Experimental Evolution <italic toggle="yes">In Vivo</italic> To Identify Selective Pressures during Pneumococcal Colonization

ABSTRACT Experimental evolution is a powerful technique to understand how populations evolve from selective pressures imparted by the surrounding environment. With the advancement of whole-population genomic sequencing, it is possible to identify and track multiple contending genotypes associated wi...

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Autores principales:	Vaughn S. Cooper, Erin Honsa, Hannah Rowe, Christopher Deitrick, Amy R. Iverson, Jonathan J. Whittall, Stephanie L. Neville, Christopher A. McDevitt, Colin Kietzman, Jason W. Rosch
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Streptococcus pneumoniae evolutionary biology pathogenesis respiratory pathogens Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2ea58d7ecf3147a1a5e0154d68163c4e
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spelling	oai:doaj.org-article:2ea58d7ecf3147a1a5e0154d68163c4e2021-12-02T18:44:35ZExperimental Evolution <italic toggle="yes">In Vivo</italic> To Identify Selective Pressures during Pneumococcal Colonization10.1128/mSystems.00352-202379-5077https://doaj.org/article/2ea58d7ecf3147a1a5e0154d68163c4e2020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00352-20https://doaj.org/toc/2379-5077ABSTRACT Experimental evolution is a powerful technique to understand how populations evolve from selective pressures imparted by the surrounding environment. With the advancement of whole-population genomic sequencing, it is possible to identify and track multiple contending genotypes associated with adaptations to specific selective pressures. This approach has been used repeatedly with model species in vitro, but only rarely in vivo. Herein we report results of replicate experimentally evolved populations of Streptococcus pneumoniae propagated by repeated murine nasal colonization with the aim of identifying gene products under strong selection as well as the population genetic dynamics of infection cycles. Frameshift mutations in one gene, dltB, responsible for incorporation of d-alanine into teichoic acids on the bacterial surface, evolved repeatedly and swept to high frequency. Targeted deletions of dltB produced a fitness advantage during initial nasal colonization coupled with a corresponding fitness disadvantage in the lungs during pulmonary infection. The underlying mechanism behind the fitness trade-off between these two niches was found to be enhanced adherence to respiratory cells balanced by increased sensitivity to host-derived antimicrobial peptides, a finding recapitulated in the murine model. Additional mutations that are predicted to affect trace metal transport, central metabolism, and regulation of biofilm production and competence were also selected. These data indicate that experimental evolution can be applied to murine models of pathogenesis to gain insight into organism-specific tissue tropisms. IMPORTANCE Evolution is a powerful force that can be experimentally harnessed to gain insight into how populations evolve in response to selective pressures. Herein we tested the applicability of experimental evolutionary approaches to gain insight into how the major human pathogen Streptococcus pneumoniae responds to repeated colonization events using a murine model. These studies revealed the population dynamics of repeated colonization events and demonstrated that in vivo experimental evolution resulted in highly reproducible trajectories that reflect the environmental niche encountered during nasal colonization. Mutations impacting the surface charge of the bacteria were repeatedly selected during colonization and provided a fitness benefit in this niche that was counterbalanced by a corresponding fitness defect during lung infection. These data indicate that experimental evolution can be applied to models of pathogenesis to gain insight into organism-specific tissue tropisms.Vaughn S. CooperErin HonsaHannah RoweChristopher DeitrickAmy R. IversonJonathan J. WhittallStephanie L. NevilleChristopher A. McDevittColin KietzmanJason W. RoschAmerican Society for MicrobiologyarticleStreptococcus pneumoniaeevolutionary biologypathogenesisrespiratory pathogensMicrobiologyQR1-502ENmSystems, Vol 5, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Streptococcus pneumoniae evolutionary biology pathogenesis respiratory pathogens Microbiology QR1-502
spellingShingle	Streptococcus pneumoniae evolutionary biology pathogenesis respiratory pathogens Microbiology QR1-502 Vaughn S. Cooper Erin Honsa Hannah Rowe Christopher Deitrick Amy R. Iverson Jonathan J. Whittall Stephanie L. Neville Christopher A. McDevitt Colin Kietzman Jason W. Rosch Experimental Evolution <italic toggle="yes">In Vivo</italic> To Identify Selective Pressures during Pneumococcal Colonization
description	ABSTRACT Experimental evolution is a powerful technique to understand how populations evolve from selective pressures imparted by the surrounding environment. With the advancement of whole-population genomic sequencing, it is possible to identify and track multiple contending genotypes associated with adaptations to specific selective pressures. This approach has been used repeatedly with model species in vitro, but only rarely in vivo. Herein we report results of replicate experimentally evolved populations of Streptococcus pneumoniae propagated by repeated murine nasal colonization with the aim of identifying gene products under strong selection as well as the population genetic dynamics of infection cycles. Frameshift mutations in one gene, dltB, responsible for incorporation of d-alanine into teichoic acids on the bacterial surface, evolved repeatedly and swept to high frequency. Targeted deletions of dltB produced a fitness advantage during initial nasal colonization coupled with a corresponding fitness disadvantage in the lungs during pulmonary infection. The underlying mechanism behind the fitness trade-off between these two niches was found to be enhanced adherence to respiratory cells balanced by increased sensitivity to host-derived antimicrobial peptides, a finding recapitulated in the murine model. Additional mutations that are predicted to affect trace metal transport, central metabolism, and regulation of biofilm production and competence were also selected. These data indicate that experimental evolution can be applied to murine models of pathogenesis to gain insight into organism-specific tissue tropisms. IMPORTANCE Evolution is a powerful force that can be experimentally harnessed to gain insight into how populations evolve in response to selective pressures. Herein we tested the applicability of experimental evolutionary approaches to gain insight into how the major human pathogen Streptococcus pneumoniae responds to repeated colonization events using a murine model. These studies revealed the population dynamics of repeated colonization events and demonstrated that in vivo experimental evolution resulted in highly reproducible trajectories that reflect the environmental niche encountered during nasal colonization. Mutations impacting the surface charge of the bacteria were repeatedly selected during colonization and provided a fitness benefit in this niche that was counterbalanced by a corresponding fitness defect during lung infection. These data indicate that experimental evolution can be applied to models of pathogenesis to gain insight into organism-specific tissue tropisms.
format	article
author	Vaughn S. Cooper Erin Honsa Hannah Rowe Christopher Deitrick Amy R. Iverson Jonathan J. Whittall Stephanie L. Neville Christopher A. McDevitt Colin Kietzman Jason W. Rosch
author_facet	Vaughn S. Cooper Erin Honsa Hannah Rowe Christopher Deitrick Amy R. Iverson Jonathan J. Whittall Stephanie L. Neville Christopher A. McDevitt Colin Kietzman Jason W. Rosch
author_sort	Vaughn S. Cooper
title	Experimental Evolution <italic toggle="yes">In Vivo</italic> To Identify Selective Pressures during Pneumococcal Colonization
title_short	Experimental Evolution <italic toggle="yes">In Vivo</italic> To Identify Selective Pressures during Pneumococcal Colonization
title_full	Experimental Evolution <italic toggle="yes">In Vivo</italic> To Identify Selective Pressures during Pneumococcal Colonization
title_fullStr	Experimental Evolution <italic toggle="yes">In Vivo</italic> To Identify Selective Pressures during Pneumococcal Colonization
title_full_unstemmed	Experimental Evolution <italic toggle="yes">In Vivo</italic> To Identify Selective Pressures during Pneumococcal Colonization
title_sort	experimental evolution <italic toggle="yes">in vivo</italic> to identify selective pressures during pneumococcal colonization
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/2ea58d7ecf3147a1a5e0154d68163c4e
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Experimental Evolution <italic toggle="yes">In Vivo</italic> To Identify Selective Pressures during Pneumococcal Colonization

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