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Volume 160, Issue 2

and models demonstrate that root colonization is an intrinsic trait of complex bacteria Free

Abstract

complex (Bcc) bacteria possess biotechnologically useful properties that contrast with their opportunistic pathogenicity. The rhizosphere fitness of Bcc bacteria is central to their biocontrol and bioremediation activities. However, it is not known whether this differs between species or between environmental and clinical strains. We investigated the ability of 26 Bcc strains representing nine different species to colonize the roots of and (pea). Viable counts, scanning electron microscopy and bioluminescence imaging were used to assess root colonization, with Bcc bacteria achieving mean (±) levels of 2.49±0.23×10 and 5.16±1.87×10 c.f.u. per centimetre of root on the and models, respectively. The rhizocompetence model was able to reveal loss of colonization phenotypes in G4 transposon mutants that had only previously been observed in competition experiments on the model. Different Bcc species colonized each plant model at different rates, and no statistical difference in root colonization was observed between isolates of clinical or environmental origin. Loss of the virulence-associated third chromosomal replicon (>1 Mb DNA) did not alter Bcc root colonization on . In summary, Bcc bacteria possess intrinsic root colonization abilities irrespective of their species or source. As Bcc rhizocompetence does not require their third chromosomal replicon, the possibility of using synthetic biology approaches to engineer virulence-attenuated biotechnological strains is tractable.

  • Received:
  • Accepted:
  • Published Online:
Funding
This study was supported by the:
  • The Leverhulme Trust (Award F/00 407/BI)
  • Natural Environment Research Council (NERC) Environmental Genomics Thematic Programme (Award NER/T/S/2001/00299)
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2014-02-01
2024-04-20
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References

  1. Agnoli K., Schwager S., Uehlinger S., Vergunst A., Viteri D. F., Nguyen D. T., Sokol P. A., Carlier A., Eberl L. ( 2012). Exposing the third chromosome of Burkholderia cepacia complex strains as a virulence plasmid. Mol Microbiol 83:362–378 [View Article][PubMed]
     [Google Scholar]
  2. Bailey M. J., Lilley A. K., Thompson I. P., Rainey P. B., Ellis R. J. ( 1995). Site directed chromosomal marking of a fluorescent pseudomonad isolated from the phytosphere of sugar beet; stability and potential for marker gene transfer. Mol Ecol 4:755–764 [View Article][PubMed]
     [Google Scholar]
  3. Baldwin A., Mahenthiralingam E., Thickett K. M., Honeybourne D., Maiden M. C., Govan J. R., Speert D. P., Lipuma J. J., Vandamme P., Dowson C. G. ( 2005). Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex. J Clin Microbiol 43:4665–4673 [View Article][PubMed]
     [Google Scholar]
  4. Baldwin A., Mahenthiralingam E., Drevinek P., Vandamme P., Govan J. R., Waine D. J., LiPuma J. J., Chiarini L., Dalmastri C. & other authors ( 2007). Environmental Burkholderia cepacia complex isolates in human infections. Emerg Infect Dis 13:458–461 [View Article][PubMed]
     [Google Scholar]
  5. Berg G., Eberl L., Hartmann A. ( 2005). The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 7:1673–1685 [View Article][PubMed]
     [Google Scholar]
  6. Bevivino A., Tabacchioni S., Chiarini L., Carusi M. V., Del Gallo M., Visca P. ( 1994). Phenotypic comparison between rhizosphere and clinical isolates of Burkholderia cepacia . Microbiology 140:1069–1077 [View Article][PubMed]
     [Google Scholar]
  7. Chiarini L., Bevivino A., Dalmastri C., Tabacchioni S., Visca P. ( 2006). Burkholderia cepacia complex species: health hazards and biotechnological potential. Trends Microbiol 14:277–286 [View Article][PubMed]
     [Google Scholar]
  8. Coenye T., Vandamme P. ( 2003). Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5:719–729 [View Article][PubMed]
     [Google Scholar]
  9. Coenye T., Mahenthiralingam E., Henry D., LiPuma J. J., Laevens S., Gillis M., Speert D. P., Vandamme P. ( 2001). Burkholderia ambifaria sp. nov., a novel member of the Burkholderia cepacia complex including biocontrol and cystic fibrosis-related isolates. Int J Syst Evol Microbiol 51:1481–1490[PubMed] [CrossRef]
     [Google Scholar]
  10. Coenye T., Vandamme P., LiPuma J. J., Govan J. R., Mahenthiralingam E. ( 2003). Updated version of the Burkholderia cepacia complex experimental strain panel. J Clin Microbiol 41:2797–2798 [View Article][PubMed]
     [Google Scholar]
  11. Compant S., Kaplan H., Sessitsch A., Nowak J., Ait Barka E., Clément C. ( 2008a). Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol 63:84–93 [View Article][PubMed]
     [Google Scholar]
  12. Compant S., Nowak J., Coenye T., Clément C., Ait Barka E. ( 2008b). Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32:607–626 [View Article][PubMed]
     [Google Scholar]
  13. Conn V. M., Walker A. R., Franco C. M. M. ( 2008). Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana . Mol Plant Microbe Interact 21:208–218 [View Article][PubMed]
     [Google Scholar]
  14. Digonnet C., Martinez Y., Denancé N., Chasseray M., Dabos P., Ranocha P., Marco Y., Jauneau A., Goffner D. ( 2012). Deciphering the route of Ralstonia solanacearum colonization in Arabidopsis thaliana roots during a compatible interaction: focus at the plant cell wall. Planta 236:1419–1431 [View Article][PubMed]
     [Google Scholar]
  15. Dong Y. M., Iniguez A. L., Triplett E. W. ( 2003). Quantitative assessments of the host range and strain specificity of endophytic colonization by Klebsiella pneumoniae 342. Plant Soil 257:49–59 [View Article]
     [Google Scholar]
  16. Drevinek P., Baldwin A., Dowson C. G., Mahenthiralingam E. ( 2008). Diversity of the parB and repA genes of the Burkholderia cepacia complex and their utility for rapid identification of Burkholderia cenocepacia . BMC Microbiol 8:44 [View Article][PubMed]
     [Google Scholar]
  17. Hareland W. A., Crawford R. L., Chapman P. J., Dagley S. ( 1975). Metabolic function and properties of 4-hydroxyphenylacetic acid 1-hydroxylase from Pseudomonas acidovorans . J Bacteriol 121:272–285[PubMed]
     [Google Scholar]
  18. Heungens K., Parke J. L. ( 2000). Zoospore homing and infection events: effects of the biocontrol bacterium Burkholderia cepacia AMMDR1 on two oomycete pathogens of pea (Pisum sativum L.). Appl Environ Microbiol 66:5192–5200 [View Article][PubMed]
     [Google Scholar]
  19. Holden M. T. G., Seth-Smith H. M. B., Crossman L. C., Sebaihia M., Bentley S. D., Cerdeño-Tárraga A. M., Thomson N. R., Bason N., Quail M. A. & other authors ( 2009). The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol 191:261–277 [View Article][PubMed]
     [Google Scholar]
  20. Hunt T. A., Kooi C., Sokol P. A., Valvano M. A. ( 2004). Identification of Burkholderia cenocepacia genes required for bacterial survival in vivo . Infect Immun 72:4010–4022 [View Article][PubMed]
     [Google Scholar]
  21. LiPuma J. J. ( 2010). The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 23:299–323 [View Article][PubMed]
     [Google Scholar]
  22. LiPuma J. J., Spilker T., Coenye T., Gonzalez C. F. ( 2002). An epidemic Burkholderia cepacia complex strain identified in soil. Lancet 359:2002–2003 [View Article][PubMed]
     [Google Scholar]
  23. Mahenthiralingam E., Drevinek P. ( 2007). Comparative genomics of Burkholderia species. Burkholderia: Molecuar Biology and Genomics53–79 Coenye T., Vandamme P. Norwich: Horizon Scientific Press;
     [Google Scholar]
  24. Mahenthiralingam E., Coenye T., Chung J. W., Speert D. P., Govan J. R. W., Taylor P., Vandamme P. ( 2000). Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol 38:910–913[PubMed]
     [Google Scholar]
  25. Mahenthiralingam E., Urban T. A., Goldberg J. B. ( 2005). The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3:144–156 [View Article][PubMed]
     [Google Scholar]
  26. Mahenthiralingam E., Baldwin A., Dowson C. G. ( 2008). Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104:1539–1551 [View Article][PubMed]
     [Google Scholar]
  27. Mendes R., Pizzirani-Kleiner A. A., Araujo W. L., Raaijmakers J. M. ( 2007). Diversity of cultivated endophytic bacteria from sugarcane: genetic and biochemical characterization of Burkholderia cepacia complex isolates. Appl Environ Microbiol 73:7259–7267 [View Article][PubMed]
     [Google Scholar]
  28. O’Sullivan L. A., Weightman A. J., Jones T. H., Marchbank A. M., Tiedje J. M., Mahenthiralingam E. ( 2007). Identifying the genetic basis of ecologically and biotechnologically useful functions of the bacterium Burkholderia vietnamiensis . Environ Microbiol 9:1017–1034 [View Article][PubMed]
     [Google Scholar]
  29. Parke J. L., Gurian-Sherman D. ( 2001). Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu Rev Phytopathol 39:225–258 [View Article][PubMed]
     [Google Scholar]
  30. Parveen A., Smith G., Salisbury V., Nelson S. M. ( 2001). Biofilm culture of Pseudomonas aeruginosa expressing lux genes as a model to study susceptibility to antimicrobials. FEMS Microbiol Lett 199:115–118 [View Article][PubMed]
     [Google Scholar]
  31. Payne G. W., Vandamme P., Morgan S. H., Lipuma J. J., Coenye T., Weightman A. J., Jones T. H., Mahenthiralingam E. ( 2005). Development of a recA gene-based identification approach for the entire Burkholderia genus. Appl Environ Microbiol 71:3917–3927 [View Article][PubMed]
     [Google Scholar]
  32. Pirone L., Chiarini L., Dalmastri C., Bevivino A., Tabacchioni S. ( 2005). Detection of cultured and uncultured Burkholderia cepacia complex bacteria naturally occurring in the maize rhizosphere. Environ Microbiol 7:1734–1742 [View Article][PubMed]
     [Google Scholar]
  33. Ramette A., LiPuma J. J., Tiedje J. M. ( 2005). Species abundance and diversity of Burkholderia cepacia complex in the environment. Appl Environ Microbiol 71:1193–1201 [View Article][PubMed]
     [Google Scholar]
  34. Suárez-Moreno Z. R., Caballero-Mellado J., Coutinho B. G., Mendonça-Previato L., James E. K., Venturi V. ( 2012). Common features of environmental and potentially beneficial plant-associated Burkholderia . Microb Ecol 63:249–266 [View Article][PubMed]
     [Google Scholar]
  35. Theocharis A., Bordiec S., Fernandez O., Paquis S., Dhondt-Cordelier S., Baillieul F., Clément C., Barka E. A. ( 2012). Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low nonfreezing temperatures. Mol Plant Microbe Interact 25:241–249 [View Article][PubMed]
     [Google Scholar]
  36. Timmusk S., Wagner E. G. H. ( 1999). The plant-growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol Plant Microbe Interact 12:951–959 [View Article][PubMed]
     [Google Scholar]
  37. Vial L., Groleau M. C., Lamarche M. G., Filion G., Castonguay-Vanier J., Dekimpe V., Daigle F., Charette S. J., Déziel E. ( 2010). Phase variation has a role in Burkholderia ambifaria niche adaptation. ISME J 4:49–60 [View Article][PubMed]
     [Google Scholar]
  38. Vial L., Chapalain A., Groleau M.-C., Déziel E. ( 2011). The various lifestyles of the Burkholderia cepacia complex species: a tribute to adaptation. Environ Microbiol 13:1–12 [View Article][PubMed]
     [Google Scholar]
  39. Vidal-Quist J. C., Rogers H. J., Mahenthiralingam E., Berry C. ( 2013). Bacillus thuringiensis colonises plant roots in a phylogeny-dependent manner. FEMS Microbiol Ecol 86:474–489 [View Article][PubMed]
     [Google Scholar]
  40. Zhang L., Xie G. ( 2007). Diversity and distribution of Burkholderia cepacia complex in the rhizosphere of rice and maize. FEMS Microbiol Lett 266:231–235 [View Article][PubMed]
     [Google Scholar]
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Arabidopsis thaliana and Pisum sativum models demonstrate that root colonization is an intrinsic trait of Burkholderia cepacia complex bacteria
Microbiology 160, 373 (2014); https://doi.org/10.1099/mic.0.074351-0
/content/journal/micro/10.1099/mic.0.074351-0
/content/journal/micro/10.1099/mic.0.074351-0
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