Peptidoglycan Synthesis Machinery in <named-content content-type="genus-species">Agrobacterium tumefaciens</named-content> During Unipolar Growth and Cell Division

ABSTRACT The synthesis of peptidoglycan (PG) in bacteria is a crucial process controlling cell shape and vitality. In contrast to bacteria such as Escherichia coli that grow by dispersed lateral insertion of PG, little is known of the processes that direct polar PG synthesis in other bacteria such a...

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Autores principales:	Todd A. Cameron, James Anderson-Furgeson, John R. Zupan, Justin J. Zik, Patricia C. Zambryski
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3ea3679181674bcebac863c74a811224
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spelling	oai:doaj.org-article:3ea3679181674bcebac863c74a8112242021-11-15T15:47:39ZPeptidoglycan Synthesis Machinery in <named-content content-type="genus-species">Agrobacterium tumefaciens</named-content> During Unipolar Growth and Cell Division10.1128/mBio.01219-142150-7511https://doaj.org/article/3ea3679181674bcebac863c74a8112242014-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01219-14https://doaj.org/toc/2150-7511ABSTRACT The synthesis of peptidoglycan (PG) in bacteria is a crucial process controlling cell shape and vitality. In contrast to bacteria such as Escherichia coli that grow by dispersed lateral insertion of PG, little is known of the processes that direct polar PG synthesis in other bacteria such as the Rhizobiales. To better understand polar growth in the Rhizobiales Agrobacterium tumefaciens, we first surveyed its genome to identify homologs of (~70) well-known PG synthesis components. Since most of the canonical cell elongation components are absent from A. tumefaciens, we made fluorescent protein fusions to other putative PG synthesis components to assay their subcellular localization patterns. The cell division scaffolds FtsZ and FtsA, PBP1a, and a Rhizobiales- and Rhodobacterales-specific l,d-transpeptidase (LDT) all associate with the elongating cell pole. All four proteins also localize to the septum during cell division. Examination of the dimensions of growing cells revealed that new cell compartments gradually increase in width as they grow in length. This increase in cell width is coincident with an expanded region of LDT-mediated PG synthesis activity, as measured directly through incorporation of exogenous d-amino acids. Thus, unipolar growth in the Rhizobiales is surprisingly dynamic and represents a significant departure from the canonical growth mechanism of E. coli and other well-studied bacilli. IMPORTANCE Many rod-shaped bacteria, including pathogens such as Brucella and Mycobacteriu, grow by adding new material to their cell poles, and yet the proteins and mechanisms contributing to this process are not yet well defined. The polarly growing plant pathogen Agrobacterium tumefaciens was used as a model bacterium to explore these polar growth mechanisms. The results obtained indicate that polar growth in this organism is facilitated by repurposed cell division components and an otherwise obscure class of alternative peptidoglycan transpeptidases (l,d-transpeptidases). This growth results in dynamically changing cell widths as the poles expand to maturity and contrasts with the tightly regulated cell widths characteristic of canonical rod-shaped growth. Furthermore, the abundance and/or activity of l,d-transpeptidases appears to associate with polar growth strategies, suggesting that these enzymes may serve as attractive targets for specifically inhibiting growth of Rhizobiales, Actinomycetales, and other polarly growing bacterial pathogens.Todd A. CameronJames Anderson-FurgesonJohn R. ZupanJustin J. ZikPatricia C. ZambryskiAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 3 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Todd A. Cameron James Anderson-Furgeson John R. Zupan Justin J. Zik Patricia C. Zambryski Peptidoglycan Synthesis Machinery in <named-content content-type="genus-species">Agrobacterium tumefaciens</named-content> During Unipolar Growth and Cell Division
description	ABSTRACT The synthesis of peptidoglycan (PG) in bacteria is a crucial process controlling cell shape and vitality. In contrast to bacteria such as Escherichia coli that grow by dispersed lateral insertion of PG, little is known of the processes that direct polar PG synthesis in other bacteria such as the Rhizobiales. To better understand polar growth in the Rhizobiales Agrobacterium tumefaciens, we first surveyed its genome to identify homologs of (~70) well-known PG synthesis components. Since most of the canonical cell elongation components are absent from A. tumefaciens, we made fluorescent protein fusions to other putative PG synthesis components to assay their subcellular localization patterns. The cell division scaffolds FtsZ and FtsA, PBP1a, and a Rhizobiales- and Rhodobacterales-specific l,d-transpeptidase (LDT) all associate with the elongating cell pole. All four proteins also localize to the septum during cell division. Examination of the dimensions of growing cells revealed that new cell compartments gradually increase in width as they grow in length. This increase in cell width is coincident with an expanded region of LDT-mediated PG synthesis activity, as measured directly through incorporation of exogenous d-amino acids. Thus, unipolar growth in the Rhizobiales is surprisingly dynamic and represents a significant departure from the canonical growth mechanism of E. coli and other well-studied bacilli. IMPORTANCE Many rod-shaped bacteria, including pathogens such as Brucella and Mycobacteriu, grow by adding new material to their cell poles, and yet the proteins and mechanisms contributing to this process are not yet well defined. The polarly growing plant pathogen Agrobacterium tumefaciens was used as a model bacterium to explore these polar growth mechanisms. The results obtained indicate that polar growth in this organism is facilitated by repurposed cell division components and an otherwise obscure class of alternative peptidoglycan transpeptidases (l,d-transpeptidases). This growth results in dynamically changing cell widths as the poles expand to maturity and contrasts with the tightly regulated cell widths characteristic of canonical rod-shaped growth. Furthermore, the abundance and/or activity of l,d-transpeptidases appears to associate with polar growth strategies, suggesting that these enzymes may serve as attractive targets for specifically inhibiting growth of Rhizobiales, Actinomycetales, and other polarly growing bacterial pathogens.
format	article
author	Todd A. Cameron James Anderson-Furgeson John R. Zupan Justin J. Zik Patricia C. Zambryski
author_facet	Todd A. Cameron James Anderson-Furgeson John R. Zupan Justin J. Zik Patricia C. Zambryski
author_sort	Todd A. Cameron
title	Peptidoglycan Synthesis Machinery in <named-content content-type="genus-species">Agrobacterium tumefaciens</named-content> During Unipolar Growth and Cell Division
title_short	Peptidoglycan Synthesis Machinery in <named-content content-type="genus-species">Agrobacterium tumefaciens</named-content> During Unipolar Growth and Cell Division
title_full	Peptidoglycan Synthesis Machinery in <named-content content-type="genus-species">Agrobacterium tumefaciens</named-content> During Unipolar Growth and Cell Division
title_fullStr	Peptidoglycan Synthesis Machinery in <named-content content-type="genus-species">Agrobacterium tumefaciens</named-content> During Unipolar Growth and Cell Division
title_full_unstemmed	Peptidoglycan Synthesis Machinery in <named-content content-type="genus-species">Agrobacterium tumefaciens</named-content> During Unipolar Growth and Cell Division
title_sort	peptidoglycan synthesis machinery in <named-content content-type="genus-species">agrobacterium tumefaciens</named-content> during unipolar growth and cell division
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/3ea3679181674bcebac863c74a811224
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Peptidoglycan Synthesis Machinery in <named-content content-type="genus-species">Agrobacterium tumefaciens</named-content> During Unipolar Growth and Cell Division

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