Competence in Streptococcus pneumoniae Is a Response to an Increasing Mutational Burden

Alyssa L. Gagne, Kathleen E. Stevens, Marco Cassone, Amit Pujari, Olufunke E. Abiola, Diana J. Chang, Michael E. Sebert

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Competence for genetic transformation in Streptococcus pneumoniae has previously been described as a quorum-sensing trait regulated by a secreted peptide pheromone. Recently we demonstrated that competence is also activated by reduction in the accuracy of protein biosynthesis. We have now investigated whether errors upstream of translation in the form of random genomic mutations can provide a similar stimulus. Here we show that generation of a mutator phenotype in S. pneumoniae through deletions of mutX, hexA or hexB enhanced the expression of competence. Similarly, chemical mutagenesis with the nucleotide analog dPTP promoted development of competence. To investigate the relationship between mutational load and the activation of competence, replicate lineages of the mutX strain were serially passaged under conditions of relaxed selection allowing random accumulation of secondary mutations. Competence increased with propagation in these lineages but not in control lineages having wild-type mutX. Resequencing of these derived strains revealed between 1 and 9 single nucleotide polymorphisms (SNPs) per lineage, which were broadly distributed across the genome and did not involve known regulators of competence. Notably, the frequency of competence development among the sequenced strains correlated significantly with the number of nonsynonymous mutations that had been acquired. Together, these observations provide support for the hypothesis that competence in S. pneumoniae is regulated in response to the accumulated burden of coding mutations in the bacterial genome. In contrast to previously described DNA damage response systems that are activated by physical lesions in the chromosome, this pneumococcal pathway may represent a unique stress response system that monitors the coding integrity of the genome.

Original languageEnglish (US)
Article numbere72613
JournalPLoS One
Volume8
Issue number8
DOIs
StatePublished - Aug 13 2013

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Streptococcus pneumoniae
Mental Competency
Genes
mutation
Nucleotides
genome
Mutagenesis
Pheromones
Biosynthesis
Chromosomes
Polymorphism
quorum sensing
genetic transformation
Chemical activation
mutagenesis
DNA damage
pheromones
single nucleotide polymorphism
translation (genetics)
stress response

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Gagne, A. L., Stevens, K. E., Cassone, M., Pujari, A., Abiola, O. E., Chang, D. J., & Sebert, M. E. (2013). Competence in Streptococcus pneumoniae Is a Response to an Increasing Mutational Burden. PLoS One, 8(8), [e72613]. https://doi.org/10.1371/journal.pone.0072613

Competence in Streptococcus pneumoniae Is a Response to an Increasing Mutational Burden. / Gagne, Alyssa L.; Stevens, Kathleen E.; Cassone, Marco; Pujari, Amit; Abiola, Olufunke E.; Chang, Diana J.; Sebert, Michael E.

In: PLoS One, Vol. 8, No. 8, e72613, 13.08.2013.

Research output: Contribution to journalArticle

Gagne, AL, Stevens, KE, Cassone, M, Pujari, A, Abiola, OE, Chang, DJ & Sebert, ME 2013, 'Competence in Streptococcus pneumoniae Is a Response to an Increasing Mutational Burden', PLoS One, vol. 8, no. 8, e72613. https://doi.org/10.1371/journal.pone.0072613
Gagne AL, Stevens KE, Cassone M, Pujari A, Abiola OE, Chang DJ et al. Competence in Streptococcus pneumoniae Is a Response to an Increasing Mutational Burden. PLoS One. 2013 Aug 13;8(8). e72613. https://doi.org/10.1371/journal.pone.0072613
Gagne, Alyssa L. ; Stevens, Kathleen E. ; Cassone, Marco ; Pujari, Amit ; Abiola, Olufunke E. ; Chang, Diana J. ; Sebert, Michael E. / Competence in Streptococcus pneumoniae Is a Response to an Increasing Mutational Burden. In: PLoS One. 2013 ; Vol. 8, No. 8.
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