Co-evolutionary Signals IdentifyBurkholderia pseudomalleiSurvival Strategies in a Hostile Environment

Abstract

The soil bacterium Burkholderia pseudomallei is the causative agent of melioidosis and a significant cause of human morbidity and mortality in many tropical and subtropical countries. The species notoriously survives harsh environmental conditions but the genetic architecture for these adaptations remains unclear. Here we employed a powerful combination of genome-wide epistasis and co-selection studies (2,011 genomes), condition-wide transcriptome analyses (82 diverse conditions), and a gene knockout assay to uncover signals of “co-selection”—that is a combination of genetic markers that have been repeatedly selected together through B. pseudomallei evolution. These enabled us to identify 13,061 mutation pairs under co-selection in distinct genes and noncoding RNA. Genes under co-selection displayed marked expression correlation when B. pseudomallei was subjected to physical stress conditions, highlighting the conditions as one of the major evolutionary driving forces for this bacterium. We identified a putative adhesin (BPSL1661) as a hub of co-selection signals, experimentally confirmed a BPSL1661 role under nutrient deprivation, and explored the functional basis of co-selection gene network surrounding BPSL1661 in facilitating the bacterial survival under nutrient depletion. Our findings suggest that nutrient-limited conditions have been the common selection pressure acting on this species, and allelic variation of BPSL1661 may have promoted B. pseudomallei survival during harsh environmental conditions by facilitating bacterial adherence to different surfaces, cells, or living hosts.

Melioidosis and Burkholderia pseudomallei: progress in epidemiology, diagnosis, treatment and vaccination

“…In a prospective study of community-acquired sepsis from Ubon Ratchathani, the three commonest bacterial pathogens recovered from blood cultures were Escherichia coli, B. pseudomallei and Staphylococcus aureus , respectively, with a substantially higher mortality in the patients with melioidosis [36]. Studies of B. pseudomallei using genomics, transcriptomics and gene knockout assays have provided important novel insights into the evolution and survival of B. pseudomallei in harsh environments, supporting the hypothesis that nutrient-limited conditions have been the common selection pressure acting on this species [37 ▪ ].…”

Environmental Factors Associated With Soil Prevalence of the Melioidosis Pathogen Burkholderia pseudomallei: A Longitudinal Seasonal Study From South West India

“…Findings of higher numbers of B. pseudomallei in deeper soil horizons below 30 cm (Manivanh et al, 2017) strengthen the hypothesis that low nutrient levels correlate with the abundance of B. pseudomallei. Recently, Chewapreecha et al (2022) suggested genetic adaptation of B. pseudomallei to nutrient depletion during evolution based on their extensive genomic and transcriptomic analyses.…”

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

“…A lack of travel history for the two Texas cases and phylogeographic analysis of the infecting strains strongly suggest these two infections were independently acquired from the local environment in Texas. Detecting B. pseudomallei in the environment has been historically challenging due to the incomplete understanding of its optimal habitat (e.g., soil composition, moisture content, presence of competing bacteria [29][30][31]). However, our findings are consistent with the idea that B. pseudomallei is quite rare in the environment in this region of Texas.…”