Parallel evolution of a type IV secretion system in radiating lineages of the host-restricted bacterial pathogen Bartonella.
Parallel evolution of a type IV secretion system in radiating lineages of the host-restricted bacterial pathogen Bartonella.
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DOI:
10.1371/journal.pgen.1001296
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发表时间:
2011-02-10
期刊:
影响因子:
4.5
通讯作者:
Dehio C
中科院分区:
文献类型:
--
作者:
Engel P;Salzburger W;Liesch M;Chang CC;Maruyama S;Lanz C;Calteau A;Lajus A;Médigue C;Schuster SC;Dehio C
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. Adaptive radiation is the rapid origination of an array of species by the divergent colonization of disparate ecological niches. In the case of pathogenic bacteria, radiations can lead to the emergence of novel human pathogens. Being divergently adapted to a range of different mammalian hosts, including humans as reservoir or incidental hosts, the genus Bartonella represents a suitable model to study genomic mechanisms underpinning divergent adaptation of pathogens. Here we show that two distinct lineages of Bartonella have radiated in parallel, resulting in two arrays of evolutionary distinct species adapted to overlapping sets of mammalian hosts. Such parallelisms display excellent models to reveal insights into the genetic mechanisms underlying these independent evolutionary processes. Our genome-wide analysis identifies a striking evolutionary parallelism in a horizontally-acquired protein secretion system in the two lineages. The parallel evolutionary trajectory of this system in the two lineages is characterized by the convergent origination of a wide array of adaptive functions dedicated to the cellular interaction within the mammalian hosts. The parallel evolution of the two radiating lineages on the ecological as well as on the molecular level suggests that the horizontal acquisition and the functional diversification of the secretion system display an evolutionary key innovation underlying adaptive evolution.
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影响因子:
11.8
作者:
Chang, CC;Chomel, BB;Piémont, Y
通讯作者:
Piémont, Y
DOI:
10.1073/pnas.0802343105
发表时间:
2008-10-07
影响因子:
11.1
作者:
Duponchelle, Fabrice;Paradis, Emmanuel;Turner, George F.
通讯作者:
Turner, George F.
影响因子:
2.9
作者:
Brakefield, P. M.;Roskam, J. C.
通讯作者:
Roskam, J. C.
影响因子:
3.7
作者:
Arvand M;Raoult D;Feil EJ
通讯作者:
Feil EJ
影响因子:
4.5
作者:
Berglund EC;Frank AC;Calteau A;Vinnere Pettersson O;Granberg F;Eriksson AS;Näslund K;Holmberg M;Lindroos H;Andersson SG
通讯作者:
Andersson SG