in

Competition for iron drives phytopathogen control by natural rhizosphere microbiomes

  • 1.

    Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).

  • 2.

    Anderson, P. K. et al. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19, 535–544 (2004).

  • 3.

    Savary, S. et al. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 3, 430–439 (2019).

  • 4.

    Andrews, J. H. & Harris, R. F. The ecology and biogeography of microorganisms on plant surfaces. Annu. Rev. Phytopathol. 38, 145–180 (2000).

  • 5.

    Dodds, P. N. & Rathjen, J. P. Plant immunity: towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet. 11, 539–548 (2010).

  • 6.

    Mansfield, J. et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13, 614–629 (2012).

  • 7.

    Poueymiro, M. & Genin, S. Secreted proteins from Ralstonia solanacearum: a hundred tricks to kill a plant. Curr. Opin. Microbiol. 12, 44–52 (2009).

  • 8.

    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).

  • 9.

    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).

  • 10.

    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).

  • 11.

    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).

  • 12.

    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).

  • 13.

    Kwak, M. J. et al. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat. Biotechnol. 36, 1100–1109 (2018).

  • 14.

    Berendsen, R. L., Pieterse, C. M. & Bakker, P. A. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486 (2012).

  • 15.

    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).

  • 16.

    Wei, Z. et al. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat. Commun. 6, 8413 (2015).

  • 17.

    Li, M. et al. Facilitation promotes invasions in plant-associated microbial communities. Ecol. Lett. 22, 149–158 (2019).

  • 18.

    Pieterse, C. M. et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347–375 (2014).

  • 19.

    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).

  • 20.

    Casper, B. B. & Jackson, R. B. Plant competition underground. Annu. Rev. Ecol. Evol. Syst. 28, 545–570 (1997).

    • Article
    • Google Scholar
  • 21.

    Cordovez, V., Dini-Andreote, F., Carrión, V. J. & Raaijmakers, J. M. Ecology and evolution of plant microbiomes. Annu. Rev. Microbiol. 73, 69–88 (2019).

  • 22.

    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).

  • 23.

    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).

  • 24.

    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).

  • 25.

    Barber, M. F. & Elde, N. C. Buried treasure: evolutionary perspectives on microbial iron piracy. Trends Genet. 31, 627–636 (2015).

  • 26.

    Andrews, S. C., Robinson, A. K. & Rodriguez-Quinones, F. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27, 215–237 (2003).

  • 27.

    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).

  • 28.

    Miethke, M. & Marahiel, M. A. Siderophore-based iron acquisition and pathogen control. Microbiol. Mol. Biol. Rev. 71, 413–451 (2007).

  • 29.

    Hider, R. C. & Kong, X. Chemistry and biology of siderophores. Nat. Prod. Rep. 27, 637–657 (2010).

  • 30.

    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).

    • CAS
    • Google Scholar
  • 31.

    Münkemüller, T. et al. How to measure and test phylogenetic signal. Methods Ecol. Evol. 3, 743–756 (2012).

    • Article
    • Google Scholar
  • 32.

    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).

  • 33.

    Jousset, A., Schmid, B., Scheu, S. & Eisenhauer, N. Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol. Lett. 14, 537–545 (2011).

  • 34.

    Kramer, J., Özkaya, Ö. & Kümmerli, R. Bacterial siderophores in community and host interactions. Nat. Rev. Microbiol. 18, 152–163 (2019).

  • 35.

    Schofield, R. K. & Taylor, A. W. The measurement of soil pH. Soil Sci. Soc. Am. J. 19, 164–167 (1955).

  • 36.

    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).

  • 37.

    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).

  • 38.

    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).

  • 39.

    Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

  • 40.

    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).

  • 41.

    Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2018).

  • 42.

    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).

  • 43.

    Schwyn, B. & Neilands, J. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160, 47–56 (1987).

  • 44.

    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).

  • 45.

    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).

  • 46.

    Meyer, J.-M. et al. Use of siderophores to type pseudomonads: the three Pseudomonas aeruginosa pyoverdine systems. Microbiology 143, 35–43 (1997).

  • 47.

    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).

  • 48.

    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).

  • 49.

    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).

  • 50.

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

  • 51.

    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).

  • 52.

    Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).

  • 53.

    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).

    • Article
    • Google Scholar
  • 54.

    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).

    • Article
    • Google Scholar

  • Source: Ecology - nature.com

    Kerry Emanuel, David Sabatini, and Peter Shor receive BBVA Frontiers of Knowledge awards

    3 Questions: Harnessing wave power to rebuild islands