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Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts.

Publication ,  Journal Article
Tamas, I; Wernegreen, JJ; Nystedt, B; Kauppinen, SN; Darby, AC; Gomez-Valero, L; Lundin, D; Poole, AM; Andersson, SGE
Published in: Proceedings of the National Academy of Sciences of the United States of America
September 2008

Among host-dependent bacteria that have evolved by extreme reductive genome evolution, long-term bacterial endosymbionts of insects have the smallest (160-790 kb) and most A + T-rich (>70%) bacterial genomes known to date. These genomes are riddled with poly(A) tracts, and 5-50% of genes contain tracts of 10 As or more. Here, we demonstrate transcriptional slippage at poly(A) tracts within genes of Buchnera aphidicola associated with aphids and Blochmannia pennsylvanicus associated with ants. Several tracts contain single frameshift deletions; these apparent pseudogenes showed patterns of constraint consistent with purifying selection on the encoded proteins. Transcriptional slippage yielded a heterogeneous population of transcripts with variable numbers of As in the tract. Across several frameshifted genes, including B. aphidicola cell wall biosynthesis genes and a B. pennsylvanicus histidine biosynthesis gene, 12-50% of transcripts contained corrected reading frames that could potentially yield full-length proteins. In situ immunostaining confirmed the production of the cell wall biosynthetic enzyme UDP-N-acetylmuramyl pentapeptide synthase encoded by the frameshifted murF gene. Simulation studies indicated an overrepresentation of poly(A) tracts in endosymbiont genomes relative to other A + T-rich bacterial genomes. Polymerase infidelity at poly(A) tracts rescues the functionality of genes with frameshift mutations and, conversely, reduces the efficiency of expression for in-frame genes carrying poly(A) regions. These features of homopolymeric tracts could be exploited to manipulate gene expression in small synthetic genomes.

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Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

September 2008

Volume

105

Issue

39

Start / End Page

14934 / 14939

Related Subject Headings

  • Transcription, Genetic
  • Symbiosis
  • RNA, Messenger
  • Polyadenylation
  • Peptide Synthases
  • Open Reading Frames
  • Molecular Sequence Data
  • Histidine
  • Genome, Bacterial
  • Gene Expression
 

Citation

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Tamas, I., Wernegreen, J. J., Nystedt, B., Kauppinen, S. N., Darby, A. C., Gomez-Valero, L., … Andersson, S. G. E. (2008). Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts. Proceedings of the National Academy of Sciences of the United States of America, 105(39), 14934–14939. https://doi.org/10.1073/pnas.0806554105
Tamas, Ivica, Jennifer J. Wernegreen, Björn Nystedt, Seth N. Kauppinen, Alistair C. Darby, Laura Gomez-Valero, Daniel Lundin, Anthony M. Poole, and Siv G. E. Andersson. “Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts.Proceedings of the National Academy of Sciences of the United States of America 105, no. 39 (September 2008): 14934–39. https://doi.org/10.1073/pnas.0806554105.
Tamas I, Wernegreen JJ, Nystedt B, Kauppinen SN, Darby AC, Gomez-Valero L, et al. Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts. Proceedings of the National Academy of Sciences of the United States of America. 2008 Sep;105(39):14934–9.
Tamas, Ivica, et al. “Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts.Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 39, Sept. 2008, pp. 14934–39. Epmc, doi:10.1073/pnas.0806554105.
Tamas I, Wernegreen JJ, Nystedt B, Kauppinen SN, Darby AC, Gomez-Valero L, Lundin D, Poole AM, Andersson SGE. Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts. Proceedings of the National Academy of Sciences of the United States of America. 2008 Sep;105(39):14934–14939.
Journal cover image

Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

September 2008

Volume

105

Issue

39

Start / End Page

14934 / 14939

Related Subject Headings

  • Transcription, Genetic
  • Symbiosis
  • RNA, Messenger
  • Polyadenylation
  • Peptide Synthases
  • Open Reading Frames
  • Molecular Sequence Data
  • Histidine
  • Genome, Bacterial
  • Gene Expression