Comparative analyses of Legionella species identifies genetic features of strains causing Legionnaires' disease

Gomez-Valero, L; Rusniok, C; Rolando, M; Neou, M; Dervins-Ravault, D; Demirtas, J; Rouy, Z; Moore, RJ; Chen, H; Petty, NK; Jarraud, S; Etienne, J; Steinert, M; Heuner, K; Gribaldo, S; Médigue, C; Glöckner, G; Hartland, EL; Buchrieser, C

Comparative analyses of Legionella species identifies genetic features of strains causing Legionnaires' disease

Gomez-Valero, L Rusniok, C Rolando, M Neou, M Dervins-Ravault, D Demirtas, J Rouy, Z Moore, RJ Chen, H Petty, NK

Jarraud, S Etienne, J Steinert, M Heuner, K Gribaldo, S Médigue, C Glöckner, G Hartland, EL Buchrieser, C

Permalink

Publication Type:: Journal Article
Citation:: Genome Biology, 2014, 15 (11)
Issue Date:: 2014-11-01

Open Access

Copyright Clearance Process

Recently Added
In Progress
Open Access

This item is open access.

Adobe PDF

Download Accepted Manuscript VersionAdobe PDF (2 MB)

View on publisher's site

View statistics

Full metadata record

Field	Value	Language
dc.contributor.author	Gomez-Valero, L	en_US
dc.contributor.author	Rusniok, C	en_US
dc.contributor.author	Rolando, M	en_US
dc.contributor.author	Neou, M	en_US
dc.contributor.author	Dervins-Ravault, D	en_US
dc.contributor.author	Demirtas, J	en_US
dc.contributor.author	Rouy, Z	en_US
dc.contributor.author	Moore, RJ	en_US
dc.contributor.author	Chen, H	en_US
dc.contributor.author	Petty, NK https://orcid.org/0000-0001-6528-9886	en_US
dc.contributor.author	Jarraud, S	en_US
dc.contributor.author	Etienne, J	en_US
dc.contributor.author	Steinert, M	en_US
dc.contributor.author	Heuner, K	en_US
dc.contributor.author	Gribaldo, S	en_US
dc.contributor.author	Médigue, C	en_US
dc.contributor.author	Glöckner, G	en_US
dc.contributor.author	Hartland, EL	en_US
dc.contributor.author	Buchrieser, C	en_US
dc.date.issued	2014-11-01	en_US
dc.identifier.citation	Genome Biology, 2014, 15 (11)	en_US
dc.identifier.issn	1474-7596	en_US
dc.identifier.uri	http://hdl.handle.net/10453/116068
dc.description.abstract	© 2014 Gomez-Valero et al. Background: The genus Legionella comprises over 60 species. However, L. pneumophila and L. longbeachae alone cause over 95% of Legionnaires' disease. To identify the genetic bases underlying the different capacities to cause disease we sequenced and compared the genomes of L. micdadei, L. hackeliae and L. fallonii (LLAP10), which are all rarely isolated from humans. Results: We show that these Legionella species possess different virulence capacities in amoeba and macrophages, correlating with their occurrence in humans. Our comparative analysis of 11 Legionella genomes belonging to five species reveals highly heterogeneous genome content with over 60% representing species-specific genes; these comprise a complete prophage in L. micdadei, the first ever identified in a Legionella genome. Mobile elements are abundant in Legionella genomes; many encode type IV secretion systems for conjugative transfer, pointing to their importance for adaptation of the genus. The Dot/Icm secretion system is conserved, although the core set of substrates is small, as only 24 out of over 300 described Dot/Icm effector genes are present in all Legionella species. We also identified new eukaryotic motifs including thaumatin, synaptobrevin or clathrin/coatomer adaptine like domains. Conclusions: Legionella genomes are highly dynamic due to a large mobilome mainly comprising type IV secretion systems, while a minority of core substrates is shared among the diverse species. Eukaryotic like proteins and motifs remain a hallmark of the genus Legionella. Key factors such as proteins involved in oxygen binding, iron storage, host membrane transport and certain Dot/Icm substrates are specific features of disease-related strains.	en_US
dc.relation.ispartof	Genome Biology	en_US
dc.relation.isbasedon	10.1186/s13059-014-0505-0	en_US
dc.subject.classification	Bioinformatics	en_US
dc.subject.mesh	Cell Line	en_US
dc.subject.mesh	Macrophages	en_US
dc.subject.mesh	Humans	en_US
dc.subject.mesh	Amoeba	en_US
dc.subject.mesh	Legionella pneumophila	en_US
dc.subject.mesh	Legionnaires' Disease	en_US
dc.subject.mesh	Disease Outbreaks	en_US
dc.subject.mesh	Species Specificity	en_US
dc.subject.mesh	Base Sequence	en_US
dc.subject.mesh	Interspersed Repetitive Sequences	en_US
dc.subject.mesh	Genome, Bacterial	en_US
dc.subject.mesh	Molecular Sequence Annotation	en_US
dc.subject.mesh	High-Throughput Nucleotide Sequencing	en_US
dc.title	Comparative analyses of Legionella species identifies genetic features of strains causing Legionnaires' disease	en_US
dc.type	Journal Article
utslib.citation.volume	11	en_US
utslib.citation.volume	15	en_US
utslib.for	110309 Infectious Diseases	en_US
utslib.for	060501 Bacteriology	en_US
utslib.for	05 Environmental Sciences	en_US
utslib.for	06 Biological Sciences	en_US
utslib.for	08 Information and Computing Sciences	en_US
pubs.embargo.period	Not known	en_US
pubs.organisational-group	/University of Technology Sydney
pubs.organisational-group	/University of Technology Sydney/Faculty of Science
pubs.organisational-group	/University of Technology Sydney/Strength - ithree - Institute of Infection, Immunity and Innovation
utslib.copyright.status	open_access
pubs.issue	11	en_US
pubs.publication-status	Published	en_US
pubs.volume	15	en_US

Abstract:

© 2014 Gomez-Valero et al. Background: The genus Legionella comprises over 60 species. However, L. pneumophila and L. longbeachae alone cause over 95% of Legionnaires' disease. To identify the genetic bases underlying the different capacities to cause disease we sequenced and compared the genomes of L. micdadei, L. hackeliae and L. fallonii (LLAP10), which are all rarely isolated from humans. Results: We show that these Legionella species possess different virulence capacities in amoeba and macrophages, correlating with their occurrence in humans. Our comparative analysis of 11 Legionella genomes belonging to five species reveals highly heterogeneous genome content with over 60% representing species-specific genes; these comprise a complete prophage in L. micdadei, the first ever identified in a Legionella genome. Mobile elements are abundant in Legionella genomes; many encode type IV secretion systems for conjugative transfer, pointing to their importance for adaptation of the genus. The Dot/Icm secretion system is conserved, although the core set of substrates is small, as only 24 out of over 300 described Dot/Icm effector genes are present in all Legionella species. We also identified new eukaryotic motifs including thaumatin, synaptobrevin or clathrin/coatomer adaptine like domains. Conclusions: Legionella genomes are highly dynamic due to a large mobilome mainly comprising type IV secretion systems, while a minority of core substrates is shared among the diverse species. Eukaryotic like proteins and motifs remain a hallmark of the genus Legionella. Key factors such as proteins involved in oxygen binding, iron storage, host membrane transport and certain Dot/Icm substrates are specific features of disease-related strains.

Please use this identifier to cite or link to this item:

http://hdl.handle.net/10453/116068