Phylogenomic, Pan-genomic, Pathogenomic and Evolutionary Genomic Insights into the Agronomically Relevant Enterobacteria Pantoea ananatis and Pantoea stewartii

Pantoea ananatis is ubiquitously found in the environment and causes disease on a wide range of plant hosts. By contrast, its sister species, Pantoea stewartii subsp. stewartii is the host-specific causative agent of the devastating maize disease Stewart’s wilt. This pathogen has a restricted lifecy...

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Main Authors: Pieter De Maayer, Habibu Aliyu, Surendra Vikram, Jochen Blom, Brion Duffy, Don A. Cowan, Theo H. M. Smits, Stephanus N. Venter, Teresa A. Coutinho
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.01755/full
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author Pieter De Maayer
Habibu Aliyu
Surendra Vikram
Jochen Blom
Brion Duffy
Don A. Cowan
Theo H. M. Smits
Stephanus N. Venter
Teresa A. Coutinho
author_facet Pieter De Maayer
Habibu Aliyu
Surendra Vikram
Jochen Blom
Brion Duffy
Don A. Cowan
Theo H. M. Smits
Stephanus N. Venter
Teresa A. Coutinho
author_sort Pieter De Maayer
collection DOAJ
description Pantoea ananatis is ubiquitously found in the environment and causes disease on a wide range of plant hosts. By contrast, its sister species, Pantoea stewartii subsp. stewartii is the host-specific causative agent of the devastating maize disease Stewart’s wilt. This pathogen has a restricted lifecycle, overwintering in an insect vector before being introduced into susceptible maize cultivars, causing disease and returning to overwinter in its vector. The other subspecies of P. stewartii subsp. indologenes, has been isolated from different plant hosts and is predicted to proliferate in different environmental niches. Here we have, by the use of comparative genomics and a comprehensive suite of bioinformatic tools, analyzed the genomes of ten P. stewartii and nineteen P. ananatis strains. Our phylogenomic analyses have revealed that there are two distinct clades within P. ananatis while far less phylogenetic diversity was observed among the P. stewartii subspecies. Pan-genome analyses revealed a large core genome comprising of 3,571 protein coding sequences is shared among the twenty-nine compared strains. Furthermore, we showed that an extensive accessory genome made up largely by a mobilome of plasmids, integrated prophages, integrative and conjugative elements and insertion elements has resulted in extensive diversification of P. stewartii and P. ananatis. While these organisms share many pathogenicity determinants, our comparative genomic analyses show that they differ in terms of the secretion systems they encode. The genomic differences identified in this study have allowed us to postulate on the divergent evolutionary histories of the analyzed P. ananatis and P. stewartii strains and on the molecular basis underlying their ecological success and host range.
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spelling doaj.art-c03b759217604f82a23958bb9372dbed2022-12-21T19:24:05ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-09-01810.3389/fmicb.2017.01755287061Phylogenomic, Pan-genomic, Pathogenomic and Evolutionary Genomic Insights into the Agronomically Relevant Enterobacteria Pantoea ananatis and Pantoea stewartiiPieter De Maayer0Habibu Aliyu1Surendra Vikram2Jochen Blom3Brion Duffy4Don A. Cowan5Theo H. M. Smits6Stephanus N. Venter7Teresa A. Coutinho8School of Molecular and Cell Biology, University of the WitwatersrandJohannesburg, South AfricaCentre for Microbial Ecology and Genomics, Genomics Research Institute, University of PretoriaPretoria, South AfricaCentre for Microbial Ecology and Genomics, Genomics Research Institute, University of PretoriaPretoria, South AfricaDepartment of Bioinformatics and Systems Biology, Justus-Liebig-University GiessenGiessen, GermanyEnvironmental Genomics and Systems Biology Research Group, Institute for Natural Resource Sciences, Zurich University of Applied SciencesWinterthur, SwitzerlandCentre for Microbial Ecology and Genomics, Genomics Research Institute, University of PretoriaPretoria, South AfricaEnvironmental Genomics and Systems Biology Research Group, Institute for Natural Resource Sciences, Zurich University of Applied SciencesWinterthur, SwitzerlandDepartment of Microbiology, Forestry and Agricultural Biotechnology Institute, University of PretoriaPretoria, South AfricaDepartment of Microbiology, Forestry and Agricultural Biotechnology Institute, University of PretoriaPretoria, South AfricaPantoea ananatis is ubiquitously found in the environment and causes disease on a wide range of plant hosts. By contrast, its sister species, Pantoea stewartii subsp. stewartii is the host-specific causative agent of the devastating maize disease Stewart’s wilt. This pathogen has a restricted lifecycle, overwintering in an insect vector before being introduced into susceptible maize cultivars, causing disease and returning to overwinter in its vector. The other subspecies of P. stewartii subsp. indologenes, has been isolated from different plant hosts and is predicted to proliferate in different environmental niches. Here we have, by the use of comparative genomics and a comprehensive suite of bioinformatic tools, analyzed the genomes of ten P. stewartii and nineteen P. ananatis strains. Our phylogenomic analyses have revealed that there are two distinct clades within P. ananatis while far less phylogenetic diversity was observed among the P. stewartii subspecies. Pan-genome analyses revealed a large core genome comprising of 3,571 protein coding sequences is shared among the twenty-nine compared strains. Furthermore, we showed that an extensive accessory genome made up largely by a mobilome of plasmids, integrated prophages, integrative and conjugative elements and insertion elements has resulted in extensive diversification of P. stewartii and P. ananatis. While these organisms share many pathogenicity determinants, our comparative genomic analyses show that they differ in terms of the secretion systems they encode. The genomic differences identified in this study have allowed us to postulate on the divergent evolutionary histories of the analyzed P. ananatis and P. stewartii strains and on the molecular basis underlying their ecological success and host range.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01755/fullStewart’s wiltmobilomepan-genomephylogenomicspathogenicity factorshost range
spellingShingle Pieter De Maayer
Habibu Aliyu
Surendra Vikram
Jochen Blom
Brion Duffy
Don A. Cowan
Theo H. M. Smits
Stephanus N. Venter
Teresa A. Coutinho
Phylogenomic, Pan-genomic, Pathogenomic and Evolutionary Genomic Insights into the Agronomically Relevant Enterobacteria Pantoea ananatis and Pantoea stewartii
Frontiers in Microbiology
Stewart’s wilt
mobilome
pan-genome
phylogenomics
pathogenicity factors
host range
title Phylogenomic, Pan-genomic, Pathogenomic and Evolutionary Genomic Insights into the Agronomically Relevant Enterobacteria Pantoea ananatis and Pantoea stewartii
title_full Phylogenomic, Pan-genomic, Pathogenomic and Evolutionary Genomic Insights into the Agronomically Relevant Enterobacteria Pantoea ananatis and Pantoea stewartii
title_fullStr Phylogenomic, Pan-genomic, Pathogenomic and Evolutionary Genomic Insights into the Agronomically Relevant Enterobacteria Pantoea ananatis and Pantoea stewartii
title_full_unstemmed Phylogenomic, Pan-genomic, Pathogenomic and Evolutionary Genomic Insights into the Agronomically Relevant Enterobacteria Pantoea ananatis and Pantoea stewartii
title_short Phylogenomic, Pan-genomic, Pathogenomic and Evolutionary Genomic Insights into the Agronomically Relevant Enterobacteria Pantoea ananatis and Pantoea stewartii
title_sort phylogenomic pan genomic pathogenomic and evolutionary genomic insights into the agronomically relevant enterobacteria pantoea ananatis and pantoea stewartii
topic Stewart’s wilt
mobilome
pan-genome
phylogenomics
pathogenicity factors
host range
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.01755/full
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