A Persisting Nontropical Focus of Burkholderia pseudomallei with Limited Genome Evolution over Five Decades

Abstract

Burkholderia pseudomallei is the causative agent of the high-mortality disease melioidosis. Although melioidosis is classified as a tropical disease, rare autochthonous cases have been reported from temperate climatic regions, with uncertainty as to whether B. pseudomallei is persistent in the local environment and whether specific genetic mechanisms facilitate the survival of B. pseudomallei outside the tropics. Sporadic cases of melioidosis occurred in a valley region (latitude 31.6°S) in southwest Western Australia, Australia, between 1966 and 1992. We report a new melioidosis cluster in the same region following high rainfall in January 2017. More than 20 animals died, and B. pseudomallei was isolated from four alpacas, a parrot, and three environmental samples taken from the farm where the alpacas resided. Epidemiological data and genomics revealed that two locations on the farm were the probable sources of the alpaca infections. We determined that B. pseudomallei isolates from the 2017 cluster belonged to sequence type 284 (ST-284), as did all isolates recovered from 1966 to 1992. Genomic analysis confirmed that the ST-284 isolates were clonal and contained conserved genomic islands and limited evidence of recombination. We identified protein-coding regions unique to these isolates that might influence the persistence of B. pseudomallei in this temperate region. We demonstrate the environmental persistence of B. pseudomallei in a temperate region for over 50 years, with limited genetic changes suggesting a latent state and with activation, potential aerosolization, and local dispersal following unusually high rainfall. IMPORTANCE Burkholderia pseudomallei is predominantly a tropical pathogen uncommonly found in the environment of temperate climatic regions. It is unclear if introduction into temperate regions is sporadic and temporary or if B. pseudomallei can persist in such environments. B. pseudomallei was identified in the environment of southwest Western Australia with melioidosis cases between 1966 and 1991. We report a new cluster with 23 animal fatalities in the same region from 2017, with B. pseudomallei again being recovered from the environment. Comparison of the isolates from the first and second clusters using genomics revealed a single sequence type, high clonality, and limited recombination, even though the time of recovery of the isolates spanned 51 years. This is a major contrast to the extensive genomic diversity seen in the tropics. Our data support the suggestion that B. pseudomallei has the ability to persist in nontropical environments, potentially in a latent state, and has the ability to activate following favorable conditions (rainfall) and then infect animals and humans.

Multiple phylogenetically-diverse, differentially-virulent Burkholderia pseudomallei isolated from a single soil sample collected in Thailand

“…Genomes sequenced in this study are shown in red. The tree was rooted with MSHR668 based on its basal position in other studies [71]. https://doi.org/10.1371/journal.pntd.0010172.g002…”

Melioidosis in Australia

“…Melioidosis in Australia is endemic across the tropical north of Australia (Figure 1) where it occurs as a sporadic infection of people who have had exposure to contaminated soil or surface water through direct transdermal inoculation, inhalation and possibly ingestion 3 . Occasional point source case clusters have occurred related to contaminated water, medical solutions or hand wash products [4][5][6][7] , and animal case clusters have been associated with flooding of pasture land 8 . The majority of acute febrile melioidosis occurs as a septicaemia with or without pneumonia, peaking during the tropical wet season, and sometimes follows in the wake of tropical cyclones 9 , though not necessarily in all of northern Australia 10 .…”

Low risk of acquiring melioidosis from the environment in the continental United States

“…The majority of melioidosis cases are reported from Southeast Asia and northern Australia although the global disease burden is thought to be drastically underestimated [9]. There has been a recent increase in reports of locally acquired melioidosis from sub-tropical regions, such as Sonora Mexico [10], Western Australia [11], and Texas in the United States (U.S) [12][13][14]. In the continental U.S. (CONUS) human melioidosis cases can be assigned to three categories in order of frequency: 1) acquired outside the CONUS during travel to endemic regions (e.g., the Caribbean, Central/South America, Southeast Asia), 2) acquired within the CONUS from contaminated items imported from endemic regions, and 3) acquired directly from the local environment in the CONUS (Table 1).…”