Pandey PP, Maslov S. Multistability and regime shifts in microbial communities explained by competition for essential nutrients. Elife 2019;8:e49720.
pubmed: 31756158
pmcid: 6874476
doi: 10.7554/eLife.49720
Coyte KZ, Schluter J, Foster KR. The ecology of the microbiome: networks, competition, and stability. Science 2015;350:663–6.
pubmed: 26542567
doi: 10.1126/science.aad2602
Garcia-Palacios P, Vandegehuchte ML, Shaw EA, Dam M, Post KH, Ramirez KS, et al. Are there links between responses of soil microbes and ecosystem functioning to elevated CO
pubmed: 25363131
doi: 10.1111/gcb.12788
Chen Y, Yan F, Chai Y, Liu H, Kolter R, Losick R, et al. Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol. 2013;15:848–64.
pubmed: 22934631
doi: 10.1111/j.1462-2920.2012.02860.x
Elphinstone J, Hennessy J, Wilson J, Stead D. Sensitivity of different methods for the detection of Ralstonia solanacearum in potato tuber extracts. EPPO Bull. 1996;26:663–78.
doi: 10.1111/j.1365-2338.1996.tb01511.x
Schonfeld J, Heuer H, van Elsas JD, Smalla K. Specific and sensitive detection of Ralstonia solanacearum in soil on the basis of PCR amplification of fliC fragments. Appl Environ Microbiol. 2003;69:7248–56.
pubmed: 14660373
pmcid: 309886
doi: 10.1128/AEM.69.12.7248-7256.2003
Wei Z, Yang X, Yin S, Shen Q, Ran W, Xu Y. Efficacy of Bacillus-fortified organic fertiliser in controlling bacterial wilt of tomato in the field. Appl Soil Ecol. 2011;48:152–9.
doi: 10.1016/j.apsoil.2011.03.013
Cardenas E, Wu WM, Leigh MB, Carley J, Carroll S, Gentry T, et al. Significant association between sulfate-reducing bacteria and uranium-reducing microbial communities as revealed by a combined massively parallel sequencing-indicator species approach. Appl Environ Microbiol. 2010;76:6778–86.
pubmed: 20729318
pmcid: 2953039
doi: 10.1128/AEM.01097-10
Gu Y, Wei Z, Wang X, Friman V-P, Huang J, Wang X, et al. Pathogen invasion indirectly changes the composition of soil microbiome via shifts in root exudation profile. Biol Fertil Soils. 2016;52:997–1005.
doi: 10.1007/s00374-016-1136-2
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.
pubmed: 23793624
pmcid: 3753973
doi: 10.1128/AEM.01043-13
Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.
pubmed: 23955772
doi: 10.1038/nmeth.2604
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011;27:2194–2200.
pubmed: 21700674
pmcid: 3150044
doi: 10.1093/bioinformatics/btr381
Edgar RC UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. BioRxiv. 2016. https://doi.org/10.1101/081257 .
Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive 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
Olsen SR, Cole CV, Watanabe FS, Dean L. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circ no. 939. Washington, DC: United States Department of Agriculture; 1954.
Heuer H, Krsek M, Baker P, Smalla K, Wellington E. Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol. 1997;63:3233–41.
pubmed: 9251210
pmcid: 168621
doi: 10.1128/aem.63.8.3233-3241.1997
R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, et al. The vegan package. Community Ecol package. 2007;10:719.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:1–18.
doi: 10.1186/gb-2011-12-6-r60
Matsumoto H, Fan X, Wang Y, Kusstatscher P, Duan J, Wu S, et al. Bacterial seed endophyte shapes disease resistance in rice. Nat Plants. 2021;7:60–72.
pubmed: 33398157
doi: 10.1038/s41477-020-00826-5
Bardgett RD, Caruso T. Soil microbial community responses to climate extremes: resistance, resilience and transitions to alternative states. Proc R Soc Lond Ser B. 2020;375:20190112.
Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JH, et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science. 2011;332:1097–100.
pubmed: 21551032
doi: 10.1126/science.1203980
Raaijmakers JM, Mazzola M. Soil immune responses. Science. 2016;352:1392–3.
pubmed: 27313024
doi: 10.1126/science.aaf3252
Gu Y, Wang X, Yang T, Friman VP, Geisen S, Wei Z, et al. Chemical structure predicts the effect of plant-derived low molecular weight compounds on soil microbiome structure and pathogen suppression. Funct Ecol. 2020;34:2158–69.
doi: 10.1111/1365-2435.13624
Burdon J, Chilvers G. Host density as a factor in plant disease ecology. Annu Rev Phytopathol. 1982;20:143–66.
doi: 10.1146/annurev.py.20.090182.001043
Rosenfeld M, Gibson RL, McNamara S, Emerson J, Burns JL, Castile R, et al. Early pulmonary infection, inflammation, and clinical outcomes in infants with cystic fibrosis. Pediatr Pulmonol. 2001;32:356–66.
pubmed: 11596160
doi: 10.1002/ppul.1144
Li J-G, Ren G-D, Jia Z-J, Dong Y-H. Composition and activity of rhizosphere microbial communities associated with healthy and diseased greenhouse tomatoes. Plant Soil. 2014;380:337–47.
doi: 10.1007/s11104-014-2097-6
Liu X, Zhang S, Jiang Q, Bai Y, Shen G, Li S, et al. Using community analysis to explore bacterial indicators for disease suppression of tobacco bacterial wilt. Sci Rep. 2016;6:36773.
pubmed: 27857159
pmcid: 5114674
doi: 10.1038/srep36773
Filion M, Hamelin RC, Bernier L, St-Arnaud M. Molecular profiling of rhizosphere microbial communities associated with healthy and diseased black spruce (Picea mariana) seedlings grown in a nursery. Appl Environ Microbiol. 2004;70:3541–51.
pubmed: 15184155
pmcid: 427751
doi: 10.1128/AEM.70.6.3541-3551.2004
Gu Y, Dong K, Geisen S, Yang W, Yan Y, Gu D, et al. The effect of microbial inoculant origin on the rhizosphere bacterial community composition and plant growth-promotion. Plant Soil. 2020;452:105–17.
doi: 10.1007/s11104-020-04545-w
Jiang G, Wang N, Zhang Y, Wang Z, Zhang Y, Yu J, et al. The relative importance of soil moisture in predicting bacterial wilt disease occurrence. Soil Ecol Lett. 2021;3:356–66.
doi: 10.1007/s42832-021-0086-2
Mendes R, Raaijmakers JM. Cross-kingdom similarities in microbiome functions. ISME J 2015;9:1905–7.
pubmed: 25647346
pmcid: 4542044
doi: 10.1038/ismej.2015.7
Dhaouadi S, Rouissi W, Mougou-Hamdane A, Nasraoui B. Evaluation of biocontrol potential of Achromobacter xylosoxidans against Fusarium wilt of melon. Eur J Plant Pathol. 2018;154:179–88.
doi: 10.1007/s10658-018-01646-2
Halet D, Defoirdt T, Van Damme P, Vervaeren H, Forrez I, Van de Wiele T, et al. Poly-beta-hydroxybutyrate-accumulating bacteria protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii. FEMS Microbiol Ecol. 2007;60:363–9.
pubmed: 17391334
doi: 10.1111/j.1574-6941.2007.00305.x
Fujiwara K, Iida Y, Someya N, Takano M, Ohnishi J, Terami F, et al. Emergence of antagonism against the pathogenic fungus Fusarium oxysporum by interplay among non-antagonistic bacteria in a hydroponics using multiple parallel mineralization. J Phytopathol. 2016;164:853–62.
doi: 10.1111/jph.12504
Garbeva P, Silby MW, Raaijmakers JM, Levy SB, de Boer W. Transcriptional and antagonistic responses of Pseudomonas fluorescens Pf0-1 to phylogenetically different bacterial competitors. ISME J. 2011;5:973–85.
pubmed: 21228890
pmcid: 3131853
doi: 10.1038/ismej.2010.196
Sato Y, Willis BL, Bourne DG. Successional changes in bacterial communities during the development of black band disease on the reef coral, Montipora hispida. ISME J. 2010;4:203–14.
pubmed: 19776765
doi: 10.1038/ismej.2009.103
Glasl B, Herndl GJ, Frade PR. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J. 2016;10:2280–92.
pubmed: 26953605
pmcid: 4989324
doi: 10.1038/ismej.2016.9
Burns AR, Stephens WZ, Stagaman K, Wong S, Rawls JF, Guillemin K, et al. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J. 2016;10:655–64.
pubmed: 26296066
doi: 10.1038/ismej.2015.142
Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM. Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem. 2013;288:4502–12.
pubmed: 23293028
pmcid: 3576057
doi: 10.1074/jbc.M112.433300
Afzal I, Shinwari ZK, Sikandar S, Shahzad S. Plant beneficial endophytic bacteria: mechanisms, diversity, host range and genetic determinants. Microbiol Res. 2019;221:36–49.
pubmed: 30825940
doi: 10.1016/j.micres.2019.02.001
Swanson JK, Montes L, Mejia L, Allen C. Detection of Latent Infections of Ralstonia solanacearum Race 3 Biovar 2 in geranium. Plant Dis. 2007;91:828–34.
pubmed: 30780392
doi: 10.1094/PDIS-91-7-0828