Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis

PLoS One. 2014 Jan 8;9(1):e83779. doi: 10.1371/journal.pone.0083779. eCollection 2014.

Abstract

Burkholderia is a diverse and dynamic genus, containing pathogenic species as well as species that form complex interactions with plants. Pathogenic strains, such as B. pseudomallei and B. mallei, can cause serious disease in mammals, while other Burkholderia strains are opportunistic pathogens, infecting humans or animals with a compromised immune system. Although some of the opportunistic Burkholderia pathogens are known to promote plant growth and even fix nitrogen, the risk of infection to infants, the elderly, and people who are immunocompromised has not only resulted in a restriction on their use, but has also limited the application of non-pathogenic, symbiotic species, several of which nodulate legume roots or have positive effects on plant growth. However, recent phylogenetic analyses have demonstrated that Burkholderia species separate into distinct lineages, suggesting the possibility for safe use of certain symbiotic species in agricultural contexts. A number of environmental strains that promote plant growth or degrade xenobiotics are also included in the symbiotic lineage. Many of these species have the potential to enhance agriculture in areas where fertilizers are not readily available and may serve in the future as inocula for crops growing in soils impacted by climate change. Here we address the pathogenic potential of several of the symbiotic Burkholderia strains using bioinformatics and functional tests. A series of infection experiments using Caenorhabditis elegans and HeLa cells, as well as genomic characterization of pathogenic loci, show that the risk of opportunistic infection by symbiotic strains such as B. tuberum is extremely low.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Bacterial Secretion Systems / genetics
  • Burkholderia / genetics
  • Burkholderia / pathogenicity
  • Burkholderia / physiology*
  • Burkholderia Infections / microbiology*
  • Caenorhabditis elegans / microbiology
  • Drug Resistance, Microbial / genetics
  • Flagella / genetics
  • Genes, Bacterial / genetics
  • Genetic Loci
  • HeLa Cells
  • Humans
  • Mammals / microbiology*
  • Multigene Family
  • Phylogeny
  • Plants / microbiology*
  • Symbiosis* / genetics
  • Virulence / genetics

Substances

  • Bacterial Secretion Systems

Grants and funding

This research was supported in part by a grant (IOB-0537497) from the National Science Foundation (USA) to GW and AMH and a Shanbrom Family Foundation grant to AMH. A University of California Office of The President, President's Postdoctoral Fellowship, supported AAA. CMA was supported by the L'Oréal USA For Women in Science Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.