Comparative Genomics of <italic toggle="yes">Bacillus thuringiensis</italic> Reveals a Path to Specialized Exploitation of Multiple Invertebrate Hosts

ABSTRACT Understanding the genetic basis of host shifts is a key genomic question for pathogen and parasite biology. The Bacillus cereus group, which encompasses Bacillus thuringiensis and Bacillus anthracis, contains pathogens that can infect insects, nematodes, and vertebrates. Since the target ra...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Jinshui Zheng, Qiuling Gao, Linlin Liu, Hualin Liu, Yueying Wang, Donghai Peng, Lifang Ruan, Ben Raymond, Ming Sun
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Bacillus thuringiensis host specialization invertebrate pathogen population genomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/511eaa59d05049b7a3cb5590c0078527
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:511eaa59d05049b7a3cb5590c0078527
record_format	dspace
spelling	oai:doaj.org-article:511eaa59d05049b7a3cb5590c00785272021-11-15T15:51:43ZComparative Genomics of <italic toggle="yes">Bacillus thuringiensis</italic> Reveals a Path to Specialized Exploitation of Multiple Invertebrate Hosts10.1128/mBio.00822-172150-7511https://doaj.org/article/511eaa59d05049b7a3cb5590c00785272017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00822-17https://doaj.org/toc/2150-7511ABSTRACT Understanding the genetic basis of host shifts is a key genomic question for pathogen and parasite biology. The Bacillus cereus group, which encompasses Bacillus thuringiensis and Bacillus anthracis, contains pathogens that can infect insects, nematodes, and vertebrates. Since the target range of the essential virulence factors (Cry toxins) and many isolates is well known, this group presents a powerful system for investigating how pathogens can diversify and adapt to phylogenetically distant hosts. Specialization to exploit insects occurs at the level of the major clade and is associated with substantial changes in the core genome, and host switching between insect orders has occurred repeatedly within subclades. The transfer of plasmids with linked cry genes may account for much of the adaptation to particular insect orders, and network analysis implies that host specialization has produced strong associations between key toxin genes with similar targets. Analysis of the distribution of plasmid minireplicons shows that plasmids with orf156 and orf157, which carry genes encoding toxins against Lepidoptera or Diptera, were contained only by B. thuringiensis in the specialized insect clade (clade 2), indicating that tight genome/plasmid associations have been important in adaptation to invertebrate hosts. Moreover, the accumulation of multiple virulence factors on transposable elements suggests that cotransfer of diverse virulence factors is advantageous in terms of expanding the insecticidal spectrum, overcoming insect resistance, or through gains in pathogenicity via synergistic interactions between toxins. IMPORTANCE Population genomics have provided many new insights into the formation, evolution, and dynamics of bacterial pathogens of humans and other higher animals, but these pathogens usually have very narrow host ranges. As a pathogen of insects and nematodes, Bacillus thuringiensis, which produces toxins showing toxicity to many orders of insects and other invertebrates, can be used as a model to study the evolution of pathogens with wide host ranges. Phylogenomic analysis revealed that host specialization and switching occur at the level of the major clade and subclade, respectively. A toxin gene co-occurrence network indicates that multiple toxins with similar targets were accumulated by the same cell in the whole species. This accumulation may be one of the strategies that B. thuringiensis has used to fight against host resistance. This kind of formation and evolution of pathogens represents a different path used against multiple invertebrate hosts from that used against higher animals.Jinshui ZhengQiuling GaoLinlin LiuHualin LiuYueying WangDonghai PengLifang RuanBen RaymondMing SunAmerican Society for MicrobiologyarticleBacillus thuringiensishost specializationinvertebrate pathogenpopulation genomicsMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacillus thuringiensis host specialization invertebrate pathogen population genomics Microbiology QR1-502
spellingShingle	Bacillus thuringiensis host specialization invertebrate pathogen population genomics Microbiology QR1-502 Jinshui Zheng Qiuling Gao Linlin Liu Hualin Liu Yueying Wang Donghai Peng Lifang Ruan Ben Raymond Ming Sun Comparative Genomics of <italic toggle="yes">Bacillus thuringiensis</italic> Reveals a Path to Specialized Exploitation of Multiple Invertebrate Hosts
description	ABSTRACT Understanding the genetic basis of host shifts is a key genomic question for pathogen and parasite biology. The Bacillus cereus group, which encompasses Bacillus thuringiensis and Bacillus anthracis, contains pathogens that can infect insects, nematodes, and vertebrates. Since the target range of the essential virulence factors (Cry toxins) and many isolates is well known, this group presents a powerful system for investigating how pathogens can diversify and adapt to phylogenetically distant hosts. Specialization to exploit insects occurs at the level of the major clade and is associated with substantial changes in the core genome, and host switching between insect orders has occurred repeatedly within subclades. The transfer of plasmids with linked cry genes may account for much of the adaptation to particular insect orders, and network analysis implies that host specialization has produced strong associations between key toxin genes with similar targets. Analysis of the distribution of plasmid minireplicons shows that plasmids with orf156 and orf157, which carry genes encoding toxins against Lepidoptera or Diptera, were contained only by B. thuringiensis in the specialized insect clade (clade 2), indicating that tight genome/plasmid associations have been important in adaptation to invertebrate hosts. Moreover, the accumulation of multiple virulence factors on transposable elements suggests that cotransfer of diverse virulence factors is advantageous in terms of expanding the insecticidal spectrum, overcoming insect resistance, or through gains in pathogenicity via synergistic interactions between toxins. IMPORTANCE Population genomics have provided many new insights into the formation, evolution, and dynamics of bacterial pathogens of humans and other higher animals, but these pathogens usually have very narrow host ranges. As a pathogen of insects and nematodes, Bacillus thuringiensis, which produces toxins showing toxicity to many orders of insects and other invertebrates, can be used as a model to study the evolution of pathogens with wide host ranges. Phylogenomic analysis revealed that host specialization and switching occur at the level of the major clade and subclade, respectively. A toxin gene co-occurrence network indicates that multiple toxins with similar targets were accumulated by the same cell in the whole species. This accumulation may be one of the strategies that B. thuringiensis has used to fight against host resistance. This kind of formation and evolution of pathogens represents a different path used against multiple invertebrate hosts from that used against higher animals.
format	article
author	Jinshui Zheng Qiuling Gao Linlin Liu Hualin Liu Yueying Wang Donghai Peng Lifang Ruan Ben Raymond Ming Sun
author_facet	Jinshui Zheng Qiuling Gao Linlin Liu Hualin Liu Yueying Wang Donghai Peng Lifang Ruan Ben Raymond Ming Sun
author_sort	Jinshui Zheng
title	Comparative Genomics of <italic toggle="yes">Bacillus thuringiensis</italic> Reveals a Path to Specialized Exploitation of Multiple Invertebrate Hosts
title_short	Comparative Genomics of <italic toggle="yes">Bacillus thuringiensis</italic> Reveals a Path to Specialized Exploitation of Multiple Invertebrate Hosts
title_full	Comparative Genomics of <italic toggle="yes">Bacillus thuringiensis</italic> Reveals a Path to Specialized Exploitation of Multiple Invertebrate Hosts
title_fullStr	Comparative Genomics of <italic toggle="yes">Bacillus thuringiensis</italic> Reveals a Path to Specialized Exploitation of Multiple Invertebrate Hosts
title_full_unstemmed	Comparative Genomics of <italic toggle="yes">Bacillus thuringiensis</italic> Reveals a Path to Specialized Exploitation of Multiple Invertebrate Hosts
title_sort	comparative genomics of <italic toggle="yes">bacillus thuringiensis</italic> reveals a path to specialized exploitation of multiple invertebrate hosts
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/511eaa59d05049b7a3cb5590c0078527
work_keys_str_mv	AT jinshuizheng comparativegenomicsofitalictoggleyesbacillusthuringiensisitalicrevealsapathtospecializedexploitationofmultipleinvertebratehosts AT qiulinggao comparativegenomicsofitalictoggleyesbacillusthuringiensisitalicrevealsapathtospecializedexploitationofmultipleinvertebratehosts AT linlinliu comparativegenomicsofitalictoggleyesbacillusthuringiensisitalicrevealsapathtospecializedexploitationofmultipleinvertebratehosts AT hualinliu comparativegenomicsofitalictoggleyesbacillusthuringiensisitalicrevealsapathtospecializedexploitationofmultipleinvertebratehosts AT yueyingwang comparativegenomicsofitalictoggleyesbacillusthuringiensisitalicrevealsapathtospecializedexploitationofmultipleinvertebratehosts AT donghaipeng comparativegenomicsofitalictoggleyesbacillusthuringiensisitalicrevealsapathtospecializedexploitationofmultipleinvertebratehosts AT lifangruan comparativegenomicsofitalictoggleyesbacillusthuringiensisitalicrevealsapathtospecializedexploitationofmultipleinvertebratehosts AT benraymond comparativegenomicsofitalictoggleyesbacillusthuringiensisitalicrevealsapathtospecializedexploitationofmultipleinvertebratehosts AT mingsun comparativegenomicsofitalictoggleyesbacillusthuringiensisitalicrevealsapathtospecializedexploitationofmultipleinvertebratehosts
_version_	1718427333680955392

Comparative Genomics of <italic toggle="yes">Bacillus thuringiensis</italic> Reveals a Path to Specialized Exploitation of Multiple Invertebrate Hosts

Ejemplares similares