Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2011 Nov 1:12:536.
doi: 10.1186/1471-2164-12-536.

Extensive recombination events and horizontal gene transfer shaped the Legionella pneumophila genomes

Affiliations

Extensive recombination events and horizontal gene transfer shaped the Legionella pneumophila genomes

Laura Gomez-Valero et al. BMC Genomics. .

Abstract

Background: Legionella pneumophila is an intracellular pathogen of environmental protozoa. When humans inhale contaminated aerosols this bacterium may cause a severe pneumonia called Legionnaires' disease. Despite the abundance of dozens of Legionella species in aquatic reservoirs, the vast majority of human disease is caused by a single serogroup (Sg) of a single species, namely L. pneumophila Sg1. To get further insights into genome dynamics and evolution of Sg1 strains, we sequenced strains Lorraine and HL 0604 1035 (Sg1) and compared them to the available sequences of Sg1 strains Paris, Lens, Corby and Philadelphia, resulting in a comprehensive multigenome analysis.

Results: We show that L. pneumophila Sg1 has a highly conserved and syntenic core genome that comprises the many eukaryotic like proteins and a conserved repertoire of over 200 Dot/Icm type IV secreted substrates. However, recombination events and horizontal gene transfer are frequent. In particular the analyses of the distribution of nucleotide polymorphisms suggests that large chromosomal fragments of over 200 kbs are exchanged between L. pneumophila strains and contribute to the genome dynamics in the natural population. The many secretion systems present might be implicated in exchange of these fragments by conjugal transfer. Plasmids also play a role in genome diversification and are exchanged among strains and circulate between different Legionella species.

Conclusion: Horizontal gene transfer among bacteria and from eukaryotes to L. pneumophila as well as recombination between strains allows different clones to evolve into predominant disease clones and others to replace them subsequently within relatively short periods of time.

PubMed Disclaimer

Figures

Figure 1
Figure 1
Shared and specific gene content of 6 L. pneumophila genomes. Each petal represents a genome with an associated color. The number in the center of the diagram represents the orthologous genes shared by all the genomes. The number inside of each individual petal corresponds to the specific genes of each genome with non-orthologous genes in any of the other genomes. The small circles inside of each petal represent the percentage of shared genes (total number divided by the number of genes in the smallest genome) between the genome of this petal and the genome represented by the color of the small circle. Yellow circle inside orange petal means that there are 88% of genes shared among Corby and Lorraine.
Figure 2
Figure 2
Schematic representation of F-type IV secretion systems (T4SSA) for conjugal DNA transfer of L. pneumophila. In green and orange, tra and trb genes respectively. L. long, Legionella longbeachae; P, Plasmid; C, Chromosome; ycaO, Protein of unknown function with a YcaO like-domain; tfu, Protein of unknown function with a TfuA domain; pil, Pilus assembly protein precursor; t, transposase; E. coli, Escherichia coli; R. beeli, Rickettsia beeli; pha, Phage repressor; int, integrase; pin, site-specific DNA recombinase e14 prophage; R; repeat. Yellow squares represent flanking repeats, with length and percentage of identity between repeats in parenthesis. tRNAs, position in the genome in parenthesis.
Figure 3
Figure 3
Schematic representation of P-type IV secretion systems (T4SSA) for conjugal DNA transfer of L. pneumophila. In green and orange, tra and trb genes respectively. L. long, Legionella longbeachae; P, Plasmid; C, Chromosome; ?, Protein of unknown function; A. tumefaciens, Agrobacterium tumefaciens; P. aeruginosa, Pseudomonas aeruginosa; t, transposase; pha, Phage repressor; Int, integrase; Pseudogenes are in discontinues squares; Yellow squares represent flanking repeats, with length and percentage of identity between repeats in parenthesis. tRNAs, their position in the genome is given in parenthesis.
Figure 4
Figure 4
Schematic representation of the repeat regions present in the rtxA gene of L. pneumophila. Colored squares represent repeated sequences where the same color corresponds to the same type of repeat. Discontinues lines indicate that the exact number of repeats has not been defined.
Figure 5
Figure 5
Phylogenetic relationships of the 6 L. pneumophila strains analyzed. a) Neighbor-net constructed from a concatenation of 31 genes from 6 L. pneumophila strains under a GTR model, with associated bootstrap values. b) Likelihood tree topology of L. pneumophila strains and the outgroup L. longbeachae based on orthologous genes present in all strains/species concatenated.
Figure 6
Figure 6
Distribution of single-nucleotide polymorphisms (SNPs) along 330 kb of the genomes of L. pneumophila HL 0604 1035, Philadelphia and Lorraine. The number of SNPs (y axis) is plotted according to the position of the corresponding 500 bp fragment on the strain Paris chromosome (x axis). A straight blue line indicates 0 polymorphism between the two strains. Numbers on the scale bar indicate the percentage of polymorphism. The green (+ strand) and red (- strand) lines depict the corresponding genes.

References

    1. Fliermans CB, Cherry WB, Orrison LH, Smith SJ, Tison DL, Pope DH. Ecological distribution of Legionella pneumophila. Appl Environ Microbiol. 1981;41(1):9–16. - PMC - PubMed
    1. Fields BS. The molecular ecology of Legionellae. Trends Microbiol. 1996;4(7):286–290. doi: 10.1016/0966-842X(96)10041-X. - DOI - PubMed
    1. Rowbotham TJ. Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol. 1980;33(12):1179–1183. doi: 10.1136/jcp.33.12.1179. - DOI - PMC - PubMed
    1. Cazalet C, Rusniok C, Bruggemann H, Zidane N, Magnier A, Ma L, Tichit M, Jarraud S, Bouchier C, Vandenesch F, Kunst F, Etienne J, Glaser P, Buchrieser C. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet. 2004;36(11):1165–1173. doi: 10.1038/ng1447. - DOI - PubMed
    1. Hubber A, Roy CR. Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol. 2010;26:261–283. doi: 10.1146/annurev-cellbio-100109-104034. - DOI - PubMed

Publication types

LinkOut - more resources