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Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium

Bradyrhizobium are abundant soil bacteria and the major symbiont of legumes. The recent availability of Bradyrhizobium genome sequences provides a large source of information for analysis of symbiotic traits. In this study, we investigated the evolutionary dynamics of the nodulation genes (nod) and...

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Autores principales: Teulet, Albin, Gully, Djamel, Rouy, Zoe, Camuel, Alicia, Koebnik, Ralf, Giraud, Eric, Lassalle, Florent
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Microbiology Society 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7643967/
https://www.ncbi.nlm.nih.gov/pubmed/32783800
http://dx.doi.org/10.1099/mgen.0.000407
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author Teulet, Albin
Gully, Djamel
Rouy, Zoe
Camuel, Alicia
Koebnik, Ralf
Giraud, Eric
Lassalle, Florent
author_facet Teulet, Albin
Gully, Djamel
Rouy, Zoe
Camuel, Alicia
Koebnik, Ralf
Giraud, Eric
Lassalle, Florent
author_sort Teulet, Albin
collection PubMed
description Bradyrhizobium are abundant soil bacteria and the major symbiont of legumes. The recent availability of Bradyrhizobium genome sequences provides a large source of information for analysis of symbiotic traits. In this study, we investigated the evolutionary dynamics of the nodulation genes (nod) and their relationship with the genes encoding type III secretion systems (T3SS) and their effectors among bradyrhizobia. Based on the comparative analysis of 146 Bradyrhizobium genome sequences, we identified six different types of T3SS gene clusters. The two predominant cluster types are designated RhcIa and RhcIb and both belong to the RhcI-T3SS family previously described in other rhizobia. They are found in 92/146 strains, most of them also containing nod genes. RhcIa and RhcIb gene clusters differ in the genes they carry: while the translocon-encoding gene nopX is systematically found in strains containing RhcIb, the nopE and nopH genes are specifically conserved in strains containing RhcIa, suggesting that these last two genes might functionally substitute nopX and play a role related to effector translocation. Phylogenetic analysis suggests that bradyrhizobia simultaneously gained nod and RhcI-T3SS gene clusters via horizontal transfer or subsequent vertical inheritance of a symbiotic island containing both. Sequence similarity searches for known Nop effector proteins in bradyrhizobial proteomes revealed the absence of a so-called core effectome, i.e. that no effector is conserved among all Bradyrhizobium strains. However, NopM and SUMO proteases were found to be the main effector families, being represented in the majority of the genus. This study indicates that bradyrhizobial T3SSs might play a more significant symbiotic role than previously thought and provides new candidates among T3SS structural proteins and effectors for future functional investigations.
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spelling pubmed-76439672020-11-09 Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium Teulet, Albin Gully, Djamel Rouy, Zoe Camuel, Alicia Koebnik, Ralf Giraud, Eric Lassalle, Florent Microb Genom Research Article Bradyrhizobium are abundant soil bacteria and the major symbiont of legumes. The recent availability of Bradyrhizobium genome sequences provides a large source of information for analysis of symbiotic traits. In this study, we investigated the evolutionary dynamics of the nodulation genes (nod) and their relationship with the genes encoding type III secretion systems (T3SS) and their effectors among bradyrhizobia. Based on the comparative analysis of 146 Bradyrhizobium genome sequences, we identified six different types of T3SS gene clusters. The two predominant cluster types are designated RhcIa and RhcIb and both belong to the RhcI-T3SS family previously described in other rhizobia. They are found in 92/146 strains, most of them also containing nod genes. RhcIa and RhcIb gene clusters differ in the genes they carry: while the translocon-encoding gene nopX is systematically found in strains containing RhcIb, the nopE and nopH genes are specifically conserved in strains containing RhcIa, suggesting that these last two genes might functionally substitute nopX and play a role related to effector translocation. Phylogenetic analysis suggests that bradyrhizobia simultaneously gained nod and RhcI-T3SS gene clusters via horizontal transfer or subsequent vertical inheritance of a symbiotic island containing both. Sequence similarity searches for known Nop effector proteins in bradyrhizobial proteomes revealed the absence of a so-called core effectome, i.e. that no effector is conserved among all Bradyrhizobium strains. However, NopM and SUMO proteases were found to be the main effector families, being represented in the majority of the genus. This study indicates that bradyrhizobial T3SSs might play a more significant symbiotic role than previously thought and provides new candidates among T3SS structural proteins and effectors for future functional investigations. Microbiology Society 2020-08-12 /pmc/articles/PMC7643967/ /pubmed/32783800 http://dx.doi.org/10.1099/mgen.0.000407 Text en © 2020 The Authors http://creativecommons.org/licenses/by-nc/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
spellingShingle Research Article
Teulet, Albin
Gully, Djamel
Rouy, Zoe
Camuel, Alicia
Koebnik, Ralf
Giraud, Eric
Lassalle, Florent
Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium
title Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium
title_full Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium
title_fullStr Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium
title_full_unstemmed Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium
title_short Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium
title_sort phylogenetic distribution and evolutionary dynamics of nod and t3ss genes in the genus bradyrhizobium
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7643967/
https://www.ncbi.nlm.nih.gov/pubmed/32783800
http://dx.doi.org/10.1099/mgen.0.000407
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