Change search
CiteExportLink to record
Permanent link

Direct link
Cite
Citation style
  • apa
  • ieee
  • modern-language-association-8th-edition
  • vancouver
  • Other style
More styles
Language
  • de-DE
  • en-GB
  • en-US
  • fi-FI
  • nn-NO
  • nn-NB
  • sv-SE
  • Other locale
More languages
Output format
  • html
  • text
  • asciidoc
  • rtf
A Unified Multitude: Experimental Studies of Bacterial Chromosome Organization
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. (Diarmaid Hughes)ORCID iD: 0000-0003-0382-0234
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Bacteria are many, old and varied; different bacterial species have been evolving for millions of years and show many disparate life-styles and types of metabolism. Nevertheless, some of the characteristics regarding how bacteria organize their chromosomes are relatively conserved, suggesting that they might be both ancient and important, and that selective pressures inhibit their modification. This thesis aims to study some of these characteristics experimentally, assessing how changes affect bacterial growth, and how, after changing conserved features, bacteria might evolve.

First, we experimentally tested what are the constraints on the horizontal transfer of a gene highly important for bacterial growth. Second, we investigated the significance of the location and orientation of a highly expressed and essential operon; and we experimentally evolved strains with suboptimal locations and orientations to assess how bacteria could adapt to these changes. Thirdly, we sought to understand the accessibility of different regions of the bacterial chromosome to engage in homologous recombination. And lastly, we constructed bacterial strains with chromosomal inversions to assess what effect the inversions had on growth rate, and how bacteria carrying costly inversions could evolve to reduce these costs.

The results provide evidence for different selective forces acting to conserve these chromosome organizational traits. Accordingly, we found that evolutionary distance, functional conservation, suboptimal expression and impaired network connectivity of a gene can affect the successful transfer of genes between bacterial species. We determined that relative location of an essential and highly expressed operon is critical for supporting fast growth rate, and that its location seems to be more important than its orientation. We also found that both the location, and relative orientation of separated duplicate sequences can affect recombination rates between these sequences in different regions of the chromosome. Finally, the data suggest that the importance of having the two arms of a circular bacterial chromosome approximately equal in size is a strong selective force acting against certain type of chromosomal inversions.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. , p. 66
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 1392
Keyword [en]
bacterial evolution, chromosome organization and structure, chromosomal inversions, EF-Tu, horizontal gene transfer
National Category
Microbiology Genetics Evolutionary Biology
Research subject
Biology with specialization in Microbiology
Identifiers
URN: urn:nbn:se:uu:diva-332471ISBN: 978-91-513-0140-2 (print)OAI: oai:DiVA.org:uu-332471DiVA, id: diva2:1153239
Public defence
2017-12-15, room B42, Uppsala Biomedical Centre (BMC), Husargatan 3, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2017-11-24 Created: 2017-10-29 Last updated: 2018-03-07
List of papers
1. Functional Constraints on Replacing an Essential Gene with Its Ancient and Modern Homologs
Open this publication in new window or tab >>Functional Constraints on Replacing an Essential Gene with Its Ancient and Modern Homologs
Show others...
2017 (English)In: mBio, ISSN 2161-2129, E-ISSN 2150-7511, Vol. 8, no 4, article id e01276-17Article in journal (Refereed) Published
Abstract [en]

Genes encoding proteins that carry out essential informational tasks in the cell, in particular where multiple interaction partners are involved, are less likely to be transferable to a foreign organism. Here, we investigated the constraints on transfer of a gene encoding a highly conserved informational protein, translation elongation factor Tu (EF-Tu), by systematically replacing the endogenous tufA gene in the Escherichia coli genome with its extant and ancestral homologs. The extant homologs represented tuf variants from both near and distant homologous organisms. The ancestral homologs represented phylogenetically resurrected tuf sequences dating from 0.7 to 3.6 billion years ago (bya). Our results demonstrate that all of the foreign tuf genes are transferable to the E. coli genome, provided that an additional copy of the EF-Tu gene, tufB, remains present in the E. coli genome. However, when the tufB gene was removed, only the variants obtained from the gammaproteobacterial family (extant and ancestral) supported growth which demonstrates the limited functional interchangeability of E. coli tuf with its homologs. Relative bacterial fitness correlated with the evolutionary distance of the extant tuf homologs inserted into the E. coli genome. This reduced fitness was associated with reduced levels of EF-Tu and reduced rates of protein synthesis. Increasing the expression of tuf partially ameliorated these fitness costs. In summary, our analysis suggests that the functional conservation of protein activity, the amount of protein expressed, and its network connectivity act to constrain the successful transfer of this essential gene into foreign bacteria.IMPORTANCE Horizontal gene transfer (HGT) is a fundamental driving force in bacterial evolution. However, whether essential genes can be acquired by HGT and whether they can be acquired from distant organisms are very poorly understood. By systematically replacing tuf with ancestral homologs and homologs from distantly related organisms, we investigated the constraints on HGT of a highly conserved gene with multiple interaction partners. The ancestral homologs represented phylogenetically resurrected tuf sequences dating from 0.7 to 3.6 bya. Only variants obtained from the gammaproteobacterial family (extant and ancestral) supported growth, demonstrating the limited functional interchangeability of E. coli tuf with its homologs. Our analysis suggests that the functional conservation of protein activity, the amount of protein expressed, and its network connectivity act to constrain the successful transfer of this essential gene into foreign bacteria.

Keyword
EF-Tu, ancient genes, horizontal gene transfer, proteobacteria, tuf
National Category
Microbiology
Research subject
Biology with specialization in Microbiology; Biology with specialization in Molecular Biology; Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-330501 (URN)10.1128/mBio.01276-17 (DOI)000409384300045 ()28851849 (PubMedID)
Available from: 2017-10-02 Created: 2017-10-02 Last updated: 2017-12-19Bibliographically approved
2. Phenotypic and Genotypic Responses to Relocating a Highly-Expressed Bacterial Operon.
Open this publication in new window or tab >>Phenotypic and Genotypic Responses to Relocating a Highly-Expressed Bacterial Operon.
(English)Manuscript (preprint) (Other academic)
Keyword
location & orientation, chromosomal organization, highly expressed genes, EF-Tu, tuf
National Category
Microbiology Genetics
Research subject
Biology with specialization in Microbiology; Biology with specialization in Molecular Biology
Identifiers
urn:nbn:se:uu:diva-332469 (URN)
Available from: 2017-10-27 Created: 2017-10-27 Last updated: 2017-10-29
3. Chromosomal Location Determines the Rate of Intrachromosomal Homologous Recombination.
Open this publication in new window or tab >>Chromosomal Location Determines the Rate of Intrachromosomal Homologous Recombination.
(English)Manuscript (preprint) (Other academic)
Keyword
Co-evolution, gene families, chromosome organization, gene orientation
National Category
Genetics Microbiology
Research subject
Biology with specialization in Microbiology; Biology with specialization in Molecular Biology
Identifiers
urn:nbn:se:uu:diva-332470 (URN)
Available from: 2017-10-27 Created: 2017-10-27 Last updated: 2017-10-29
4. The Selective Advantage of Replichore Balance in Salmonella Typhimurium.
Open this publication in new window or tab >>The Selective Advantage of Replichore Balance in Salmonella Typhimurium.
(English)Manuscript (preprint) (Other academic)
Keyword
chromosome organization, inversions, rearrangements, experimental evolution
National Category
Microbiology Genetics Evolutionary Biology
Research subject
Biology with specialization in Microbiology
Identifiers
urn:nbn:se:uu:diva-332484 (URN)
Available from: 2017-10-27 Created: 2017-10-27 Last updated: 2017-10-29

Open Access in DiVA

fulltext(1290 kB)111 downloads
File information
File name FULLTEXT01.pdfFile size 1290 kBChecksum SHA-512
8251101f2591d04db32a1c87c4148ae15eb867636303d1ca86e35d0d5a1fc9c5711d405c745c6f60894682c9466e0fbc171d7940973bba343b529b11383ccbab
Type fulltextMimetype application/pdf
Buy this publication >>

Search in DiVA

By author/editor
Garmendia, Eva
By organisation
Department of Medical Biochemistry and Microbiology
MicrobiologyGeneticsEvolutionary Biology

Search outside of DiVA

GoogleGoogle Scholar
Total: 111 downloads
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

isbn
urn-nbn

Altmetric score

isbn
urn-nbn
Total: 510 hits
CiteExportLink to record
Permanent link

Direct link
Cite
Citation style
  • apa
  • ieee
  • modern-language-association-8th-edition
  • vancouver
  • Other style
More styles
Language
  • de-DE
  • en-GB
  • en-US
  • fi-FI
  • nn-NO
  • nn-NB
  • sv-SE
  • Other locale
More languages
Output format
  • html
  • text
  • asciidoc
  • rtf
v. 2.34-SNAPSHOT
|