Within-host evolution of bacterial pathogens

Didelot, Xavier; Walker, A Sarah; Peto, Tim E. A.; Crook, Derrick W.; Wilson, Daniel J.

doi:10.1038/nrmicro.2015.13

Cited by 396 publications

(406 citation statements)

References 148 publications

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“…This relationship is distinct from those of hosts and their pathogens, which can also exhibit within-host evolution (44); for obligate, heritable symbiotic partners, hosts must maintain a viable symbiosis even if it involves a fitness cost. This study shows that intraspecific variation in hosts affects the regulation of obligate symbiosis and sheds light on its potential long-term evolutionary consequences.…”

Section: Discussionmentioning

confidence: 99%

Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts

Chong

Moran

2016

Proc. Natl. Acad. Sci. U.S.A.

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Symbiotic relationships promote biological diversification by unlocking new ecological niches. Over evolutionary time, hosts and symbionts often enter intimate and permanent relationships, which must be maintained and regulated for both lineages to persist. Many insect species harbor obligate, heritable symbiotic bacteria that provision essential nutrients and enable hosts to exploit niches that would otherwise be unavailable. Hosts must regulate symbiont population sizes, but optimal regulation may be affected by the need to respond to the ongoing evolution of symbionts, which experience high levels of genetic drift and potential selection for selfish traits. We address the extent of intraspecific variation in the regulation of a mutually obligate symbiosis, between the pea aphid (Acyrthosiphon pisum) and its maternally transmitted symbiont, Buchnera aphidicola. Using experimental crosses to identify effects of host genotypes, we measured symbiont titer, as the ratio of genomic copy numbers of symbiont and host, as well as developmental time and fecundity of hosts. We find a large (>10-fold) range in symbiont titer among genetically distinct aphid lines harboring the same Buchnera haplotype. Aphid clones also vary in fitness, measured as developmental time and fecundity, and genetically based variation in titer is correlated with host fitness, with higher titers corresponding to lower reproductive rates of hosts. Our work shows that obligate symbiosis is not static but instead is subject to short-term evolutionary dynamics, potentially reflecting coevolutionary interactions between host and symbiont.

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Section: Discussionmentioning

confidence: 99%

Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts

Chong

Moran

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…This frequent horizontal gene transfer incidence among community, together with previously observed high abundance of ARGs against vancomycin in human feces samples (Li et al, 2015), implied rapid adaptation towards newly introduced antibiotics of human pathogens under current infectious treatment. In addition, majority of these exogenous ARG-carrying fragments (68%) from clinically important pathogen species of Escherichia coli, Shigella flexneri, Acinetobacter baumannii and Enterococcus faecium, suggesting gene transfer, has had crucial role in adaptation to antibiotic stress in these pathogen species (Dijkshoorn et al, 2007;Stokes and Gillings, 2011;Didelot et al, 2016). Overall, both genetic linkage and composition-based analysis revealed surprisingly high extent and relevance of horizontal gene transfer events to resistome development in human-associated bacteria, especially human pathogens.…”

Section: Transfer Potential Of Args and Mrgsmentioning

confidence: 99%

Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection

2016

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The high frequency of antibiotic resistance is a global public health concern. More seriously, widespread metal pressure in the environment may facilitate the proliferation of antibiotic resistance via coselection of antibiotic resistance genes (ARGs) and metal resistance genes (MRGs). Given the lack of comprehensive understanding of the ARG and MRG coselection, in this study both abundance relationship and genetic linkage between ARGs and MRGs were rigorously investigated by performing a genomic analysis of a large complete genome collection. Many more ARGs were enriched in human-associated bacteria compared with those subjected to less anthropogenic interference. The signatures of ARG and MRG co-occurrence were much more frequent and the distance linkages between ARGs and MRGs were much more intimate in human pathogens than those less human-associated bacteria. Moreover, the co-occurrence structures in the habitat divisions were significantly different, which could be attributed to their distinct gene transfer potentials. More exogenous ARGs and MRGs on the genomes of human pathogens indicated the importance of recent resistance acquisition in resistome development of human commensal flora. Overall, the study emphasizes the potential risk associated with ARG and MRG coselection of both environmental and medical relevance.

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“…Whole-genome sequencing provides single-base resolution of bacterial evolution in CF lung infections (Didelot et al 2016). Similar approaches in P. aeruginosa, Burkholderia dolosa, and Burkholderia multivorans have shown that mutations accumulate in clonal lineages during adaptation to the lung.…”

mentioning

confidence: 99%

Phenotypic diversity and genotypic flexibility of Burkholderia cenocepacia during long-term chronic infection of cystic fibrosis lungs

et al. 2017

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Chronic bacterial infections of the lung are the leading cause of morbidity and mortality in cystic fibrosis patients. Tracking bacterial evolution during chronic infections can provide insights into how host selection pressures-including immune responses and therapeutic interventions-shape bacterial genomes. We carried out genomic and phenotypic analyses of 215 serially collected Burkholderia cenocepacia isolates from 16 cystic fibrosis patients, spanning a period of 2-20 yr and a broad range of epidemic lineages. Systematic phenotypic tests identified longitudinal bacterial series that manifested progressive changes in liquid media growth, motility, biofilm formation, and acute insect virulence, but not in mucoidy. The results suggest that distinct lineages follow distinct evolutionary trajectories during lung infection. Pan-genome analysis identified 10,110 homologous gene clusters present only in a subset of strains, including genes restricted to different molecular types. Our phylogenetic analysis based on 2148 orthologous gene clusters from all isolates is consistent with patient-specific clades. This suggests that initial colonization of patients was likely by individual strains, followed by subsequent diversification. Evidence of clonal lineages shared by some patients was observed, suggesting inter-patient transmission. We observed recurrent gene losses in multiple independent longitudinal series, including complete loss of Chromosome III and deletions on other chromosomes. Recurrently observed loss-of-function mutations were associated with decreases in motility and biofilm formation. Together, our study provides the first comprehensive genome-phenome analyses of B. cenocepacia infection in cystic fibrosis lungs and serves as a valuable resource for understanding the genomic and phenotypic underpinnings of bacterial evolution.

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Within-host evolution of bacterial pathogens

Cited by 396 publications

References 148 publications

Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts

Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts

Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection

Phenotypic diversity and genotypic flexibility of Burkholderia cenocepacia during long-term chronic infection of cystic fibrosis lungs

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