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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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Genomic organization of the virB T4SS and bep gene loci in the two radiating lineages.Synteny plot of Bc (lineage 3) and Bq (lineage 4) generated in MaGe [58] and genetic organization of the virB T4SS loci. Syntenic relationships comprising at least five genes are indicated by violet and blue lines for genes found on the same or the opposite strand, respectively. The genomic integration sites of virB loci are indicated. Additional bep loci in lineage 3 are marked by arrows. For the depicted genomic loci, orthologous genes are connected via gray boxes. For bep genes, connections are drawn if they belong to the same Bep clade (Figure 4) or if they are top blast hits of one another. The glutamine syntethase I gene (glnA) and its fragments which are flanking the two inverted virB T4SS copies are colored in green. The fragments are indicated by an asterisk.
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pgen-1001296-g003: Genomic organization of the virB T4SS and bep gene loci in the two radiating lineages.Synteny plot of Bc (lineage 3) and Bq (lineage 4) generated in MaGe [58] and genetic organization of the virB T4SS loci. Syntenic relationships comprising at least five genes are indicated by violet and blue lines for genes found on the same or the opposite strand, respectively. The genomic integration sites of virB loci are indicated. Additional bep loci in lineage 3 are marked by arrows. For the depicted genomic loci, orthologous genes are connected via gray boxes. For bep genes, connections are drawn if they belong to the same Bep clade (Figure 4) or if they are top blast hits of one another. The glutamine syntethase I gene (glnA) and its fragments which are flanking the two inverted virB T4SS copies are colored in green. The fragments are indicated by an asterisk.

Mentions: To further assess the role of the VirB T4SS for the independent adaptive radiations of Bartonella, we compared the chromosomal organization of the VirB and effector protein-encoding genes of the two lineages. Remarkably, our analysis uncovered independent evolutionary scenarios for the chromosomal incorporation of this horizontally acquired trait. In the genomes of lineage 4 (Bg, Bh, Bq, and Bt), the virB T4SS genes, virB2-virB11 and the coupling protein gene virD4, are encoded at the same chromosomal location (Figure 3, Figure S4). Also, the bep genes are encoded in this region. In contrast, the genome sequences of lineage 3 (Bc, Br, BAR15, and B1-1C) revealed marked differences in organization, copy number, and chromosomal localization of the genes encoding the VirB T4SS. In the completely assembled genome of Bc, we found three copies of the virB2-virB10 genes encoded at two different chromosomal locations (Figure 3, Figure S4). Two copies are encoded at the same locus and belong to inverted repeats of ∼10kb. They are separated by several bep genes and the gene virD4. A third copy of the virB2-virB10 cluster including an additional bep gene is encoded in another genomic region highly conserved across different Bartonella lineages (Figure 3).


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)

Genomic organization of the virB T4SS and bep gene loci in the two radiating lineages.Synteny plot of Bc (lineage 3) and Bq (lineage 4) generated in MaGe [58] and genetic organization of the virB T4SS loci. Syntenic relationships comprising at least five genes are indicated by violet and blue lines for genes found on the same or the opposite strand, respectively. The genomic integration sites of virB loci are indicated. Additional bep loci in lineage 3 are marked by arrows. For the depicted genomic loci, orthologous genes are connected via gray boxes. For bep genes, connections are drawn if they belong to the same Bep clade (Figure 4) or if they are top blast hits of one another. The glutamine syntethase I gene (glnA) and its fragments which are flanking the two inverted virB T4SS copies are colored in green. The fragments are indicated by an asterisk.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3037411&req=5

pgen-1001296-g003: Genomic organization of the virB T4SS and bep gene loci in the two radiating lineages.Synteny plot of Bc (lineage 3) and Bq (lineage 4) generated in MaGe [58] and genetic organization of the virB T4SS loci. Syntenic relationships comprising at least five genes are indicated by violet and blue lines for genes found on the same or the opposite strand, respectively. The genomic integration sites of virB loci are indicated. Additional bep loci in lineage 3 are marked by arrows. For the depicted genomic loci, orthologous genes are connected via gray boxes. For bep genes, connections are drawn if they belong to the same Bep clade (Figure 4) or if they are top blast hits of one another. The glutamine syntethase I gene (glnA) and its fragments which are flanking the two inverted virB T4SS copies are colored in green. The fragments are indicated by an asterisk.
Mentions: To further assess the role of the VirB T4SS for the independent adaptive radiations of Bartonella, we compared the chromosomal organization of the VirB and effector protein-encoding genes of the two lineages. Remarkably, our analysis uncovered independent evolutionary scenarios for the chromosomal incorporation of this horizontally acquired trait. In the genomes of lineage 4 (Bg, Bh, Bq, and Bt), the virB T4SS genes, virB2-virB11 and the coupling protein gene virD4, are encoded at the same chromosomal location (Figure 3, Figure S4). Also, the bep genes are encoded in this region. In contrast, the genome sequences of lineage 3 (Bc, Br, BAR15, and B1-1C) revealed marked differences in organization, copy number, and chromosomal localization of the genes encoding the VirB T4SS. In the completely assembled genome of Bc, we found three copies of the virB2-virB10 genes encoded at two different chromosomal locations (Figure 3, Figure S4). Two copies are encoded at the same locus and belong to inverted repeats of ∼10kb. They are separated by several bep genes and the gene virD4. A third copy of the virB2-virB10 cluster including an additional bep gene is encoded in another genomic region highly conserved across different Bartonella lineages (Figure 3).

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