uu.seUppsala University Publications
Change search
ReferencesLink to record
Permanent link

Direct link
Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
Show others and affiliations
2008 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 105, no 39, 14934-14939 p.Article in journal (Refereed) Published
Abstract [en]

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.

Place, publisher, year, edition, pages
2008. Vol. 105, no 39, 14934-14939 p.
Keyword [en]
homopolymeric tracts, pseudogenes, Blochmannia pennsylvanicus, transcriptional slippage, Buchnera aphidicola
National Category
Biological Sciences
URN: urn:nbn:se:uu:diva-107728DOI: 10.1073/pnas.0806554105ISI: 000261914300022PubMedID: 18815381OAI: oai:DiVA.org:uu-107728DiVA: diva2:232623
Available from: 2009-08-24 Created: 2009-08-24 Last updated: 2010-08-09Bibliographically approved
In thesis
1. Evolutionary Processes and Genome Dynamics in Host-Adapted Bacteria
Open this publication in new window or tab >>Evolutionary Processes and Genome Dynamics in Host-Adapted Bacteria
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Many bacteria live in close association with other organisms such as plants and animals, with important implications for both health and disease. This thesis investigates bacteria that are well adapted to live inside an animal host, and describes the molecular evolutionary processes underlying host-adaptation, based on bacterial genome comparisons.

Insect-transmitted bacteria of the genus Bartonella infect the red blood cells of mammals, and we investigate host adaptation and genome evolution in this genus. In Bartonella, many host-interaction systems are encoded in a highly variable chromosomal segment previously shown to be amplified and packaged into bacteriophage particles. Among all genes imported into the Bartonella ancestor, we identify the short gene cluster encoding these phage particles as the most evolutionary conserved, indicating a strong selective advantage and a role in niche adaptation. We also provide an overview of the remarkable evolutionary dynamics of type IV and type V secretion systems, including a detailed analysis of the type IV secretion system trw. Our results highlight the importance of recombination and gene conversion in the evolution of host-adaptation systems, and reveal how these mutational mechanisms result in strikingly different outcomes depending on the selective constraints.

In the insect endosymbionts Buchnera and Blochmannia, we show that genes frameshifted at poly(A) tracts can remain functional due to transcriptional slippage. Selection against poly(A) tracts is very inefficient in these genomes compared to other bacteria, and we discuss why this can lead to increased rates of gene loss. Using the human pathogen Helicobacter pylori as a model, we provide a deeper understanding of why highly expressed genes evolve slowly.

This thesis emphasizes the power of using complete genome sequences to study evolutionary processes. In particular, we argue that knowledge about the complex evolution of duplicated gene segments is crucial to understand host adaptation in bacteria.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2009. 64 p.
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 668
molecular evolution, pathogen, secretion system, Bartonella, Buchnera, Blochmannia, Helicobacter
National Category
Bioinformatics and Systems Biology
Research subject
Evolutionary Genetics
urn:nbn:se:uu:diva-107720 (URN)978-91-554-7596-3 (ISBN)
Public defence
2009-10-09, Lindahlsalen, EBC, Norbyvägen 18, Uppsala, 09:15 (English)
Available from: 2009-09-18 Created: 2009-08-24 Last updated: 2009-09-22

Open Access in DiVA

No full text

Other links

Publisher's full textPubMed
By organisation
Molecular Evolution
In the same journal
Proceedings of the National Academy of Sciences of the United States of America
Biological Sciences

Search outside of DiVA

GoogleGoogle Scholar
The number of downloads is the sum of all downloads of full texts. It may include eg previous versions that are now no longer available

Altmetric score

Total: 192 hits
ReferencesLink to record
Permanent link

Direct link