A gene transfer agent and a dynamic repertoire of secretion systems hold the keys to the explosive radiation of the emerging pathogen Bartonella.
A gene transfer agent and a dynamic repertoire of secretion systems hold the keys to the explosive radiation of the emerging pathogen Bartonella.
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DOI:
10.1371/journal.pgen.1003393
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发表时间:
2013-03
期刊:
影响因子:
4.5
通讯作者:
Andersson SG
中科院分区:
文献类型:
--
作者:
Guy L;Nystedt B;Toft C;Zaremba-Niedzwiedzka K;Berglund EC;Granberg F;Näslund K;Eriksson AS;Andersson SG
Gene transfer agents (GTAs) randomly transfer short fragments of a bacterial genome. A novel putative GTA was recently discovered in the mouse-infecting bacterium Bartonella grahamii. Although GTAs are widespread in phylogenetically diverse bacteria, their role in evolution is largely unknown. Here, we present a comparative analysis of 16 Bartonella genomes ranging from 1.4 to 2.6 Mb in size, including six novel genomes from Bartonella isolated from a cow, two moose, two dogs, and a kangaroo. A phylogenetic tree inferred from 428 orthologous core genes indicates that the deadly human pathogen B. bacilliformis is related to the ruminant-adapted clade, rather than being the earliest diverging species in the genus as previously thought. A gene flux analysis identified 12 genes for a GTA and a phage-derived origin of replication as the most conserved innovations. These are located in a region of a few hundred kb that also contains 8 insertions of gene clusters for type III, IV, and V secretion systems, and genes for putatively secreted molecules such as cholera-like toxins. The phylogenies indicate a recent transfer of seven genes in the virB gene cluster for a type IV secretion system from a cat-adapted B. henselae to a dog-adapted B. vinsonii strain. We show that the B. henselae GTA is functional and can transfer genes in vitro. We suggest that the maintenance of the GTA is driven by selection to increase the likelihood of horizontal gene transfer and argue that this process is beneficial at the population level, by facilitating adaptive evolution of the host-adaptation systems and thereby expansion of the host range size. The process counters gene loss and forces all cells to contribute to the production of the GTA and the secreted molecules. The results advance our understanding of the role that GTAs play for the evolution of bacterial genomes. Viruses are selfish genetic elements that replicate and transfer their own DNA, often killing the host cell in the process. Unlike viruses, gene transfer agents (GTAs) transfer random pieces of the bacterial genome rather than their own DNA. GTAs are widespread in bacterial genomes, but it is not known whether they are beneficial to the bacterium. In this study, we have used the emerging pathogen Bartonella as our model to study the evolution of GTAs. We sequenced the genomes of six isolates of Bartonella, including two new strains isolated from wild moose in Sweden. Using a comparative genomics approach, we searched for innovations in the last common ancestor that could help explain the explosive radiation of the genus. Surprisingly, we found that a gene cluster for a GTA and a phage-derived origin of replication was the most conserved innovation, indicative of strong selective constraints. We argue that the reason for the remarkable stability of the GTA is that it provides a mechanism to duplicate and recombine genes for secretion systems. This leads to adaptability to a broad range of hosts.
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影响因子:
10.7
作者:
Castresana, J
通讯作者:
Castresana, J
DOI:
10.1073/pnas.0400975101
发表时间:
2004-06-29
影响因子:
11.1
作者:
Boussau, B;Karlberg, EO;Andersson, SGE
通讯作者:
Andersson, SGE
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
影响因子:
9.4
作者:
BRENNER, DJ;OCONNOR, SP;STEIGERWALT, AG
通讯作者:
STEIGERWALT, AG
影响因子:
4.9
作者:
Berglund, Eva C.;Ellegaard, Kirsten;Andersson, Siv G. E.
通讯作者:
Andersson, Siv G. E.