Project

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Genomic Islands and Bacterial Host Adaptation

English title Genomic Islands and Bacterial Host Adaptation
Applicant van der Meer Jan Roelof
Number 124711
Funding scheme Project funding
Research institution Département de Microbiologie Fondamentale Faculté de Biologie et de Médecine Université de Lausanne
Institution of higher education University of Lausanne - LA
Main discipline Experimental Microbiology
Start/End 01.09.2009 - 31.08.2012
Approved amount 431'882.00
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Keywords (8)

Evolution; Pseudomonas aeruginosa; Betaproteobacteria; Xenobiotic metabolism; intgrative and conjugative elements; Bacteria; Horizontal Gene Transfer; Genomic Islands

Lay Summary (English)

Lead
Lay summary
Rapid adaptation to changing conditions is one of the remarkable characteristics of bacterial life forms. Nowadays, de novo bacterial adaptation is mostly evident from acquired antibiotic resistance, new appearance of virulence traits, and spontaneous toxic compound removal. The past ten years have dramatically changed our view on the importance of horizontal gene transfer in adaptation through the availability of hundreds of bacterial genome sequences. In particular, it has become much more evident that adaptation is to a large extent determined by discrete regions of DNA that differ among closely related species. There has been a real revolution in our appreciation of the importance of transfer mechanisms resulting from chromosomally integrated mobile DNA elements, or 'genomic islands' (GEI), which frequently carry the functions for virulence factors, antibiotic resistances or toxic compound degradation. Despite their widespread occurrence in bacterial chromosomes, however, very little is known about the factors controlling GEI transfer, successful integration in the bacterial host and long-term evolutionary establishment. This project will focus on a model GEI, called ICEclc, which is representative for a large class of elements in primarily Gamma- and Betaproteobacteria. ICEclc is self-transferable to quite a few different recipient bacteria, and invokes a clear phenotype, and is thus is an excellent model for this research. ICEclc seems to establish itself without large fitness cost on the host, and hence, we are highly interested to know if and which specific molecular factors contribute to this success. Our working hypothesis is that ICEclc and other GEI have evolved specific mechanisms to ensure efficient transfer and subsequent establishment in the host, which contributes to their widespread distribution. The specific goals of the underlying proposal are, therefore, to discover, which factors encoded by ICEclc (as model for GEI more in general) give adaptive advantages to self-distribution and/or host establishment. In addition, we would like to study which host factors are important in this evolutionary adaptation. In particular we would like to follow host-ICEclc establishment after entry into the host and understand which changes are pivotal for successful host-GEI interaction.
Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
Comparative genome analysis of Pseudomonas knackmussii  B13, the first bacterium known to degrade chloroaromatic compounds Comparative genome analysis of P .  knackmussii  B13
Miyazaki Ryo, Bertelli Claire, Benaglio Paola, Canton Jonas, De Coi Nicoló, Gharib Walid H., Gjoksi Bebeka, Goesmann Alexander, Greub Gilbert, Harshman Keith, Linke Burkhard, Mikulic Josip, Mueller Linda, Nicolas Damien, Robinson-Rechavi Marc, Rivolta Carlo, Roggo Clémence, Roy Shantanu, Sentchilo Vladimir, Siebenthal Alexandra Von, Falquet Laurent, van der Meer Jan Roelof (2015), Comparative genome analysis of Pseudomonas knackmussii  B13, the first bacterium known to degrade chloroaromatic compounds Comparative genome analysis of P .  knackmussii  B13, in Environmental Microbiology, 17(1), 91-104.
Sequencing and characterizing the genome of Estrella lausannensis as an undergraduate project: training students and biological insights
Bertelli Claire, Aeby Sébastien, Chassot Bérénice, Clulow James, Hilfiker Olivier, Rappo Samuel, Ritzmann Sébastien, Schumacher Paolo, Terrettaz Céline, Benaglio Paola, Falquet Laurent, Farinelli Laurent, Gharib Walid H., Goesmann Alexander, Harshman Keith, Linke Burkhard, Miyazaki Ryo, Rivolta Carlo, Robinson-Rechavi Marc, van der Meer Jan Roelof, Greub Gilbert (2015), Sequencing and characterizing the genome of Estrella lausannensis as an undergraduate project: training students and biological insights, in Frontiers in Microbiology, 6, 101.
A New Large-DNA-Fragment Delivery System Based on Integrase Activity from an Integrative and Conjugative Element
Miyazaki R., van der Meer J. R. (2013), A New Large-DNA-Fragment Delivery System Based on Integrase Activity from an Integrative and Conjugative Element, in Applied and Environmental Microbiology, 79(14), 4440-4447.
Cell Differentiation to “Mating Bodies” Induced by an Integrating and Conjugative Element in Free-Living Bacteria
Reinhard Friedrich, Miyazaki Ryo, Pradervand Nicolas, van der Meer Jan Roelof (2013), Cell Differentiation to “Mating Bodies” Induced by an Integrating and Conjugative Element in Free-Living Bacteria, in Current Biology, 23(3), 255-259.
Cellular Variability of RpoS Expression Underlies Subpopulation Activation of an Integrative and Conjugative Element
Miyazaki Ryo, Minoia Marco, Pradervand Nicolas, Sulser Sandra, Reinhard Friedrich, van der Meer Jan Roelof (2012), Cellular Variability of RpoS Expression Underlies Subpopulation Activation of an Integrative and Conjugative Element, in PLoS Genetics, 8(7), e1002818-14.
How can a dual oriT system contribute to efficient transfer of an integrative and conjugative element?
Miyazaki R., van der Meer J. R. (2011), How can a dual oriT system contribute to efficient transfer of an integrative and conjugative element?, in Mobile Genetic Elements, 1, 82-84.
The clc element and related genomic islands in Proteobacteria.
Miyazaki R., Minoia M., Pradervand N., Sentchilo V., Sulser S., Reinhard F., van der Meer J. R. (2011), The clc element and related genomic islands in Proteobacteria., in Roberts A. P., Mullany P. (ed.), Landes Biosciences, Austin, TX, 36-51.
A dual functional origin of transfer in the ICEclc genomic island of Pseudomonas knackmussii B13
Miyazaki R., van der Meer J. R. (2010), A dual functional origin of transfer in the ICEclc genomic island of Pseudomonas knackmussii B13, in Mol Microbiol, 79, 743-758.
Transcriptome analysis of the mobile genome ICEclc in Pseudomonas knackmussii B13
Gaillard M., Pradervand N., Minoia M., Sentchilo V., Johnson D. R., van der Meer J. R. (2010), Transcriptome analysis of the mobile genome ICEclc in Pseudomonas knackmussii B13, in BMC Microbiol, 10, 153-167.
Genomic islands: tools of bacterial horizontal gene transfer and evolution
Juhas M., van der Meer J. R., Gaillard M., Harding R. M., Hood D. W., Crook D. W. (2009), Genomic islands: tools of bacterial horizontal gene transfer and evolution, in FEMS Microbiol Rev, 33, 376-393.
Intracellular excision and reintegration dynamics of the ICEclc genomic island of Pseudomonas knackmussii sp. strain B13
Sentchilo V., Czechowska K., Pradervand N., Minoia M., Miyazaki R., van der Meer J. R. (2009), Intracellular excision and reintegration dynamics of the ICEclc genomic island of Pseudomonas knackmussii sp. strain B13, in Mol Microbiol, 72, 1293-1306.

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
ISME 13. International Symposium on Microbial Ecology. Individual talk The secret life of ICE 20.08.2012 Copenhagen, Denmark Miyazaki Ryo; van der Meer Jan Roelof; Sulser Sandra Daniela;
2nd Molecular Microbiology symposium Talk given at a conference Origins of replication of ICEclc 25.04.2012 Würzburg, Germany van der Meer Jan Roelof;
FEMS 2011 Conference on prokaryotic microbiology. Poster Regulation of bistable ICEclc transfer in Pseudomonas knackmussii B13 26.06.2011 Geneva, Switzerland Miyazaki Ryo; Sulser Sandra Daniela;
Institut Pasteur. Individual talk Stochasticity and bistability in genomic island transfer in Pseudomonas. 29.01.2010 Paris, France van der Meer Jan Roelof;
Pseudomonas Conference. Talk given at a conference Eating junk: the versatile ways of evolution in Pseudomonas 28.01.2010 Milan, Italy van der Meer Jan Roelof;


Self-organised

Title Date Place
Microbial individuality Minisymposium DMF 12.11.2010 Lausanne, Switzerland
Prokagenomics 05.10.2009 Göttingen, Germany

Awards

Title Year
DC White Young Investigator Award to Friedrich Reinhard 2010

Associated projects

Number Title Start Funding scheme
144141 Genomic Islands and Bacterial Host Adaptation 01.10.2012 Project funding
108199 Horizontal gene transfer of genomic islands in Beta- and Gammaproteobacteria 01.10.2005 Project funding

Abstract

IntroductionRapid adaptation to changing conditions is one of the remarkable characteristics of bacterial life forms. Nowadays, de novo bacterial adaptation is mostly evident from acquired antibiotic resistance, new appearance of virulence traits, and spontaneous toxic compound removal. The past ten years have dramatically changed our view on the importance of horizontal gene transfer in adaptation through the availability of hundreds of bacterial genome sequences. In particular, it has become much more evident that adaptation is to a large extent determined by discrete regions of DNA (up to several hundred kilobase-pairs) that differ among closely related species. There has been a real revolution in our appreciation of the importance of transfer mechanisms resulting from chromosomally integrated mobile DNA elements, or ‘genomic islands’ (GEI), which frequently carry the functions for virulence factors, antibiotic resistances or toxic compound degradation. Despite their widespread occurrence in bacterial chromosomes, however, very little is known about the factors controlling GEI transfer, successful integration in the bacterial host and long-term evolutionary establishment. Working hypothesis and project aimsOur group has been studying a model GEI, called ICEclc, which is representative for a large class of elements in primarly Gamma- and Betaproteobacteria, among which Pseudomonas aeruginosa and Burkholderia. ICEclc is self-transferable to quite a few different recipient bacteria, and invokes a clear phenotype, and is thus is an excellent model for this research. ICEclc seems to establish itself without large fitness cost on the host, and hence, we are highly interested to know if and which specific molecular factors contribute to this success. Our working hypothesis is that ICEclc and other GEI have evolved specific mechanisms to ensure efficient transfer and subsequent establishment in the host, which contributes to their widespread distribution.The specific goals of the underlying proposal are, therefore, to discover, which factors encoded by ICEclc (as model for GEI more in general) give adaptive advantages to self-distribution and/or host establishment. In addition, we would like to study which host factors are important in this evolutionary adaptation. In particular we would like to follow host-ICEclc establishment from the earliest moment after transfer to long-term (1000 generations) co-occurrence, and understand which changes are pivotal for successful host-GEI interaction. Methods and experimental strategiesThe research will to a large extent be based on (i) transcriptome studies of ICEclc in different hosts and of the host itself by array hybridizations and single-cell reporter gene expression, to unravel expression patterns and specific functions in the ‘process of establishment’, and (ii) on the discovery of adaptive and control functions encoded by ICEclc (and if possible, host) via transposon mutagenesis and flow cytometric-based screening procedures, followed by genetic and molecular studies. Expected impactWe expect to make key fundamental evolutionary discoveries in the factors controlling GEI distribution and establishment in bacterial hosts, by using ICEclc of Pseudomonas knackmussii as model. This can help to understand why GEIs are so successful in colonizing bacterial host and provide the host with potential to adapt to adverse conditions. Our research may have two important longer term consequences, (i) understanding the mechanisms and conditions promoting fast formation of virulence and pathogenicity traits via GEI, and (ii) appreciating and perhaps manipulating conditions leading to rapid bacterial adaptation to detoxify environmental pollutants.
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