The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems.

Type 3 secretion systems (T3SSs) are essential components of two complex bacterial machineries: the flagellum, which drives cell motility, and the non-flagellar T3SS (NF-T3SS), which delivers effectors into eukaryotic cells. Yet the origin, specialization, and diversification of these machineries re...

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Main Authors: Sophie S Abby, Eduardo P C Rocha
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-09-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3459982?pdf=render
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spelling doaj-8be7be0e35f04081b971da5d075dfdac2020-11-25T01:16:11ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042012-09-0189e100298310.1371/journal.pgen.1002983The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems.Sophie S AbbyEduardo P C RochaType 3 secretion systems (T3SSs) are essential components of two complex bacterial machineries: the flagellum, which drives cell motility, and the non-flagellar T3SS (NF-T3SS), which delivers effectors into eukaryotic cells. Yet the origin, specialization, and diversification of these machineries remained unclear. We developed computational tools to identify homologous components of the two systems and to discriminate between them. Our analysis of >1,000 genomes identified 921 T3SSs, including 222 NF-T3SSs. Phylogenomic and comparative analyses of these systems argue that the NF-T3SS arose from an exaptation of the flagellum, i.e. the recruitment of part of the flagellum structure for the evolution of the new protein delivery function. This reconstructed chronology of the exaptation process proceeded in at least two steps. An intermediate ancestral form of NF-T3SS, whose descendants still exist in Myxococcales, lacked elements that are essential for motility and included a subset of NF-T3SS features. We argue that this ancestral version was involved in protein translocation. A second major step in the evolution of NF-T3SSs occurred via recruitment of secretins to the NF-T3SS, an event that occurred at least three times from different systems. In rhizobiales, a partial homologous gene replacement of the secretin resulted in two genes of complementary function. Acquisition of a secretin was followed by the rapid adaptation of the resulting NF-T3SSs to multiple, distinct eukaryotic cell envelopes where they became key in parasitic and mutualistic associations between prokaryotes and eukaryotes. Our work elucidates major steps of the evolutionary scenario leading to extant NF-T3SSs. It demonstrates how molecular evolution can convert one complex molecular machine into a second, equally complex machine by successive deletions, innovations, and recruitment from other molecular systems.http://europepmc.org/articles/PMC3459982?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Sophie S Abby
Eduardo P C Rocha
spellingShingle Sophie S Abby
Eduardo P C Rocha
The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems.
PLoS Genetics
author_facet Sophie S Abby
Eduardo P C Rocha
author_sort Sophie S Abby
title The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems.
title_short The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems.
title_full The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems.
title_fullStr The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems.
title_full_unstemmed The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems.
title_sort non-flagellar type iii secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2012-09-01
description Type 3 secretion systems (T3SSs) are essential components of two complex bacterial machineries: the flagellum, which drives cell motility, and the non-flagellar T3SS (NF-T3SS), which delivers effectors into eukaryotic cells. Yet the origin, specialization, and diversification of these machineries remained unclear. We developed computational tools to identify homologous components of the two systems and to discriminate between them. Our analysis of >1,000 genomes identified 921 T3SSs, including 222 NF-T3SSs. Phylogenomic and comparative analyses of these systems argue that the NF-T3SS arose from an exaptation of the flagellum, i.e. the recruitment of part of the flagellum structure for the evolution of the new protein delivery function. This reconstructed chronology of the exaptation process proceeded in at least two steps. An intermediate ancestral form of NF-T3SS, whose descendants still exist in Myxococcales, lacked elements that are essential for motility and included a subset of NF-T3SS features. We argue that this ancestral version was involved in protein translocation. A second major step in the evolution of NF-T3SSs occurred via recruitment of secretins to the NF-T3SS, an event that occurred at least three times from different systems. In rhizobiales, a partial homologous gene replacement of the secretin resulted in two genes of complementary function. Acquisition of a secretin was followed by the rapid adaptation of the resulting NF-T3SSs to multiple, distinct eukaryotic cell envelopes where they became key in parasitic and mutualistic associations between prokaryotes and eukaryotes. Our work elucidates major steps of the evolutionary scenario leading to extant NF-T3SSs. It demonstrates how molecular evolution can convert one complex molecular machine into a second, equally complex machine by successive deletions, innovations, and recruitment from other molecular systems.
url http://europepmc.org/articles/PMC3459982?pdf=render
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