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Parallel evolution of a type IV secretion system in radiating lineages of the host-restricted bacterial pathogen Bartonella.

Engel P, Salzburger W, Liesch M, Chang CC, Maruyama S, Lanz C, Calteau A, Lajus A, Médigue C, Schuster SC, Dehio C - PLoS Genet. (2011)

Bottom Line: Whereas most Beps maintained their ancestral domain constitution, strikingly, a novel type of effector protein emerged convergently in both lineages.The parallel molecular evolution of the VirB/Bep system displays a striking example of a key innovation involved in independent adaptive processes and the emergence of bacterial pathogens.Furthermore, our study highlights the remarkable evolvability of T4SSs and their effector proteins, explaining their broad application in bacterial interactions with the environment.

View Article: PubMed Central - PubMed

Affiliation: Focal Area Infection Biology, Biozentrum, University of Basel, Basel, Switzerland.

ABSTRACT
Adaptive radiation is the rapid origination of multiple species from a single ancestor as the result of concurrent adaptation to disparate environments. This fundamental evolutionary process is considered to be responsible for the genesis of a great portion of the diversity of life. Bacteria have evolved enormous biological diversity by exploiting an exceptional range of environments, yet diversification of bacteria via adaptive radiation has been documented in a few cases only and the underlying molecular mechanisms are largely unknown. Here we show a compelling example of adaptive radiation in pathogenic bacteria and reveal their genetic basis. Our evolutionary genomic analyses of the α-proteobacterial genus Bartonella uncover two parallel adaptive radiations within these host-restricted mammalian pathogens. We identify a horizontally-acquired protein secretion system, which has evolved to target specific bacterial effector proteins into host cells as the evolutionary key innovation triggering these parallel adaptive radiations. We show that the functional versatility and adaptive potential of the VirB type IV secretion system (T4SS), and thereby translocated Bartonella effector proteins (Beps), evolved in parallel in the two lineages prior to their radiations. Independent chromosomal fixation of the virB operon and consecutive rounds of lineage-specific bep gene duplications followed by their functional diversification characterize these parallel evolutionary trajectories. Whereas most Beps maintained their ancestral domain constitution, strikingly, a novel type of effector protein emerged convergently in both lineages. This resulted in similar arrays of host cell-targeted effector proteins in the two lineages of Bartonella as the basis of their independent radiation. The parallel molecular evolution of the VirB/Bep system displays a striking example of a key innovation involved in independent adaptive processes and the emergence of bacterial pathogens. Furthermore, our study highlights the remarkable evolvability of T4SSs and their effector proteins, explaining their broad application in bacterial interactions with the environment.

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Phylogeny of Bartonella based on a genome-wide dataset.Maximum likelihood analysis using an alignment of 478 genes (515,751 nt) of ten sequenced Bartonella species (indicated by bold and color type) and Brucella abortus. Based on sequence data from rpoB, gltA, ribC, and groEL genes, additional Bartonella species were included in the analysis. Numbers above the branches represent maximum likelihood bootstraps (100 replicates); numbers below represent Bayesian posterior probabilities. Values ≥80% are shown. Lineages harboring the VirB T4SS [16] are shaded in gray; the primary mammalian hosts are indicated for each species. Phylogenetic trees inferred from either the genomic data set excluding non-sequenced bartonellae or the sequences from only rpoB, gltA, ribC, and groEL genes revealed the same four lineages for the Bartonella ingroup (Figure S1). Estimates of average evolutionary divergence over sequence pairs within lineages and between lineages are presented in Table S1. l1, lineage 1.
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pgen-1001296-g001: Phylogeny of Bartonella based on a genome-wide dataset.Maximum likelihood analysis using an alignment of 478 genes (515,751 nt) of ten sequenced Bartonella species (indicated by bold and color type) and Brucella abortus. Based on sequence data from rpoB, gltA, ribC, and groEL genes, additional Bartonella species were included in the analysis. Numbers above the branches represent maximum likelihood bootstraps (100 replicates); numbers below represent Bayesian posterior probabilities. Values ≥80% are shown. Lineages harboring the VirB T4SS [16] are shaded in gray; the primary mammalian hosts are indicated for each species. Phylogenetic trees inferred from either the genomic data set excluding non-sequenced bartonellae or the sequences from only rpoB, gltA, ribC, and groEL genes revealed the same four lineages for the Bartonella ingroup (Figure S1). Estimates of average evolutionary divergence over sequence pairs within lineages and between lineages are presented in Table S1. l1, lineage 1.

Mentions: Genome sequencing by 454-pyrosequencing resulted in an average sequence coverage of >35x. The single chromosome of the completely assembled genome of Bc was found to be 1,522,743 bp in size and thus belongs to the smaller genomes of Bartonella (Table 1). The draft genomes of Br, BAR15, B1-1C, and Bs consist of 13 to 19 contigs with total genome sizes similar to the one of Bc. On average, 99% of all 454-sequencing reads were assembled into the analyzed 13 to 19 contigs indicating that our draft genomes did not miss essential sequence data for subsequent analysis. Genomic features of the strains used in this study are summarized in Table 1.


Parallel evolution of a type IV secretion system in radiating lineages of the host-restricted bacterial pathogen Bartonella.

Engel P, Salzburger W, Liesch M, Chang CC, Maruyama S, Lanz C, Calteau A, Lajus A, Médigue C, Schuster SC, Dehio C - PLoS Genet. (2011)

Phylogeny of Bartonella based on a genome-wide dataset.Maximum likelihood analysis using an alignment of 478 genes (515,751 nt) of ten sequenced Bartonella species (indicated by bold and color type) and Brucella abortus. Based on sequence data from rpoB, gltA, ribC, and groEL genes, additional Bartonella species were included in the analysis. Numbers above the branches represent maximum likelihood bootstraps (100 replicates); numbers below represent Bayesian posterior probabilities. Values ≥80% are shown. Lineages harboring the VirB T4SS [16] are shaded in gray; the primary mammalian hosts are indicated for each species. Phylogenetic trees inferred from either the genomic data set excluding non-sequenced bartonellae or the sequences from only rpoB, gltA, ribC, and groEL genes revealed the same four lineages for the Bartonella ingroup (Figure S1). Estimates of average evolutionary divergence over sequence pairs within lineages and between lineages are presented in Table S1. l1, lineage 1.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3037411&req=5

pgen-1001296-g001: Phylogeny of Bartonella based on a genome-wide dataset.Maximum likelihood analysis using an alignment of 478 genes (515,751 nt) of ten sequenced Bartonella species (indicated by bold and color type) and Brucella abortus. Based on sequence data from rpoB, gltA, ribC, and groEL genes, additional Bartonella species were included in the analysis. Numbers above the branches represent maximum likelihood bootstraps (100 replicates); numbers below represent Bayesian posterior probabilities. Values ≥80% are shown. Lineages harboring the VirB T4SS [16] are shaded in gray; the primary mammalian hosts are indicated for each species. Phylogenetic trees inferred from either the genomic data set excluding non-sequenced bartonellae or the sequences from only rpoB, gltA, ribC, and groEL genes revealed the same four lineages for the Bartonella ingroup (Figure S1). Estimates of average evolutionary divergence over sequence pairs within lineages and between lineages are presented in Table S1. l1, lineage 1.
Mentions: Genome sequencing by 454-pyrosequencing resulted in an average sequence coverage of >35x. The single chromosome of the completely assembled genome of Bc was found to be 1,522,743 bp in size and thus belongs to the smaller genomes of Bartonella (Table 1). The draft genomes of Br, BAR15, B1-1C, and Bs consist of 13 to 19 contigs with total genome sizes similar to the one of Bc. On average, 99% of all 454-sequencing reads were assembled into the analyzed 13 to 19 contigs indicating that our draft genomes did not miss essential sequence data for subsequent analysis. Genomic features of the strains used in this study are summarized in Table 1.

Bottom Line: Whereas most Beps maintained their ancestral domain constitution, strikingly, a novel type of effector protein emerged convergently in both lineages.The parallel molecular evolution of the VirB/Bep system displays a striking example of a key innovation involved in independent adaptive processes and the emergence of bacterial pathogens.Furthermore, our study highlights the remarkable evolvability of T4SSs and their effector proteins, explaining their broad application in bacterial interactions with the environment.

View Article: PubMed Central - PubMed

Affiliation: Focal Area Infection Biology, Biozentrum, University of Basel, Basel, Switzerland.

ABSTRACT
Adaptive radiation is the rapid origination of multiple species from a single ancestor as the result of concurrent adaptation to disparate environments. This fundamental evolutionary process is considered to be responsible for the genesis of a great portion of the diversity of life. Bacteria have evolved enormous biological diversity by exploiting an exceptional range of environments, yet diversification of bacteria via adaptive radiation has been documented in a few cases only and the underlying molecular mechanisms are largely unknown. Here we show a compelling example of adaptive radiation in pathogenic bacteria and reveal their genetic basis. Our evolutionary genomic analyses of the α-proteobacterial genus Bartonella uncover two parallel adaptive radiations within these host-restricted mammalian pathogens. We identify a horizontally-acquired protein secretion system, which has evolved to target specific bacterial effector proteins into host cells as the evolutionary key innovation triggering these parallel adaptive radiations. We show that the functional versatility and adaptive potential of the VirB type IV secretion system (T4SS), and thereby translocated Bartonella effector proteins (Beps), evolved in parallel in the two lineages prior to their radiations. Independent chromosomal fixation of the virB operon and consecutive rounds of lineage-specific bep gene duplications followed by their functional diversification characterize these parallel evolutionary trajectories. Whereas most Beps maintained their ancestral domain constitution, strikingly, a novel type of effector protein emerged convergently in both lineages. This resulted in similar arrays of host cell-targeted effector proteins in the two lineages of Bartonella as the basis of their independent radiation. The parallel molecular evolution of the VirB/Bep system displays a striking example of a key innovation involved in independent adaptive processes and the emergence of bacterial pathogens. Furthermore, our study highlights the remarkable evolvability of T4SSs and their effector proteins, explaining their broad application in bacterial interactions with the environment.

Show MeSH
Related in: MedlinePlus