Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 105, Issue 39, Pages 14934-14939Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.0806554105
Keywords
homopolymeric tracts; pseudogenes; Blochmannia pennsylvanicus; transcriptional slippage; Buchnera aphidicola
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Funding
- National Institutes of Health and the National Science Foundation
- Swedish Research Council and the Knut and Alice Wallenberg Foundation
- Swedish Agricultural Research Council
- Swedish Research Council
- Goran Gustafsson Foundation
- Swedish Foundation for Strategic Research
- Knut and Alice Wallenberg Foundation
- European Union
- Direct For Biological Sciences
- Div Of Molecular and Cellular Bioscience [1103113] Funding Source: National Science Foundation
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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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