Competition for iron drives phytopathogen control by natural rhizosphere microbiomes.
DNA, Bacterial
/ genetics
Host-Pathogen Interactions
Iron
/ metabolism
Solanum lycopersicum
/ metabolism
Microbiota
Phylogeny
Plant Diseases
/ microbiology
Plant Roots
/ microbiology
RNA, Ribosomal, 16S
/ genetics
Ralstonia solanacearum
/ isolation & purification
Rhizosphere
Sequence Analysis, DNA
Siderophores
Soil
/ chemistry
Soil Microbiology
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
05
06
2019
accepted:
03
04
2020
pubmed:
13
5
2020
medline:
18
11
2020
entrez:
13
5
2020
Statut:
ppublish
Résumé
Plant pathogenic bacteria cause high crop and economic losses to human societies
Identifiants
pubmed: 32393858
doi: 10.1038/s41564-020-0719-8
pii: 10.1038/s41564-020-0719-8
pmc: PMC7116525
mid: EMS108832
doi:
Substances chimiques
DNA, Bacterial
0
RNA, Ribosomal, 16S
0
Siderophores
0
Soil
0
Iron
E1UOL152H7
Banques de données
Dryad
['10.5061/dryad.p8cz8w9mb']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1002-1010Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Swiss National Science Foundation
ID : 182499
Pays : Switzerland
Organisme : European Research Council
ID : 681295
Pays : International
Organisme : Wellcome Trust
ID : 105624
Pays : United Kingdom
Commentaires et corrections
Type : CommentIn
Références
Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).
pubmed: 22498624
doi: 10.1038/nature10947
Anderson, P. K. et al. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19, 535–544 (2004).
pubmed: 16701319
doi: 10.1016/j.tree.2004.07.021
Savary, S. et al. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 3, 430–439 (2019).
pubmed: 30718852
doi: 10.1038/s41559-018-0793-y
Andrews, J. H. & Harris, R. F. The ecology and biogeography of microorganisms on plant surfaces. Annu. Rev. Phytopathol. 38, 145–180 (2000).
pubmed: 11701840
doi: 10.1146/annurev.phyto.38.1.145
Dodds, P. N. & Rathjen, J. P. Plant immunity: towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet. 11, 539–548 (2010).
pubmed: 20585331
doi: 10.1038/nrg2812
Mansfield, J. et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13, 614–629 (2012).
pubmed: 22672649
pmcid: 6638704
doi: 10.1111/j.1364-3703.2012.00804.x
Poueymiro, M. & Genin, S. Secreted proteins from Ralstonia solanacearum: a hundred tricks to kill a plant. Curr. Opin. Microbiol. 12, 44–52 (2009).
pubmed: 19144559
doi: 10.1016/j.mib.2008.11.008
Niehus, R., Picot, A., Oliveira, N. M., Mitri, S. & Foster, K. R. The evolution of siderophore production as a competitive trait. Evolution 71, 1443–1455 (2017).
Bruce, J. B., Cooper, G. A., Chabas, H., West, S. A. & Griffin, A. S. Cheating and resistance to cheating in natural populations of the bacterium Pseudomonas fluorescens. Evolution 71, 2484–2495 (2017).
pubmed: 28833073
doi: 10.1111/evo.13328
Butaite, E., Kramer, J., Wyder, S. & Kummerli, R. Environmental determinants of pyoverdine production, exploitation and competition in natural Pseudomonas communities. Environ. Microbiol. 20, 3629–3642 (2018).
pubmed: 30003663
pmcid: 6824905
doi: 10.1111/1462-2920.14355
Smith, E. E., Sims, E. H., Spencer, D. H., Kaul, R. & Olson, M. V. Evidence for diversifying selection at the pyoverdine locus of Pseudomonas aeruginosa. J. Bacteriol. 187, 2138–2147 (2005).
pubmed: 15743962
pmcid: 1064051
doi: 10.1128/JB.187.6.2138-2147.2005
Butaite, E., Baumgartner, M., Wyder, S. & Kummerli, R. Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities. Nat. Commun. 8, 414 (2017).
pubmed: 28871205
pmcid: 5583256
doi: 10.1038/s41467-017-00509-4
Kwak, M. J. et al. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat. Biotechnol. 36, 1100–1109 (2018).
Berendsen, R. L., Pieterse, C. M. & Bakker, P. A. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486 (2012).
pubmed: 22564542
doi: 10.1016/j.tplants.2012.04.001
Compant, S., Samad, A., Faist, H. & Sessitsch, A. J. A review on the plant microbiome: ecology, functions and emerging trends in microbial application. J. Adv. Res. 19, 29–37 (2019).
Wei, Z. et al. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat. Commun. 6, 8413 (2015).
pubmed: 26400552
doi: 10.1038/ncomms9413
Li, M. et al. Facilitation promotes invasions in plant-associated microbial communities. Ecol. Lett. 22, 149–158 (2019).
pubmed: 30460736
doi: 10.1111/ele.13177
Pieterse, C. M. et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347–375 (2014).
pubmed: 24906124
doi: 10.1146/annurev-phyto-082712-102340
van der Meij, A., van Wezel, G. P., Hutchings, M. I. & Worsley, S. F. Chemical ecology of antibiotic production by actinomycetes. FEMS Microbiol. Rev. 41, 392–416 (2017).
pubmed: 28521336
doi: 10.1093/femsre/fux005
Casper, B. B. & Jackson, R. B. Plant competition underground. Annu. Rev. Ecol. Evol. Syst. 28, 545–570 (1997).
doi: 10.1146/annurev.ecolsys.28.1.545
Cordovez, V., Dini-Andreote, F., Carrión, V. J. & Raaijmakers, J. M. Ecology and evolution of plant microbiomes. Annu. Rev. Microbiol. 73, 69–88 (2019).
pubmed: 31091418
doi: 10.1146/annurev-micro-090817-062524
Cordero, O. X., Ventouras, L. A., DeLong, E. F. & Polz, M. F. Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations. Proc. Natl Acad. Sci. USA 109, 20059–20064 (2012).
pubmed: 23169633
doi: 10.1073/pnas.1213344109
pmcid: 3523850
Kummerli, R., Schiessl, K. T., Waldvogel, T., McNeill, K. & Ackermann, M. Habitat structure and the evolution of diffusible siderophores in bacteria. Ecol. Lett. 17, 1536–1544 (2014).
pubmed: 25250530
doi: 10.1111/ele.12371
Andersen, S. B., Marvig, R. L., Molin, S., Krogh Johansen, H. & Griffin, A. S. Long-term social dynamics drive loss of function in pathogenic bacteria. Proc. Natl Acad. Sci. USA 112, 10756–10761 (2015).
pubmed: 26240352
doi: 10.1073/pnas.1508324112
pmcid: 4553784
Barber, M. F. & Elde, N. C. Buried treasure: evolutionary perspectives on microbial iron piracy. Trends Genet. 31, 627–636 (2015).
pubmed: 26431675
pmcid: 4639441
doi: 10.1016/j.tig.2015.09.001
Andrews, S. C., Robinson, A. K. & Rodriguez-Quinones, F. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27, 215–237 (2003).
pubmed: 12829269
doi: 10.1016/S0168-6445(03)00055-X
Colombo, C., Palumbo, G., He, J.-Z., Pinton, R. & Cesco, S. Review on iron availability in soil: interaction of Fe minerals, plants, and microbes. J. Soils Sediments 14, 538–548 (2014).
doi: 10.1007/s11368-013-0814-z
Miethke, M. & Marahiel, M. A. Siderophore-based iron acquisition and pathogen control. Microbiol. Mol. Biol. Rev. 71, 413–451 (2007).
pubmed: 17804665
pmcid: 2168645
doi: 10.1128/MMBR.00012-07
Hider, R. C. & Kong, X. Chemistry and biology of siderophores. Nat. Prod. Rep. 27, 637–657 (2010).
pubmed: 20376388
doi: 10.1039/b906679a
Lagos, L. et al. Current overview on the study of bacteria in the rhizosphere by modern molecular techniques: a mini-review. J. Soil Sci. Plant Nutr. 15, 504–523 (2015).
Münkemüller, T. et al. How to measure and test phylogenetic signal. Methods Ecol. Evol. 3, 743–756 (2012).
doi: 10.1111/j.2041-210X.2012.00196.x
Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8, 15–25 (2010).
pubmed: 19946288
pmcid: 2879262
doi: 10.1038/nrmicro2259
Jousset, A., Schmid, B., Scheu, S. & Eisenhauer, N. Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol. Lett. 14, 537–545 (2011).
pubmed: 21435139
doi: 10.1111/j.1461-0248.2011.01613.x
Kramer, J., Özkaya, Ö. & Kümmerli, R. Bacterial siderophores in community and host interactions. Nat. Rev. Microbiol. 18, 152–163 (2019).
pubmed: 31748738
doi: 10.1038/s41579-019-0284-4
pmcid: 7116523
Schofield, R. K. & Taylor, A. W. The measurement of soil pH. Soil Sci. Soc. Am. J. 19, 164–167 (1955).
doi: 10.2136/sssaj1955.03615995001900020013x
Loper, J. E. & Henkels, M. D. Availability of iron to Pseudomonas fluorescens in rhizosphere and bulk soil evaluated with an ice nucleation reporter gene. Appl. Environ. Microbiol. 63, 99–105 (1997).
pubmed: 8979343
pmcid: 168306
doi: 10.1128/aem.63.1.99-105.1997
Heuer, H., Krsek, M., Baker, P., Smalla, K. & Wellington, E. M. Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl. Environ. Microbiol. 63, 3233–3241 (1997).
pubmed: 9251210
pmcid: 168621
doi: 10.1128/aem.63.8.3233-3241.1997
Tamura, K., Nei, M. & Kumar, S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl Acad. Sci. USA 101, 11030–11035 (2004).
pubmed: 15258291
doi: 10.1073/pnas.0404206101
pmcid: 491989
Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).
pubmed: 27004904
doi: 10.1093/molbev/msw054
pmcid: 8210823
Keck, F., Rimet, F., Bouchez, A. & Franc, A. phylosignal: an R package to measure, test, and explore phylogenetic signal. Ecol. Evol. 6, 2774–2780 (2016).
Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2018).
doi: 10.1093/bioinformatics/bty633
Höfte, M., Buysens, S., Koedam, N. & Cornelis, P. Zinc affects siderophore-mediated high affinity iron uptake systems in the rhizosphere Pseudomonas aeruginosa 7NSK2. Biometals 6, 85–91 (1993).
pubmed: 8358210
doi: 10.1007/BF00140108
Schwyn, B. & Neilands, J. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160, 47–56 (1987).
pubmed: 2952030
doi: 10.1016/0003-2697(87)90612-9
Ghysels, B. et al. The Pseudomonas aeruginosa pirA gene encodes a second receptor for ferrienterobactin and synthetic catecholate analogues. FEMS Microbiol. Lett. 246, 167–174 (2005).
pubmed: 15899402
doi: 10.1016/j.femsle.2005.04.010
Sathe, S., Mathew, A., Agnoli, K., Eberl, L. & Kümmerli, R. Genetic architecture constrains exploitation of siderophore cooperation in the bacterium Burkholderia cenocepacia. Evol. Lett. 3, 610–622 (2019).
pubmed: 31844554
pmcid: 6906993
doi: 10.1002/evl3.144
Meyer, J.-M. et al. Use of siderophores to type pseudomonads: the three Pseudomonas aeruginosa pyoverdine systems. Microbiology 143, 35–43 (1997).
pubmed: 9025276
doi: 10.1099/00221287-143-1-35
Schonfeld, J., Heuer, H., Van Elsas, J. D. & Smalla, K. Specific and sensitive detection of Ralstonia solanacearum in soil on the basis of PCR amplification of fliC fragments. Appl. Environ. Microbiol. 69, 7248–7256 (2003).
pubmed: 14660373
pmcid: 309886
doi: 10.1128/AEM.69.12.7248-7256.2003
Chen, Y. et al. A real-time PCR assay for the quantitative detection of Ralstonia solanacearum in horticultural soil and plant tissues. J. Microbiol. Biotech. 20, 193–201 (2010).
doi: 10.4014/jmb.0906.06019
Cardenas, E. 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. 76, 6778–6786 (2010).
pubmed: 20729318
pmcid: 2953039
doi: 10.1128/AEM.01097-10
Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).
pubmed: 23955772
doi: 10.1038/nmeth.2604
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).
pubmed: 21700674
pmcid: 3150044
doi: 10.1093/bioinformatics/btr381
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).
pubmed: 20383131
pmcid: 3156573
doi: 10.1038/nmeth.f.303
Wei, Z. et al. Efficacy of Bacillus-fortified organic fertiliser in controlling bacterial wilt of tomato in the field. Appl. Soil Ecol. 48, 152–159 (2011).
doi: 10.1016/j.apsoil.2011.03.013
Jeger, M. J. & Viljanen-Rollinson, S. L. H. The use of the area under the disease-progress curve (AUDPC) to assess quantitative disease resistance in crop cultivars. Theor. Appl. Genet. 102, 32–40 (2001).
doi: 10.1007/s001220051615