Microbial Ecology

, Volume 76, Issue 3, pp 579–583 | Cite as

Plant Growth-Promoting Genes can Switch to be Virulence Factors via Horizontal Gene Transfer

  • Margarita Stritzler
  • Gabriela Soto
  • Nicolás AyubEmail author


There are increasing evidences that horizontal gene transfer (HGT) is a critical mechanism of bacterial evolution, while its complete impact remains unclear. A main constraint of HGT effects on microbial evolution seems to be the conservation of the function of the horizontally transferred genes. From this perspective, inflexible nomenclature and functionality criteria have been established for some mobile genetic elements such as pathogenic and symbiotic islands. Adhesion is a universal prerequisite for both beneficial and pathogenic plant-microbe interactions, and thus, adhesion systems (e.g., the Lap cluster) are candidates to have a dual function depending on the genomic background. In this study, we showed that the virulent factor Lap of the phytopathogen Erwinia carotovora SCRI1043, which is located within a genomic island, was acquired by HGT and probably derived from Pseudomonas. The transformation of the phytopathogen Erwinia pyrifoliae Ep1/96 with the beneficial factor Lap from the plant growth-promoting bacterium Pseudomonas fluorescens Pf-5 significantly increased its natural virulence, experimentally recapitulating the beneficial-to-virulence functional switch of the Lap cluster via HGT. To our knowledge, this is the first report of a functional switch of an individual gene or a cluster of genes mediated by HGT.


HGT Evolution Erwinia Pseudomonas Lap cluster Adhesion 


  1. 1.
    Banuelos-Vazquez LA, Torres Tejerizo G, Brom S (2017) Regulation of conjugative transfer of plasmids and integrative conjugative elements. Plasmid 91:82–89CrossRefPubMedGoogle Scholar
  2. 2.
    Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405(6784):299–304CrossRefPubMedGoogle Scholar
  3. 3.
    Harrison EM, Carter ME, Luck S, Ou HY, He X, Deng Z, O'Callaghan C, Kadioglu A, Rajakumar K (2010) Pathogenicity islands PAPI-1 and PAPI-2 contribute individually and synergistically to the virulence of Pseudomonas aeruginosa strain PA14. Infect Immun 78(4):1437–1446CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Toussaint A, Merlin C, Monchy S, Benotmane MA, Leplae R, Mergeay M, Springael D (2003) The biphenyl- and 4-chlorobiphenyl-catabolic transposon Tn4371, a member of a new family of genomic islands related to IncP and Ti plasmids. Appl Environ Microbiol 69(8):4837–4845CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Pitman AR, Jackson RW, Mansfield JW, Kaitell V, Thwaites R, Arnold DL (2005) Exposure to host resistance mechanisms drives evolution of bacterial virulence in plants. Curr Biol 15(24):2230–2235CrossRefPubMedGoogle Scholar
  6. 6.
    Ayub ND, Pettinari MJ, Mendez BS, Lopez NI (2007) The polyhydroxyalkanoate genes of a stress resistant Antarctic pseudomonas are situated within a genomic island. Plasmid 58(3):240–248CrossRefPubMedGoogle Scholar
  7. 7.
    Ayub ND, Tribelli PM, Lopez NI (2009) Polyhydroxyalkanoates are essential for maintenance of redox state in the Antarctic bacterium pseudomonas sp. 14-3 during low temperature adaptation. Extremophiles 13(1):59–66CrossRefPubMedGoogle Scholar
  8. 8.
    Setten L, Soto G, Mozzicafreddo M, Fox AR, Lisi C, Cuccioloni M, Angeletti M, Pagano E, Diaz-Paleo A, Ayub ND (2013) Engineering pseudomonas protegens Pf-5 for nitrogen fixation and its application to improve plant growth under nitrogen-deficient conditions. PLoS One 8(5):e63666CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Fox AR, Soto G, Valverde C, Russo D, Lagares Jr A, Zorreguieta A, Alleva K, Pascuan C, Frare R, Mercado-Blanco J et al (2016) Major cereal crops benefit from biological nitrogen fixation when inoculated with the nitrogen-fixing bacterium pseudomonas protegens Pf-5 X940. Environ Microbiol 18(10):3522–3534CrossRefPubMedGoogle Scholar
  10. 10.
    Iribarren MJ, Pascuan C, Soto G, Ayub ND (2015) Genetic analysis of environmental strains of the plant pathogen Phytophthora capsici reveals heterogeneous repertoire of effectors and possible effector evolution via genomic island. FEMS Microbiol Lett 362(22).
  11. 11.
    Moriconi V, Sellaro R, Ayub N, Soto G, Rugnone M, Shah R, Pathak GP, Gartner W, Casal JJ (2013) LOV-domain photoreceptor, encoded in a genomic island, attenuates the virulence of pseudomonas syringae in light-exposed Arabidopsis leaves. Plant J 76(2):322–331PubMedGoogle Scholar
  12. 12.
    Hinsa SM, Espinosa-Urgel M, Ramos JL, O'Toole GA (2003) Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas Fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol Microbiol 49(4):905–918CrossRefPubMedGoogle Scholar
  13. 13.
    Newell PD, Monds RD, O'Toole GA (2009) LapD is a bis-(3′,5′)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas Fluorescens Pf0-1. Proc Natl Acad Sci U S A 106(9):3461–3466CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Boyd CD, Smith TJ, El-Kirat-Chatel S, Newell PD, Dufrene YF, O'Toole GA (2014) Structural features of the Pseudomonas Fluorescens biofilm adhesin LapA required for LapG-dependent cleavage, biofilm formation, and cell surface localization. J Bacteriol 196(15):2775–2788CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Ayub ND, Fox AR, Garcia AN, Mozzicafreddo M, Cuccioloni M, Angeletti M, Pagano E, Soto G (2015) Pseudomonas fluorescens Pf-5 genome-wide mutant screen for resistance to the antimicrobial peptide alfalfa snakin-1. FEMS Microbiol Lett 362(2):1–6CrossRefPubMedGoogle Scholar
  16. 16.
    Perez-Mendoza D, Coulthurst SJ, Humphris S, Campbell E, Welch M, Toth IK, Salmond GP (2011) A multi-repeat adhesin of the phytopathogen, Pectobacterium atrosepticum, is secreted by a type I pathway and is subject to complex regulation involving a non-canonical diguanylate cyclase. Mol Microbiol 82(3):719–733CrossRefPubMedGoogle Scholar
  17. 17.
    Tan H, West JA, Ramsay JP, Monson RE, Griffin JL, Toth IK, Salmond GP (2014) Comprehensive overexpression analysis of cyclic-di-GMP signalling proteins in the phytopathogen Pectobacterium atrosepticum reveals diverse effects on motility and virulence phenotypes. Microbiology 160(Pt 7):1427–1439CrossRefPubMedGoogle Scholar
  18. 18.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874CrossRefPubMedGoogle Scholar
  19. 19.
    Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Campanella JJ, Bitincka L, Smalley J (2003) MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 4:29CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Perez Di Giorgio J, Soto G, Alleva K, Jozefkowicz C, Amodeo G, Muschietti JP, Ayub ND (2014) Prediction of aquaporin function by integrating evolutionary and functional analyses. J Membr Biol 247(2):107–125CrossRefPubMedGoogle Scholar
  22. 22.
    Newman AM, Cooper JB (2007) XSTREAM: a practical algorithm for identification and architecture modeling of tandem repeats in protein sequences. BMC Bioinformatics 8:382CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Monds RD, Newell PD, Gross RH, O'Toole GA (2007) Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas Fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol Microbiol 63(3):656–679CrossRefPubMedGoogle Scholar
  24. 24.
    Kube M, Migdoll AM, Gehring I, Heitmann K, Mayer Y, Kuhl H, Knaust F, Geider K, Reinhardt R (2010) Genome comparison of the epiphytic bacteria Erwinia billingiae and E. Tasmaniensis with the pear pathogen E. Pyrifoliae. BMC Genomics 11:393CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Ye C, Lan R, Xia S, Zhang J, Sun Q, Zhang S, Jing H, Wang L, Li Z, Zhou Z et al (2010) Emergence of a new multidrug-resistant serotype X variant in an epidemic clone of Shigella flexneri. J Clin Microbiol 48(2):419–426CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)CABAArgentina
  2. 2.Instituto Nacional de Tecnología Agropecuaria (INTA)CastelarArgentina

Personalised recommendations