Virulence from the rhizosphere: ecology and evolution of Burkholderia pseudomallei-complex species

Burkholderia pseudomallei ( Bp ) is an environmental organism that inhabits the rhizosphere, a rich and diverse zone of soil supported by a network of plant roots. In the rhizosphere, Bp faces intense competition with other bacterial species and fungi, as well as predation by protozoa, nematodes, and insects. Our hypothesis is that Bp virulence determinants that promote disease in mammals arose to defend against environmental predators. In this context, infections of humans and animals are likely to be incidental occurrences. We speculate that most Bp virulence determinants that are critical for intracellular survival could have relevant roles for interactions with ecological species, including the Bsa type III secretion system (T3SS Bsa ), BimA-mediated actin polymerization and type VI secretion (T6SS-5) in promoting intracellular survival and cell-cell spread in nematodes, grazing insects and social amoebae. Bp possesses two more T3SSs and numerous polyketide/non-ribosomal peptide synthetases (PKS/NRPS) that resemble systems in phytopathogenic bacteria, hinting at its ability to interact with plants or fungi. Bp is capable of adopting a lifestyle of obligate parasitism, as shown by the divergence of the equine host-restricted B. mallei . Some environmental species that prey on Bp may double as host organisms, and although not proven, it is conceivable that Bp may use them as a survival niche. Understanding the lifestyle of Bp in an ecological context will shed light on the mechanisms that promote human infections, and may potentially help explain the broad differentials in virulence and the genetic diversity that is a hallmark of the species. • The Burkholderia pseudomallei ( Bp ) complex includes pathogenic and non-pathogenic species. • With the exception of Burkholderia mallei , which is adapted to survival in equine hosts , Bp- complex species are environmental microbes. • Virulence traits include type III and type VI secretion systems (T3SS Bsa , T6SS-5), and actin-based motility. • We hypothesize that ecological interactions with eukaryotic predators provide selection for virulence traits that promote human infections. • Understanding the ecology of the Bp complex should provide insight into the origin of virulence mechanisms in these and other pathogens. Burkholderia pseudomallei ( Bp ) and Burkholderia mallei ( Bm ) cause the often-lethal infectious diseases melioidosis and glanders, respectively. Curiously, closely related species within the Bp complex share a nearly identical arsenal of virulence traits, yet are harmless to humans. Clues to the origin of virulence in this group can be found in their genetics and ecology. As a resident of the rhizosphere, Bp faces competition for nutrients and predation by other organisms. Adaptation over millennia has enabled Bp to accumulate mechanisms that overlap in their ability to promote fitness in the environment and virulence in mammals. Here, we review the ecology of Bp and its range of virulence attributes, and offer hypotheses on the evolution of virulence in the Bp complex which are relevant to other environmental pathogens.