Petrobactin Protects against Oxidative Stress and Enhances Sporulation Efficiency in <named-content content-type="genus-species">Bacillus anthracis</named-content> Sterne

ABSTRACT Bacillus anthracis is a Gram-positive bacillus that under conditions of environmental stress, such as low nutrients, can convert from a vegetative bacillus to a highly durable spore that enables long-term survival. The sporulation process is regulated by a sequential cascade of dedicated tr...

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Autores principales:	Ada K. Hagan, Yael M. Plotnick, Ryan E. Dingle, Zachary I. Mendel, Stephen R. Cendrowski, David H. Sherman, Ashootosh Tripathi, Philip C. Hanna
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Bacillus anthracis LAESI-MS oxidative stress petrobactin siderophore sporulation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/074d819a7d234329a00097ef8de7cd07
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spelling	oai:doaj.org-article:074d819a7d234329a00097ef8de7cd072021-11-15T15:52:18ZPetrobactin Protects against Oxidative Stress and Enhances Sporulation Efficiency in <named-content content-type="genus-species">Bacillus anthracis</named-content> Sterne10.1128/mBio.02079-182150-7511https://doaj.org/article/074d819a7d234329a00097ef8de7cd072018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02079-18https://doaj.org/toc/2150-7511ABSTRACT Bacillus anthracis is a Gram-positive bacillus that under conditions of environmental stress, such as low nutrients, can convert from a vegetative bacillus to a highly durable spore that enables long-term survival. The sporulation process is regulated by a sequential cascade of dedicated transcription factors but requires key nutrients to complete, one of which is iron. Iron acquisition by the iron-scavenging siderophore petrobactin is required for vegetative growth of B. anthracis under iron-depleted conditions and in the host. However, the extent to which petrobactin is involved in spore formation is unknown. This work shows that efficient in vitro sporulation of B. anthracis requires petrobactin, that the petrobactin biosynthesis operon (asbA to -F) is induced prior to sporulation, and that the siderophore itself associates with spores. Petrobactin is also required for oxidative stress protection during late-stage growth and for wild-type levels of sporulation in sporulation medium. Sporulation in bovine blood was found to be petrobactin dependent. Collectively, the in vitro contributions of petrobactin to sporulation as well as growth imply that petrobactin may be required for B. anthracis transmission via the spore during natural infections, in addition to its key known functions during active anthrax infections. IMPORTANCE Bacillus anthracis causes the disease anthrax, which is transmitted via its dormant, spore phase. However, conversion from bacillus to spore is a complex, energetically costly process that requires many nutrients, including iron. B. anthracis requires the siderophore petrobactin to scavenge iron from host environments. We show that, in the Sterne strain, petrobactin is required for efficient sporulation, even when ample iron is available. The petrobactin biosynthesis operon is expressed during sporulation, and petrobactin is biosynthesized during growth in high-iron sporulation medium, but instead of being exported, the petrobactin remains intracellular to protect against oxidative stress and improve sporulation. It is also required for full growth and sporulation in blood (bovine), an essential step for anthrax transmission between mammalian hosts.Ada K. HaganYael M. PlotnickRyan E. DingleZachary I. MendelStephen R. CendrowskiDavid H. ShermanAshootosh TripathiPhilip C. HannaAmerican Society for MicrobiologyarticleBacillus anthracisLAESI-MSoxidative stresspetrobactinsiderophoresporulationMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacillus anthracis LAESI-MS oxidative stress petrobactin siderophore sporulation Microbiology QR1-502
spellingShingle	Bacillus anthracis LAESI-MS oxidative stress petrobactin siderophore sporulation Microbiology QR1-502 Ada K. Hagan Yael M. Plotnick Ryan E. Dingle Zachary I. Mendel Stephen R. Cendrowski David H. Sherman Ashootosh Tripathi Philip C. Hanna Petrobactin Protects against Oxidative Stress and Enhances Sporulation Efficiency in <named-content content-type="genus-species">Bacillus anthracis</named-content> Sterne
description	ABSTRACT Bacillus anthracis is a Gram-positive bacillus that under conditions of environmental stress, such as low nutrients, can convert from a vegetative bacillus to a highly durable spore that enables long-term survival. The sporulation process is regulated by a sequential cascade of dedicated transcription factors but requires key nutrients to complete, one of which is iron. Iron acquisition by the iron-scavenging siderophore petrobactin is required for vegetative growth of B. anthracis under iron-depleted conditions and in the host. However, the extent to which petrobactin is involved in spore formation is unknown. This work shows that efficient in vitro sporulation of B. anthracis requires petrobactin, that the petrobactin biosynthesis operon (asbA to -F) is induced prior to sporulation, and that the siderophore itself associates with spores. Petrobactin is also required for oxidative stress protection during late-stage growth and for wild-type levels of sporulation in sporulation medium. Sporulation in bovine blood was found to be petrobactin dependent. Collectively, the in vitro contributions of petrobactin to sporulation as well as growth imply that petrobactin may be required for B. anthracis transmission via the spore during natural infections, in addition to its key known functions during active anthrax infections. IMPORTANCE Bacillus anthracis causes the disease anthrax, which is transmitted via its dormant, spore phase. However, conversion from bacillus to spore is a complex, energetically costly process that requires many nutrients, including iron. B. anthracis requires the siderophore petrobactin to scavenge iron from host environments. We show that, in the Sterne strain, petrobactin is required for efficient sporulation, even when ample iron is available. The petrobactin biosynthesis operon is expressed during sporulation, and petrobactin is biosynthesized during growth in high-iron sporulation medium, but instead of being exported, the petrobactin remains intracellular to protect against oxidative stress and improve sporulation. It is also required for full growth and sporulation in blood (bovine), an essential step for anthrax transmission between mammalian hosts.
format	article
author	Ada K. Hagan Yael M. Plotnick Ryan E. Dingle Zachary I. Mendel Stephen R. Cendrowski David H. Sherman Ashootosh Tripathi Philip C. Hanna
author_facet	Ada K. Hagan Yael M. Plotnick Ryan E. Dingle Zachary I. Mendel Stephen R. Cendrowski David H. Sherman Ashootosh Tripathi Philip C. Hanna
author_sort	Ada K. Hagan
title	Petrobactin Protects against Oxidative Stress and Enhances Sporulation Efficiency in <named-content content-type="genus-species">Bacillus anthracis</named-content> Sterne
title_short	Petrobactin Protects against Oxidative Stress and Enhances Sporulation Efficiency in <named-content content-type="genus-species">Bacillus anthracis</named-content> Sterne
title_full	Petrobactin Protects against Oxidative Stress and Enhances Sporulation Efficiency in <named-content content-type="genus-species">Bacillus anthracis</named-content> Sterne
title_fullStr	Petrobactin Protects against Oxidative Stress and Enhances Sporulation Efficiency in <named-content content-type="genus-species">Bacillus anthracis</named-content> Sterne
title_full_unstemmed	Petrobactin Protects against Oxidative Stress and Enhances Sporulation Efficiency in <named-content content-type="genus-species">Bacillus anthracis</named-content> Sterne
title_sort	petrobactin protects against oxidative stress and enhances sporulation efficiency in <named-content content-type="genus-species">bacillus anthracis</named-content> sterne
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/074d819a7d234329a00097ef8de7cd07
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Petrobactin Protects against Oxidative Stress and Enhances Sporulation Efficiency in <named-content content-type="genus-species">Bacillus anthracis</named-content> Sterne

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