Environmental Attributes Influencing the Distribution of Burkholderia pseudomallei in Northern Australia

PLOS ONE, Dec 2019

Factors responsible for the spatial and temporal clustering of Burkholderia pseudomallei in the environment remain to be elucidated. Whilst laboratory based experiments have been performed to analyse survival of the organism in various soil types, such approaches are strongly influenced by alterations to the soil micro ecology during soil sanitisation and translocation. During the monsoonal season in Townsville, Australia, B. pseudomallei is discharged from Castle Hill (an area with a very high soil prevalence of the organism) by groundwater seeps and is washed through a nearby area where intensive sampling in the dry season has been unable to detect the organism. We undertook environmental sampling and soil and plant characterisation in both areas to ascertain physiochemical and macro-floral differences between the two sites that may affect the prevalence of B. pseudomallei. In contrast to previous studies, the presence of B. pseudomallei was correlated with a low gravimetric water content and low nutrient availability (nitrogen and sulphur) and higher exchangeable potassium in soils favouring recovery. Relatively low levels of copper, iron and zinc favoured survival. The prevalence of the organism was found to be highest under the grasses Aristida sp. and Heteropogon contortus and to a lesser extent under Melinis repens. The findings of this study indicate that a greater variety of factors influence the endemicity of melioidosis than has previously been reported, and suggest that biogeographical boundaries to the organisms’ distribution involve complex interactions.

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Environmental Attributes Influencing the Distribution of Burkholderia pseudomallei in Northern Australia

September Environmental Attributes Influencing the Distribution of Burkholderia pseudomallei in Northern Australia Anthony L. Baker 0 1 Jessica Ezzahir 0 1 Christopher Gardiner 0 1 Warren Shipton 0 1 Jeffrey M. Warner 0 1 0 1 Environmental and Public Health Microbiology Research Group, School of Veterinary and Biomedical Sciences, James Cook University , Townsville , Australia , 2 Tasmanian Institute of Agriculture, University of Tasmania, Sandy Bay Campus , Hobart , Australia , 3 Faculty of Science, Asia-Pacific International University , MuakLek, Saraburi , Thailand 1 Editor: R. Mark Wooten, University of Toledo School of Medicine, UNITED STATES Factors responsible for the spatial and temporal clustering of Burkholderia pseudomallei in the environment remain to be elucidated. Whilst laboratory based experiments have been performed to analyse survival of the organism in various soil types, such approaches are strongly influenced by alterations to the soil micro ecology during soil sanitisation and translocation. During the monsoonal season in Townsville, Australia, B. pseudomallei is discharged from Castle Hill (an area with a very high soil prevalence of the organism) by groundwater seeps and is washed through a nearby area where intensive sampling in the dry season has been unable to detect the organism. We undertook environmental sampling and soil and plant characterisation in both areas to ascertain physiochemical and macro-floral differences between the two sites that may affect the prevalence of B. pseudomallei. In contrast to previous studies, the presence of B. pseudomallei was correlated with a low gravimetric water content and low nutrient availability (nitrogen and sulphur) and higher exchangeable potassium in soils favouring recovery. Relatively low levels of copper, iron and zinc favoured survival. The prevalence of the organism was found to be highest under the grasses Aristida sp. and Heteropogon contortus and to a lesser extent under Melinis repens. The findings of this study indicate that a greater variety of factors influence the endemicity of melioidosis than has previously been reported, and suggest that biogeographical boundaries to the organisms' distribution involve complex interactions. - Competing Interests: The authors have declared that no competing interests exist. Burkholderia pseudomallei is a Gram-negative saprophytic bacterium which is the causative agent of melioidosis; a clinically diverse and often fatal cause of community acquired pneumonia in tropical and subtropical regions worldwide [1]. The environmental distribution of the organism is clustered over both spatial and temporal scales and distinct biogeographical boundaries to the free dispersal of the organism have been identified [2–4]. Endemic foci of B. pseudomallei are often identified through spatial analysis of clinical cases [5, 6], however it is clear that melioidosis case clusters are prevalent throughout tropical regions of Australasia and Southeast Asia. In these regions, the highest incidence of melioidosis and the highest environmental prevalence of B. pseudomallei occurs during the monsoonal seasons when cases of melioidosis spike following high rainfall events [7]. Such events may be associated with translocation of the organism from a subterranean reservoir through mobilisation of the bacterium by groundwater [8–10]. Although much is known about melioidosis pathophysiology, a considerable gap remains regarding the natural ecology of the organism. Laboratory based comparisons of the organisms survival in different soil types are biased in that they largely ignore important considerations such as disturbance of the soil in pots and climactic effects; whilst field based seeding of B. pseudomallei is not possible due the organisms high pathogenicity. Environmental studies have indicated that there are distinct soil physiochemical attributes associated with the biogeography of the organism in the soil, including pH, iron content and water availability [11–13], however the complex nature of soil ecosystems means that only limited studies have been performed in this field. We have previously described an endemic focus of B. pseudomallei associated with Castle Hill; a granite monolith in Townsville city, northern Australia [10]. The formation represents one of three foci of clinical melioidosis in Queensland, Australia [14], and represents a unique study area in that groundwater seeps are prevalent on Castle Hill. Large quantities of viable B. pseudomallei thus are mobilised following rainfall events into a nearby area which shows a very low environmental prevalence of the organism during the dry season. This phenomenon indicates that environmental differences between the two areas likely contribute to a failure of the organism to establish in the downstream area. A detailed comparative study of the two areas therefore may hold important clues as to the small-scale environmental properties that affect th (...truncated)


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Anthony L. Baker, Jessica Ezzahir, Christopher Gardiner, Warren Shipton, Jeffrey M. Warner. Environmental Attributes Influencing the Distribution of Burkholderia pseudomallei in Northern Australia, PLOS ONE, 2015, Volume 10, Issue 9, DOI: 10.1371/journal.pone.0138953