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Published VersionCC BY V4.0, Open Access
Journal article
Pathogen to commensal? Longitudinal within-host population dynamics, evolution, and adaptation during a chronic >16-year Burkholderia pseudomallei infection
PLoS Pathogens, Vol.16(3), e1008298
2020
Abstract
Although acute melioidosis is the most common outcome of Burkholderia pseudomallei infection, we have documented a case, P314, where disease severity lessened with time, and the pathogen evolved towards a commensal relationship with the host. In the current study, we used whole-genome sequencing to monitor this long-term symbiotic relationship to better understand B. pseudomallei persistence in P314's sputum despite intensive initial therapeutic regimens. We collected and sequenced 118 B. pseudomallei isolates from P314's airways over a >16-year period, and also sampled the patient's home environment, recovering six closely related B. pseudomallei isolates from the household water system. Using comparative genomics, we identified 126 SNPs in the core genome of the 124 isolates or 162 SNPs/indels when the accessory genome was included. The core SNPs were used to construct a phylogenetic tree, which demonstrated a close relationship between environmental and clinical isolates and detailed within-host evolutionary patterns. The phylogeny had little homoplasy, consistent with a strictly clonal mode of genetic inheritance. Repeated sampling revealed evidence of genetic diversification, but frequent extinctions left only one successful lineage through the first four years and two lineages after that. Overall, the evolution of this population is nonadaptive and best explained by genetic drift. However, some genetic and phenotypic changes are consistent with in situ adaptation. Using a mouse model, P314 isolates caused greatly reduced morbidity and mortality compared to the environmental isolates. Additionally, potentially adaptive phenotypes emerged and included differences in the O-antigen, capsular polysaccharide, motility, and colony morphology. The >13-year co-existence of two long-lived lineages presents interesting hypotheses that can be tested in future studies to provide additional insights into selective pressures, niche differentiation, and microbial adaptation. This unusual melioidosis case presents a rare example of the evolutionary progression towards commensalism by a highly virulent pathogen within a single human host.
Details
- Title
- Pathogen to commensal? Longitudinal within-host population dynamics, evolution, and adaptation during a chronic >16-year Burkholderia pseudomallei infection
- Authors
- Talima Pearson (Author) - Northern Arizona University, United StatesJason W Sahl (Author) - Northern Arizona University, United StatesCrystal M Hepp (Author) - Northern Arizona University, United StatesKarthik Handady (Author) - Northern Arizona University, United StatesHeidie Hornstra (Author) - Northern Arizona University, United StatesAdam J Vazquez (Author) - Northern Arizona University, United StatesErik Settles (Author) - Northern Arizona University, United StatesMark Mayo (Author) - Northern Arizona University, United StatesMirjam Kaestli (Author) - Menzies School of Health ResearchCharles H D Williamson (Author) - Northern Arizona University, United StatesErin P Price (Author) - Northern Arizona University, United StatesDerek S Sarovich (Author) - Northern Arizona University, United StatesJames M Cook (Author) - Northern Arizona University, United StatesSpenser R Wolken (Author) - Northern Arizona University, United StatesRichard A Bowen (Author) - Colorado State University, United StatesApichai Tuanyok (Author) - Northern Arizona University, United StatesJeffrey T Foster (Author) - Northern Arizona University, United StatesKevin P Drees (Author) - Northern Arizona University, United StatesTimothy J Kidd (Author) - University of QueenslandScott C Bell (Author) - Prince Charles HospitalBart J Currie (Author) - Northern Arizona University, United StatesPaul Keim (Author) - Menzies School of Health Research
- Publication details
- PLoS Pathogens, Vol.16(3), e1008298
- Publisher
- Public Library of Science
- Date published
- 2020
- DOI
- 10.1371/journal.ppat.1008298
- ISSN
- 1553-7374; 1553-7374
- Copyright note
- Copyright © 2020 Pearson et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
- Organisation Unit
- University of the Sunshine Coast, Queensland; Centre for Bioinnovation
- Language
- English
- Record Identifier
- 99451105902621
- Output Type
- Journal article
- Research Statement
- false
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- Microbiology
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