Dataset Information

Distribution of Secretion Systems in the Genus Legionella and Its Correlation with Pathogenicity.

ABSTRACT: The genus Legionella comprises over 60 species, which are important human pathogens. Secretion systems in Legionella pneumophila have been studied extensively because of the essential role of protein secretion in bacterial infection. However, there are few reports describing the secretion systems in non-L. pneumophila species. In this study, we analyzed the distribution of secretion systems in L. pneumophila and 18 species of non-L. pneumophila based on whole genome sequences. A total of 74 whole genome sequences from 19 species of Legionella were analyzed. Type II and IVB secretion systems were detected in all Legionella strains, but the type I secretion systems was restricted to L. pneumophila. The type IVA secretion system was randomly distributed among different species. Furthermore, we found the type VI secretion system in three non-L. pneumophila strains (Legionella cherrii DSM 19213, Legionella dumoffii Tex-KL, and Legionella gormanii ATCC 33297). In population structure analysis, L. pneumophila formed a conservative cluster and was located at the terminal of the evolutionary tree. At the same time, L. pneumophila, especially eight clone groups (named MCGG1-MCGG8), showed higher intracellular growth ability than non-L. pneumophila species. These results suggest that L. pneumophila has acquired additional secretion systems during evolution, resulting in increased pathogenicity.

SUBMITTER: Qin T

PROVIDER: S-EPMC5348487 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Distribution of Secretion Systems in the Genus Legionella and Its Correlation with Pathogenicity.

Qin Tian T Zhou Haijian H Ren Hongyu H Liu Wenbin W

Frontiers in microbiology 20170314

The genus Legionella comprises over 60 species, which are important human pathogens. Secretion systems in Legionella pneumophila have been studied extensively because of the essential role of protein secretion in bacterial infection. However, there are few reports describing the secretion systems in non-L. pneumophila species. In this study, we analyzed the distribution of secretion systems in L. pneumophila and 18 species of non-L. pneumophila based on whole g ...[more]

PMID: 28352254

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Project description:Type 1 secretion systems (T1SSs) are broadly distributed among bacteria and translocate effectors with diverse function across the bacterial cell membrane. Legionella pneumophila, the species most commonly associated with Legionellosis, encodes a T1SS at the lssXYZABD locus which is responsible for the secretion of the virulence factor RtxA. Many investigations have failed to detect lssD, the gene encoding the membrane fusion protein of the RtxA T1SS, in non-pneumophila Legionella, which has led to the assumption that this system is a virulence factor exclusively possessed by L. pneumophila. Here we discovered RtxA and its associated T1SS in a novel Legionella taurinensis strain, leading us to question whether this system may be more widespread than previously thought. Through a bioinformatic analysis of publicly available data, we classified and determined the distribution of four T1SSs including the RtxA T1SS and four novel T1SSs among diverse Legionella spp. The ABC transporter of the novel Legionella T1SS Legionella repeat protein secretion system shares structural similarity to those of diverse T1SS families, including the alkaline protease T1SS in Pseudomonas aeruginosa. The Legionella bacteriocin (1-3) secretion systems T1SSs are novel putative bacteriocin transporting T1SSs as their ABC transporters include C-39 peptidase domains in their N-terminal regions, with LB2SS and LB3SS likely constituting a nitrile hydratase leader peptide transport T1SSs. The LB1SS is more closely related to the colicin V T1SS in Escherichia coli. Of 45 Legionella spp. whole genomes examined, 19 (42%) were determined to possess lssB and lssD homologs. Of these 19, only 7 (37%) are known pathogens. There was no difference in the proportions of disease associated and non-disease associated species that possessed the RtxA T1SS (p = 0.4), contrary to the current consensus regarding the RtxA T1SS. These results draw into question the nature of RtxA and its T1SS as a singular virulence factor. Future studies should investigate mechanistic explanations for the association of RtxA with virulence.

Project description:Legionella encodes multiple classes of Type IV Secretion Systems (T4SSs), including the Dot/Icm protein secretion system that is essential for intracellular multiplication in amoebal and human hosts. Other T4SSs not essential for virulence are thought to facilitate the acquisition of niche-specific adaptation genes including the numerous effector genes that are a hallmark of this genus. Previously, we identified two novel gene clusters in the draft genome of Legionella pneumophila strain 130b that encode homologues of a subtype of T4SS, the genomic island-associated T4SS (GI-T4SS), usually associated with integrative and conjugative elements (ICE). In this study, we performed genomic analyses of 14 homologous GI-T4SS clusters found in eight publicly available Legionella genomes and show that this cluster is unusually well conserved in a region of high plasticity. Phylogenetic analyses show that Legionella GI-T4SSs are substantially divergent from other members of this subtype of T4SS and represent a novel clade of GI-T4SSs only found in this genus. The GI-T4SS was found to be under purifying selection, suggesting it is functional and may play an important role in the evolution and adaptation of Legionella. Like other GI-T4SSs, the Legionella clusters are also associated with ICEs, but lack the typical integration and replication modules of related ICEs. The absence of complete replication and DNA pre-processing modules, together with the presence of Legionella-specific regulatory elements, suggest the Legionella GI-T4SS-associated ICE is unique and may employ novel mechanisms of regulation, maintenance and excision. The Legionella GI-T4SS cluster was found to be associated with several cargo genes, including numerous antibiotic resistance and virulence factors, which may confer a fitness benefit to the organism. The in-silico characterisation of this new T4SS furthers our understanding of the diversity of secretion systems involved in the frequent horizontal gene transfers that allow Legionella to adapt to and exploit diverse environmental niches.

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Dataset Information

Distribution of Secretion Systems in the Genus Legionella and Its Correlation with Pathogenicity.

Publications

Distribution of Secretion Systems in the Genus <i>Legionella</i> and Its Correlation with Pathogenicity.

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