Limits...
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 - Genome Biol. (2014)

Bottom Line: 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.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.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.

View Article: PubMed Central - PubMed

ABSTRACT

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.

Show MeSH

Related in: MedlinePlus

Phylogenetic tree of sixLegionellaspecies and sevenL. pneumophilastrains and their shared Dot/Icm substrates. Neighbor-joining tree based on the concatenation of 816 protein-coding genes from 11 Legionella genomes. C. burnetii was used as out-group. The tree was constructed using MEGA and JTT as model of evolution. The values above nodes indicate the bootstrap values. The values in blue circles represent the number of Dot/Icm substrates shared by the species in the corresponding cluster, suggesting that they were present in the common ancestor. The values inside blues squares are the number of Dot/Icm substrates shared between L. pneumophila strains and the remaining species (for example, the species L. micdadei and L. pneumophila share 33 Dot/Icm substrates).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC4256840&req=5

Fig3: Phylogenetic tree of sixLegionellaspecies and sevenL. pneumophilastrains and their shared Dot/Icm substrates. Neighbor-joining tree based on the concatenation of 816 protein-coding genes from 11 Legionella genomes. C. burnetii was used as out-group. The tree was constructed using MEGA and JTT as model of evolution. The values above nodes indicate the bootstrap values. The values in blue circles represent the number of Dot/Icm substrates shared by the species in the corresponding cluster, suggesting that they were present in the common ancestor. The values inside blues squares are the number of Dot/Icm substrates shared between L. pneumophila strains and the remaining species (for example, the species L. micdadei and L. pneumophila share 33 Dot/Icm substrates).

Mentions: To establish a whole genome-based phylogeny of these Legionella species we used either 29 housekeeping genes or 816 orthologous genes shared among the 11 Legionella strains analyzed. Coxiella burnetii was used as outgroup. Phylogenetic reconstructions using either the nucleotide or the amino acid sequences gave the same tree topology for the different species. In contrast, the tree topology of the L. pneumophila strains was different depending on the data set or the phylogenetic method used, probably due to the high recombination rate of this species [12,22]. Our phylogenetic analyses showed that L. pneumophila, L. fallonii and L. longbeachae group together, with L. fallonii being phylogenetically the closest to L. pneumophila. L. micdadei and L. hackeliae formed a second cluster (Figure 3). Except for the place of L. fallonii, this is in agreement with previous phylogenies of the genus Legionella [23,24]. In previous work L. pneumophila was described as phylogenetically closer to L. longbeachae than to L. fallonii [25] or L. fallonii closer to L. longbeachae than to L. pneumophila [26]. However, these studies are based on 16S RNA sequences and bootstrap values associated with the corresponding nodes to evaluate its statistical support are not provided.Figure 3


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 - Genome Biol. (2014)

Phylogenetic tree of sixLegionellaspecies and sevenL. pneumophilastrains and their shared Dot/Icm substrates. Neighbor-joining tree based on the concatenation of 816 protein-coding genes from 11 Legionella genomes. C. burnetii was used as out-group. The tree was constructed using MEGA and JTT as model of evolution. The values above nodes indicate the bootstrap values. The values in blue circles represent the number of Dot/Icm substrates shared by the species in the corresponding cluster, suggesting that they were present in the common ancestor. The values inside blues squares are the number of Dot/Icm substrates shared between L. pneumophila strains and the remaining species (for example, the species L. micdadei and L. pneumophila share 33 Dot/Icm substrates).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4256840&req=5

Fig3: Phylogenetic tree of sixLegionellaspecies and sevenL. pneumophilastrains and their shared Dot/Icm substrates. Neighbor-joining tree based on the concatenation of 816 protein-coding genes from 11 Legionella genomes. C. burnetii was used as out-group. The tree was constructed using MEGA and JTT as model of evolution. The values above nodes indicate the bootstrap values. The values in blue circles represent the number of Dot/Icm substrates shared by the species in the corresponding cluster, suggesting that they were present in the common ancestor. The values inside blues squares are the number of Dot/Icm substrates shared between L. pneumophila strains and the remaining species (for example, the species L. micdadei and L. pneumophila share 33 Dot/Icm substrates).
Mentions: To establish a whole genome-based phylogeny of these Legionella species we used either 29 housekeeping genes or 816 orthologous genes shared among the 11 Legionella strains analyzed. Coxiella burnetii was used as outgroup. Phylogenetic reconstructions using either the nucleotide or the amino acid sequences gave the same tree topology for the different species. In contrast, the tree topology of the L. pneumophila strains was different depending on the data set or the phylogenetic method used, probably due to the high recombination rate of this species [12,22]. Our phylogenetic analyses showed that L. pneumophila, L. fallonii and L. longbeachae group together, with L. fallonii being phylogenetically the closest to L. pneumophila. L. micdadei and L. hackeliae formed a second cluster (Figure 3). Except for the place of L. fallonii, this is in agreement with previous phylogenies of the genus Legionella [23,24]. In previous work L. pneumophila was described as phylogenetically closer to L. longbeachae than to L. fallonii [25] or L. fallonii closer to L. longbeachae than to L. pneumophila [26]. However, these studies are based on 16S RNA sequences and bootstrap values associated with the corresponding nodes to evaluate its statistical support are not provided.Figure 3

Bottom Line: 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.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.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.

View Article: PubMed Central - PubMed

ABSTRACT

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.

Show MeSH
Related in: MedlinePlus