Coordinated Assembly of the <named-content content-type="genus-species">Bacillus anthracis</named-content> Coat and Exosporium during Bacterial Spore Outer Layer Formation

ABSTRACT Bacterial spores produced by the Bacillales are composed of concentric shells, each of which contributes to spore function. Spores from all species possess a cortex and coat, but spores from many species possess additional outer layers. The outermost layer of Bacillus anthracis spores, the...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Tyler J. Boone, Michael Mallozzi, Alex Nelson, Brian Thompson, Mark Khemmani, Dörte Lehmann, Alexis Dunkle, Paul Hoeprich, Amy Rasley, George Stewart, Adam Driks
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Bacillus anthracis assembly coat exosporium spore Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/47227a09c2324a56be7ace9c3123d643
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:47227a09c2324a56be7ace9c3123d643
record_format	dspace
spelling	oai:doaj.org-article:47227a09c2324a56be7ace9c3123d6432021-11-15T15:52:19ZCoordinated Assembly of the <named-content content-type="genus-species">Bacillus anthracis</named-content> Coat and Exosporium during Bacterial Spore Outer Layer Formation10.1128/mBio.01166-182150-7511https://doaj.org/article/47227a09c2324a56be7ace9c3123d6432018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01166-18https://doaj.org/toc/2150-7511ABSTRACT Bacterial spores produced by the Bacillales are composed of concentric shells, each of which contributes to spore function. Spores from all species possess a cortex and coat, but spores from many species possess additional outer layers. The outermost layer of Bacillus anthracis spores, the exosporium, is separated from the coat by a gap known as the interspace. Exosporium and interspace assembly remains largely mysterious. As a result, we have a poor understanding of the overarching mechanisms driving the assembly of one of the most ubiquitous cell types in nature. To elucidate the mechanisms directing exosporium assembly, we generated strains bearing mutations in candidate exosporium-controlling genes and analyzed the effect on exosporium formation. Biochemical and cell biological analyses argue that CotE directs the assembly of CotO into the spore and that CotO might be located at or close to the interior side of the cap. Taken together with data showing that CotE and CotO interact directly in vitro, we propose a model in which CotE and CotO are important components of a protein interaction network that connects the exosporium to the forespore during cap formation and exosporium elongation. Our data also suggest that the cap interferes with coat assembly at one pole of the spore, altering the pattern of coat deposition compared to the model organism Bacillus subtilis. We propose that the difference in coat assembly patterns between these two species is due to an inherent flexibility in coat assembly, which may facilitate the evolution of spore outer layer complexity. IMPORTANCE This work dramatically improves our understanding of the assembly of the outermost layer of the B. anthracis spore, the exosporium, a layer that encases spores from many bacterial species and likely plays important roles in the spore’s interactions with the environment, including host tissues. Nonetheless, the mechanisms directing exosporium assembly into a shell surrounding the spore are still very poorly understood. In this study, we clarify these mechanisms by the identification of a novel protein interaction network that directs assembly to initiate at a specific subcellular location in the developing cell. Our results further suggest that the presence or absence of an exosporium has a major impact on the assembly of other more interior spore layers, thereby potentially explaining long-noted differences in spore assembly between B. anthracis and the model organism B. subtilis.Tyler J. BooneMichael MallozziAlex NelsonBrian ThompsonMark KhemmaniDörte LehmannAlexis DunklePaul HoeprichAmy RasleyGeorge StewartAdam DriksAmerican Society for MicrobiologyarticleBacillus anthracisassemblycoatexosporiumsporeMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacillus anthracis assembly coat exosporium spore Microbiology QR1-502
spellingShingle	Bacillus anthracis assembly coat exosporium spore Microbiology QR1-502 Tyler J. Boone Michael Mallozzi Alex Nelson Brian Thompson Mark Khemmani Dörte Lehmann Alexis Dunkle Paul Hoeprich Amy Rasley George Stewart Adam Driks Coordinated Assembly of the <named-content content-type="genus-species">Bacillus anthracis</named-content> Coat and Exosporium during Bacterial Spore Outer Layer Formation
description	ABSTRACT Bacterial spores produced by the Bacillales are composed of concentric shells, each of which contributes to spore function. Spores from all species possess a cortex and coat, but spores from many species possess additional outer layers. The outermost layer of Bacillus anthracis spores, the exosporium, is separated from the coat by a gap known as the interspace. Exosporium and interspace assembly remains largely mysterious. As a result, we have a poor understanding of the overarching mechanisms driving the assembly of one of the most ubiquitous cell types in nature. To elucidate the mechanisms directing exosporium assembly, we generated strains bearing mutations in candidate exosporium-controlling genes and analyzed the effect on exosporium formation. Biochemical and cell biological analyses argue that CotE directs the assembly of CotO into the spore and that CotO might be located at or close to the interior side of the cap. Taken together with data showing that CotE and CotO interact directly in vitro, we propose a model in which CotE and CotO are important components of a protein interaction network that connects the exosporium to the forespore during cap formation and exosporium elongation. Our data also suggest that the cap interferes with coat assembly at one pole of the spore, altering the pattern of coat deposition compared to the model organism Bacillus subtilis. We propose that the difference in coat assembly patterns between these two species is due to an inherent flexibility in coat assembly, which may facilitate the evolution of spore outer layer complexity. IMPORTANCE This work dramatically improves our understanding of the assembly of the outermost layer of the B. anthracis spore, the exosporium, a layer that encases spores from many bacterial species and likely plays important roles in the spore’s interactions with the environment, including host tissues. Nonetheless, the mechanisms directing exosporium assembly into a shell surrounding the spore are still very poorly understood. In this study, we clarify these mechanisms by the identification of a novel protein interaction network that directs assembly to initiate at a specific subcellular location in the developing cell. Our results further suggest that the presence or absence of an exosporium has a major impact on the assembly of other more interior spore layers, thereby potentially explaining long-noted differences in spore assembly between B. anthracis and the model organism B. subtilis.
format	article
author	Tyler J. Boone Michael Mallozzi Alex Nelson Brian Thompson Mark Khemmani Dörte Lehmann Alexis Dunkle Paul Hoeprich Amy Rasley George Stewart Adam Driks
author_facet	Tyler J. Boone Michael Mallozzi Alex Nelson Brian Thompson Mark Khemmani Dörte Lehmann Alexis Dunkle Paul Hoeprich Amy Rasley George Stewart Adam Driks
author_sort	Tyler J. Boone
title	Coordinated Assembly of the <named-content content-type="genus-species">Bacillus anthracis</named-content> Coat and Exosporium during Bacterial Spore Outer Layer Formation
title_short	Coordinated Assembly of the <named-content content-type="genus-species">Bacillus anthracis</named-content> Coat and Exosporium during Bacterial Spore Outer Layer Formation
title_full	Coordinated Assembly of the <named-content content-type="genus-species">Bacillus anthracis</named-content> Coat and Exosporium during Bacterial Spore Outer Layer Formation
title_fullStr	Coordinated Assembly of the <named-content content-type="genus-species">Bacillus anthracis</named-content> Coat and Exosporium during Bacterial Spore Outer Layer Formation
title_full_unstemmed	Coordinated Assembly of the <named-content content-type="genus-species">Bacillus anthracis</named-content> Coat and Exosporium during Bacterial Spore Outer Layer Formation
title_sort	coordinated assembly of the <named-content content-type="genus-species">bacillus anthracis</named-content> coat and exosporium during bacterial spore outer layer formation
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/47227a09c2324a56be7ace9c3123d643
work_keys_str_mv	AT tylerjboone coordinatedassemblyofthenamedcontentcontenttypegenusspeciesbacillusanthracisnamedcontentcoatandexosporiumduringbacterialsporeouterlayerformation AT michaelmallozzi coordinatedassemblyofthenamedcontentcontenttypegenusspeciesbacillusanthracisnamedcontentcoatandexosporiumduringbacterialsporeouterlayerformation AT alexnelson coordinatedassemblyofthenamedcontentcontenttypegenusspeciesbacillusanthracisnamedcontentcoatandexosporiumduringbacterialsporeouterlayerformation AT brianthompson coordinatedassemblyofthenamedcontentcontenttypegenusspeciesbacillusanthracisnamedcontentcoatandexosporiumduringbacterialsporeouterlayerformation AT markkhemmani coordinatedassemblyofthenamedcontentcontenttypegenusspeciesbacillusanthracisnamedcontentcoatandexosporiumduringbacterialsporeouterlayerformation AT dortelehmann coordinatedassemblyofthenamedcontentcontenttypegenusspeciesbacillusanthracisnamedcontentcoatandexosporiumduringbacterialsporeouterlayerformation AT alexisdunkle coordinatedassemblyofthenamedcontentcontenttypegenusspeciesbacillusanthracisnamedcontentcoatandexosporiumduringbacterialsporeouterlayerformation AT paulhoeprich coordinatedassemblyofthenamedcontentcontenttypegenusspeciesbacillusanthracisnamedcontentcoatandexosporiumduringbacterialsporeouterlayerformation AT amyrasley coordinatedassemblyofthenamedcontentcontenttypegenusspeciesbacillusanthracisnamedcontentcoatandexosporiumduringbacterialsporeouterlayerformation AT georgestewart coordinatedassemblyofthenamedcontentcontenttypegenusspeciesbacillusanthracisnamedcontentcoatandexosporiumduringbacterialsporeouterlayerformation AT adamdriks coordinatedassemblyofthenamedcontentcontenttypegenusspeciesbacillusanthracisnamedcontentcoatandexosporiumduringbacterialsporeouterlayerformation
_version_	1718427271856914432

Coordinated Assembly of the <named-content content-type="genus-species">Bacillus anthracis</named-content> Coat and Exosporium during Bacterial Spore Outer Layer Formation

Ejemplares similares