Genome-Wide Analyses Revealed Remarkable Heterogeneity in Pathogenicity Determinants, Antimicrobial Compounds, and CRISPR-Cas Systems of Complex Phytopathogenic Genus <i>Pectobacterium</i>

The<b> </b><i>Pectobacterium</i> genus comprises pectolytic enterobacteria defined as the causal agents of soft rot, blackleg, and aerial stem rot diseases of potato and economically important crops. In this study, we undertook extensive genome-wide comparative analyses of tw...

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Main Authors: Dario Arizala, Mohammad Arif
Format: Article
Language:English
Published: MDPI AG 2019-11-01
Series:Pathogens
Subjects:
Online Access:https://www.mdpi.com/2076-0817/8/4/247
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author Dario Arizala
Mohammad Arif
author_facet Dario Arizala
Mohammad Arif
author_sort Dario Arizala
collection DOAJ
description The<b> </b><i>Pectobacterium</i> genus comprises pectolytic enterobacteria defined as the causal agents of soft rot, blackleg, and aerial stem rot diseases of potato and economically important crops. In this study, we undertook extensive genome-wide comparative analyses of twelve species that conform the <i>Pectobacterium</i> genus. Bioinformatics approaches outlined a low nucleotide identity of <i>P. parmentieri </i>and <i>P. wasabiae</i> with other species, while <i>P</i>. <i>carotovorum</i> subsp. <i>odoriferum</i> was shown to harbor numerous pseudogenes, which suggests low coding capacity and genomic degradation. The genome atlases allowed for distinguishing distinct DNA structures and highlighted suspicious high transcription zones. The analyses unveiled a noteworthy heterogeneity in the pathogenicity determinants. Specifically, phytotoxins, polysaccharides, iron uptake systems, and the type secretion systems III&#8722;V were observed in just some species. Likewise, a comparison of gene clusters encoding antimicrobial compounds put in evidence for high conservation of carotovoricin, whereas a few species possessed the phenazine, carbapenem, and carocins. Moreover, three clustered regularly interspaced short palindromic repeats-Cas (CRISPR-Cas) systems: I-E, I-F, and III-A were identified. Surrounding some CRISPR-Cas regions, different toxin and antitoxin systems were found, which suggests bacterial suicide in the case of an immune system failure. Multiple whole-genome alignments shed light on to the presence of a novel cellobiose phosphotransferase system (PTS) exclusive to <i>P. parmenteri,</i> and an unreported T5SS conserved in almost all species. Several regions that were associated with virulence, microbe antagonism, and adaptive immune systems were predicted within genomic islands, which underscored the essential role that horizontal gene transfer has imparted in the dynamic evolution and speciation of <i>Pectobacterium</i> species<i>.</i> Overall, the results decipher the different strategies that each species has developed to infect their hosts, outcompete for food resources, and defend against bacteriophages. Our investigation provides novel genetic insights that will assist in understanding the pathogenic lifestyle of <i>Pectobacterium</i>, a genus that jeopardizes the agriculture sustainability of important crops worldwide.
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spelling doaj.art-93aa1338193049fb907e23f475e4c8f82022-12-22T04:23:16ZengMDPI AGPathogens2076-08172019-11-018424710.3390/pathogens8040247pathogens8040247Genome-Wide Analyses Revealed Remarkable Heterogeneity in Pathogenicity Determinants, Antimicrobial Compounds, and CRISPR-Cas Systems of Complex Phytopathogenic Genus <i>Pectobacterium</i>Dario Arizala0Mohammad Arif1Department of Plant and Environmental Protection Sciences, University of Hawaii at Manoa, Honolulu, HI 96822, USADepartment of Plant and Environmental Protection Sciences, University of Hawaii at Manoa, Honolulu, HI 96822, USAThe<b> </b><i>Pectobacterium</i> genus comprises pectolytic enterobacteria defined as the causal agents of soft rot, blackleg, and aerial stem rot diseases of potato and economically important crops. In this study, we undertook extensive genome-wide comparative analyses of twelve species that conform the <i>Pectobacterium</i> genus. Bioinformatics approaches outlined a low nucleotide identity of <i>P. parmentieri </i>and <i>P. wasabiae</i> with other species, while <i>P</i>. <i>carotovorum</i> subsp. <i>odoriferum</i> was shown to harbor numerous pseudogenes, which suggests low coding capacity and genomic degradation. The genome atlases allowed for distinguishing distinct DNA structures and highlighted suspicious high transcription zones. The analyses unveiled a noteworthy heterogeneity in the pathogenicity determinants. Specifically, phytotoxins, polysaccharides, iron uptake systems, and the type secretion systems III&#8722;V were observed in just some species. Likewise, a comparison of gene clusters encoding antimicrobial compounds put in evidence for high conservation of carotovoricin, whereas a few species possessed the phenazine, carbapenem, and carocins. Moreover, three clustered regularly interspaced short palindromic repeats-Cas (CRISPR-Cas) systems: I-E, I-F, and III-A were identified. Surrounding some CRISPR-Cas regions, different toxin and antitoxin systems were found, which suggests bacterial suicide in the case of an immune system failure. Multiple whole-genome alignments shed light on to the presence of a novel cellobiose phosphotransferase system (PTS) exclusive to <i>P. parmenteri,</i> and an unreported T5SS conserved in almost all species. Several regions that were associated with virulence, microbe antagonism, and adaptive immune systems were predicted within genomic islands, which underscored the essential role that horizontal gene transfer has imparted in the dynamic evolution and speciation of <i>Pectobacterium</i> species<i>.</i> Overall, the results decipher the different strategies that each species has developed to infect their hosts, outcompete for food resources, and defend against bacteriophages. Our investigation provides novel genetic insights that will assist in understanding the pathogenic lifestyle of <i>Pectobacterium</i>, a genus that jeopardizes the agriculture sustainability of important crops worldwide.https://www.mdpi.com/2076-0817/8/4/247pectobacteriumcomparative genomicspathogenicity determinantsantimicrobial compoundscrispr-cashorizontal gene transferdynamic evolution
spellingShingle Dario Arizala
Mohammad Arif
Genome-Wide Analyses Revealed Remarkable Heterogeneity in Pathogenicity Determinants, Antimicrobial Compounds, and CRISPR-Cas Systems of Complex Phytopathogenic Genus <i>Pectobacterium</i>
Pathogens
pectobacterium
comparative genomics
pathogenicity determinants
antimicrobial compounds
crispr-cas
horizontal gene transfer
dynamic evolution
title Genome-Wide Analyses Revealed Remarkable Heterogeneity in Pathogenicity Determinants, Antimicrobial Compounds, and CRISPR-Cas Systems of Complex Phytopathogenic Genus <i>Pectobacterium</i>
title_full Genome-Wide Analyses Revealed Remarkable Heterogeneity in Pathogenicity Determinants, Antimicrobial Compounds, and CRISPR-Cas Systems of Complex Phytopathogenic Genus <i>Pectobacterium</i>
title_fullStr Genome-Wide Analyses Revealed Remarkable Heterogeneity in Pathogenicity Determinants, Antimicrobial Compounds, and CRISPR-Cas Systems of Complex Phytopathogenic Genus <i>Pectobacterium</i>
title_full_unstemmed Genome-Wide Analyses Revealed Remarkable Heterogeneity in Pathogenicity Determinants, Antimicrobial Compounds, and CRISPR-Cas Systems of Complex Phytopathogenic Genus <i>Pectobacterium</i>
title_short Genome-Wide Analyses Revealed Remarkable Heterogeneity in Pathogenicity Determinants, Antimicrobial Compounds, and CRISPR-Cas Systems of Complex Phytopathogenic Genus <i>Pectobacterium</i>
title_sort genome wide analyses revealed remarkable heterogeneity in pathogenicity determinants antimicrobial compounds and crispr cas systems of complex phytopathogenic genus i pectobacterium i
topic pectobacterium
comparative genomics
pathogenicity determinants
antimicrobial compounds
crispr-cas
horizontal gene transfer
dynamic evolution
url https://www.mdpi.com/2076-0817/8/4/247
work_keys_str_mv AT darioarizala genomewideanalysesrevealedremarkableheterogeneityinpathogenicitydeterminantsantimicrobialcompoundsandcrisprcassystemsofcomplexphytopathogenicgenusipectobacteriumi
AT mohammadarif genomewideanalysesrevealedremarkableheterogeneityinpathogenicitydeterminantsantimicrobialcompoundsandcrisprcassystemsofcomplexphytopathogenicgenusipectobacteriumi