Genomic loss in environmental and isogenic morphotype isolates of Burkholderia pseudomallei is associated with intracellular survival and plaque-forming efficiency

Saiprom, Natnaree; Sangsri, Tanes; Tandhavanant, Sarunporn; Sengyee, Sineenart; Phunpang, Rungnapa; Preechanukul, Anucha; Surin, Uriwan; Tuanyok, Apichai; Lertmemongkolchai, Ganjana; Chantratita, Wasun; West, T. Eoin; Chantratita, Narisara

doi:10.1371/journal.pntd.0008590

Cited by 5 publications

(11 citation statements)

References 64 publications

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“…Of those, the deleted genes are including genes involved in T3SS-3 and T6SS-5 systems. Interestingly, Saiprom et al (2020) also identified an absence of multiple T3SS-1 genes of previously described Thai environmental strain RF80.…”

Section: Genetic Structural or Molecular Variations Observed In Hostmentioning

confidence: 63%

An Evolutionary Arms Race Between Burkholderia pseudomallei and Host Immune System: What Do We Know?

et al. 2021

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A better understanding of co-evolution between pathogens and hosts holds promise for better prevention and control strategies. This review will explore the interactions between Burkholderia pseudomallei, an environmental and opportunistic pathogen, and the human host immune system. B. pseudomallei causes “Melioidosis,” a rapidly fatal tropical infectious disease predicted to affect 165,000 cases annually worldwide, of which 89,000 are fatal. Genetic heterogeneities were reported in both B. pseudomallei and human host population, some of which may, at least in part, contribute to inter-individual differences in disease susceptibility. Here, we review (i) a multi-host—pathogen characteristic of the interaction; (ii) selection pressures acting on B. pseudomallei and human genomes with the former being driven by bacterial adaptation across ranges of ecological niches while the latter are driven by human encounter of broad ranges of pathogens; (iii) the mechanisms that generate genetic diversity in bacterial and host population particularly in sequences encoding proteins functioning in host—pathogen interaction; (iv) reported genetic and structural variations of proteins or molecules observed in B. pseudomallei—human host interactions and their implications in infection outcomes. Together, these predict bacterial and host evolutionary trajectory which continues to generate genetic diversity in bacterium and operates host immune selection at the molecular level.

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Section: Genetic Structural or Molecular Variations Observed In Hostmentioning

confidence: 63%

An Evolutionary Arms Race Between Burkholderia pseudomallei and Host Immune System: What Do We Know?

et al. 2021

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“…Although the function of cell-to-cell fusion in the pathogenesis of melioidosis is not yet well-determined, B. pseudomallei is capable of inducing MNGC in lung tissue of melioidosis patients and infected mice ( Wong et al, 1995 ; Conejero et al, 2011 ). In addition, deletion of T6SS-5 genes drastically decreased intracellular replication, cell-to-cell fusion, and virulence of B. pseudomallei in mammalian models of acute infection ( Pilatz et al, 2006 ; Burtnick et al, 2011 ; French et al, 2011 ; Hopf et al, 2014 ; Schwarz et al, 2014 ; Toesca et al, 2014 ; Saiprom et al, 2020 ). Thus, it is possible that the dramatic within-host adaptive changes in intracellular replication and cell-to-cell fusion may enhance the virulence in vivo , which could influence the outcome of P17.…”

Section: Discussionmentioning

confidence: 99%

“…An intracellular bacterial survival assay was performed to compare the ability of B. pseudomallei pairs to grow within the host cells. The assay was performed in two independent experiments as previously described ( Saiprom et al, 2020 ), but with some modifications. Briefly, A549 cells were seeded at 1.5 × 10 4 cells per well into a 96-well plate, washed with PBS, and infected with B. pseudomallei at MOI of 30:1 as described in the MNGC assay.…”

Section: Methodsmentioning

confidence: 99%

“…Growth curve analysis was performed to determine the ability of B. pseudomallei to grow in an enrichment medium as previously described ( Saiprom et al, 2020 ). A single colony of B. pseudomallei was inoculated in 3 ml of Luria-Bertani (LB) broth and incubated at 37°C with shaking at 200 rpm for 18 h. Culture bacteria were centrifuged at 12,000 rpm for 5 min, washed with PBS, and resuspended with PBS.…”

Section: Methodsmentioning

confidence: 99%

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Phenotypic and genetic alterations of Burkholderia pseudomallei in patients during relapse and persistent infections

et al. 2023

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The bacterium Burkholderia pseudomallei is the causative agent of melioidosis, a severe tropical disease associated with high mortality and relapse and persistent infections. Treatment of melioidosis requires prolonged antibiotic therapy; however, little is known about relapse and persistent infections, particularly the phenotypic and genetic alterations of B. pseudomallei in patients. In this study, we performed pulsed-field gel electrophoresis (PFGE) to compare the bacterial genotype between the initial isolate and the subsequent isolate from each of 23 suspected recurrent and persistent melioidosis patients in Northeast Thailand. We used whole-genome sequencing (WGS) to investigate multilocus sequence types and genetic alterations of within-host strain pairs. We also investigated the bacterial phenotypes associated with relapse and persistent infections, including multinucleated giant cell (MNGC) formation efficiency and intracellular multiplication. We first identified 13 (1.2%) relapse, 7 (0.7%) persistent, and 3 (0.3%) reinfection patients from 1,046 survivors. Each of the 20 within-host strain pairs from patients with relapse and persistent infections shared the same genotype, suggesting that the subsequent isolates arise from the infecting isolate. Logistic regression analysis of clinical data revealed regimen and duration of oral antibiotic therapies as risk factors associated with relapse and persistent infections. WGS analysis demonstrated 17 within-host genetic alteration events in 6 of 20 paired isolates, including a relatively large deletion and 16 single-nucleotide polymorphism (stocktickerSNP) mutations distributed across 12 genes. In 1 of 20 paired isolates, we observed significantly increased cell-to-cell fusion and intracellular replication in the second isolate compared with the initial isolate from a patient with persistent infection. WGS analysis suggested that a non-synonymous mutation in the tssB-5 gene, which encoded an essential component of the type VI secretion system, may be associated with the increased intracellular replication and MNGC formation efficiency of the second isolate of the patient. This information provides insights into genetic and phenotypic alterations in B. pseudomallei in human melioidosis, which may represent a bacterial strategy for persistent and relapse infections.

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“…were resuspended in 2 mL of PBS and adjusted to a 0.5 McFarland standard solution. Fluorescent staining was performed as previously described with modifications [ 25 ]. Briefly, A549 cells suspended in RPMI containing 1% FBS were seeded at 5 × 10 5 cells/well on a sterile glass coverslip placed in a 6-well tissue culture plate and incubated overnight at 37 °C with 5% CO 2 .…”

Section: Methodsmentioning

confidence: 99%

Characterization of Virulence Factors in Candida Species Causing Candidemia in a Tertiary Care Hospital in Bangkok, Thailand

Saiprom

Wongsuk

Oonanant

et al. 2023

JoF

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Candidemia is often associated with high mortality, and Candida albicans, Candida tropicalis, Candida glabrata, and Candida parapsilosis are common causes of this disease. The pathogenicity characteristics of specific Candida spp. that cause candidemia in Thailand are poorly understood. This study aimed to characterize the virulence factors of Candida spp. Thirty-eight isolates of different Candida species from blood cultures were evaluated for their virulence properties, including exoenzyme and biofilm production, cell surface hydrophobicity, tissue invasion, epithelial cell damage, morphogenesis, and phagocytosis resistance; the identity and frequency of mutations in ERG11 contributing to azole-resistance were also determined. C. albicans had the highest epithelial cell invasion rate and phospholipase activity, with true hyphae formation, whereas C. tropicalis produced the most biofilm, hydrophobicity, protease activity, and host cell damage and true hyphae formation. ERG11 mutations Y132F and S154F were observed in all azole-resistant C. tropicalis. C. glabrata had the most hemolytic activity while cell invasion was low with no morphologic transition. C. glabrata was more easily phagocytosed than other species. C. parapsilosis generated pseudohyphae but not hyphae and did not exhibit any trends in exoenzyme production. This knowledge will be crucial for understanding the pathogenicity of Candida spp. and will help to explore antivirulence-based treatment.

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Genomic loss in environmental and isogenic morphotype isolates of Burkholderia pseudomallei is associated with intracellular survival and plaque-forming efficiency

Cited by 5 publications

References 64 publications

An Evolutionary Arms Race Between Burkholderia pseudomallei and Host Immune System: What Do We Know?

An Evolutionary Arms Race Between Burkholderia pseudomallei and Host Immune System: What Do We Know?

Phenotypic and genetic alterations of Burkholderia pseudomallei in patients during relapse and persistent infections

Characterization of Virulence Factors in Candida Species Causing Candidemia in a Tertiary Care Hospital in Bangkok, Thailand

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