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Parallel evolution in streptococcus pneumoniae biofilms

Parallel evolution in streptococcus pneumoniae biofilms
Parallel evolution in streptococcus pneumoniae biofilms
Streptococcus pneumoniae is a commensal human pathogen and the causative agent of various invasive and noninvasive diseases. Carriage of the pneumococcus in the nasopharynx is thought to be mediated by biofilm formation, an environment where isogenic populations frequently give rise to morphological colony variants, including small colony variant (SCV) phenotypes. We employed metabolic characterization and whole-genome sequencing of biofilm-derived S. pneumoniae serotype 22F pneumococcal SCVs to investigate diversification during biofilm formation. Phenotypic profiling revealed that SCVs exhibit reduced growth rates, reduced capsule expression, altered metabolic profiles, and increased biofilm formation compared to the ancestral strain. Whole-genome sequencing of 12 SCVs from independent biofilm experiments revealed that all SCVs studied had mutations within the DNA-directed RNA polymerase delta subunit (RpoE). Mutations included four large-scale deletions ranging from 51 to 264 bp, one insertion resulting in a coding frameshift, and seven nonsense single-nucleotide substitutions that result in a truncated gene product. This work links mutations in the rpoE gene to SCV formation and enhanced biofilm development in S. pneumoniae and therefore may have important implications for colonization, carriage, and persistence of the organism. Furthermore, recurrent mutation of the pneumococcal rpoE gene presents an unprecedented level of parallel evolution in pneumococcal biofilm development.
1759-6653
1316-1326
Churton, Nicholas W.V.
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Misra, Raju V.
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Howlin, Robert P.
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Allan, Raymond N.
390a7d0a-38e1-410a-8dfe-c8ef8408f5e1
Jefferies, Johanna
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Faust, Saul N.
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Gharbia, Saheer E.
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Edwards, Richard J.
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Clarke, Stuart C.
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Webb, Jeremy S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Churton, Nicholas W.V.
94b72087-288c-475f-ac3c-068218c69aae
Misra, Raju V.
fb20e035-b95c-4a49-88e1-ffbe3b858dc2
Howlin, Robert P.
8c2bdf0d-d6c1-4308-bd94-c8e81a24f527
Allan, Raymond N.
390a7d0a-38e1-410a-8dfe-c8ef8408f5e1
Jefferies, Johanna
9468e292-0b41-412d-9470-944e257c7bcf
Faust, Saul N.
f97df780-9f9b-418e-b349-7adf63e150c1
Gharbia, Saheer E.
ab49d416-0848-4f02-837d-56cea523a1c6
Edwards, Richard J.
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Clarke, Stuart C.
f7d7f7a2-4b1f-4b36-883a-0f967e73fb17
Webb, Jeremy S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d

Churton, Nicholas W.V., Misra, Raju V., Howlin, Robert P., Allan, Raymond N., Jefferies, Johanna, Faust, Saul N., Gharbia, Saheer E., Edwards, Richard J., Clarke, Stuart C. and Webb, Jeremy S. (2016) Parallel evolution in streptococcus pneumoniae biofilms. Genome Biology and Evolution, 8 (5), 1316-1326. (doi:10.1093/gbe/evw072). (PMID:27190203)

Record type: Article

Abstract

Streptococcus pneumoniae is a commensal human pathogen and the causative agent of various invasive and noninvasive diseases. Carriage of the pneumococcus in the nasopharynx is thought to be mediated by biofilm formation, an environment where isogenic populations frequently give rise to morphological colony variants, including small colony variant (SCV) phenotypes. We employed metabolic characterization and whole-genome sequencing of biofilm-derived S. pneumoniae serotype 22F pneumococcal SCVs to investigate diversification during biofilm formation. Phenotypic profiling revealed that SCVs exhibit reduced growth rates, reduced capsule expression, altered metabolic profiles, and increased biofilm formation compared to the ancestral strain. Whole-genome sequencing of 12 SCVs from independent biofilm experiments revealed that all SCVs studied had mutations within the DNA-directed RNA polymerase delta subunit (RpoE). Mutations included four large-scale deletions ranging from 51 to 264 bp, one insertion resulting in a coding frameshift, and seven nonsense single-nucleotide substitutions that result in a truncated gene product. This work links mutations in the rpoE gene to SCV formation and enhanced biofilm development in S. pneumoniae and therefore may have important implications for colonization, carriage, and persistence of the organism. Furthermore, recurrent mutation of the pneumococcal rpoE gene presents an unprecedented level of parallel evolution in pneumococcal biofilm development.

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More information

Accepted/In Press date: 26 March 2016
e-pub ahead of print date: 15 April 2016
Published date: 9 May 2016
Organisations: Centre for Biological Sciences

Identifiers

Local EPrints ID: 397135
URI: http://eprints.soton.ac.uk/id/eprint/397135
ISSN: 1759-6653
PURE UUID: 96e30df4-0838-4d3d-b242-b61cf10d8610
ORCID for Saul N. Faust: ORCID iD orcid.org/0000-0003-3410-7642
ORCID for Stuart C. Clarke: ORCID iD orcid.org/0000-0002-7009-1548
ORCID for Jeremy S. Webb: ORCID iD orcid.org/0000-0003-2068-8589

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Date deposited: 21 Jun 2016 09:16
Last modified: 03 Dec 2019 01:46

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