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Dynamics of the peptidoglycan biosynthetic machinery in the stalked budding bacterium Hyphomonas neptunium

Cserti, Emöke and Rosskopf, Sabine and Chang, Yi-Wei and Eisheuer, Sabrina and Selter, Lars and Shi, Jian and Regh, Christina and Koert, Ulrich and Jensen, Grant J. and Thanbichler, Martin (2017) Dynamics of the peptidoglycan biosynthetic machinery in the stalked budding bacterium Hyphomonas neptunium. Molecular Microbiology, 103 (5). pp. 875-895. ISSN 0950-382X. https://resolver.caltech.edu/CaltechAUTHORS:20170104-102831596

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Abstract

Most commonly studied bacteria grow symmetrically and divide by binary fission, generating two siblings of equal morphology. An exception to this rule are budding bacteria, in which new offspring emerges de novo from a morphologically invariant mother cell. Although this mode of proliferation is widespread in diverse bacterial lineages, the underlying mechanisms are still incompletely understood. Here, we perform the first molecular-level analysis of growth and morphogenesis in the stalked budding alphaproteobacterium Hyphomonas neptunium. Peptidoglycan labeling shows that, in this species, buds originate from a stalk-like extension of the mother cell whose terminal segment is gradually remodeled into a new cell compartment. As a first step toward identifying the machinery mediating the budding process, we performed comprehensive mutational and localization studies of predicted peptidoglycan biosynthetic proteins in H. neptunium. These analyses identify factors that localize to distinct zones of dispersed and zonal growth, and they suggest a critical role of the MreB-controlled elongasome in cell morphogenesis. Collectively, our work shows that the mechanism of growth in H. neptunium is distinct from that in related, polarly growing members of the order Rhizobiales, setting the stage for in-depth analyses of the molecular principles regulating the fascinating developmental cycle of this species.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1111/mmi.13593DOIArticle
http://onlinelibrary.wiley.com/doi/10.1111/mmi.13593/abstractPublisherArticle
ORCID:
AuthorORCID
Chang, Yi-Wei0000-0003-2391-473X
Shi, Jian0000-0003-3810-5302
Jensen, Grant J.0000-0003-1556-4864
Thanbichler, Martin0000-0002-1303-1442
Alternate Title:Morphogenesis of Hyphomonas neptunium
Additional Information:© 2016 John Wiley & Sons, Inc. Accepted manuscript online: 20 December 2016; Manuscript Revised: 8 November 2016; Manuscript Received: 31 August 2016. We thank Erkin Kuru and Yves Brun for advice on the use and synthesis of HADA, Julia Rosum for excellent technical assistance, and Wolfgang Strobel for support in the initial phases of this work. Moreover, we are grateful to Daniela Kiekebusch, Maria Billini, and Alexandra Jung for critical reading of the manuscript. M.T. acknowledges core support from Philipps-Universität Marburg, funding from the German Research Foundation (DFG) through Research Training Group (GRK) 1216, and a Max Planck Fellowship from the Max Planck Society. Work in the laboratory of G.J.J. is supported by the Howard Hughes Medical Institute. Authors' Contributions: EC, SR, SE, and CR performed the genetic and cell biological analyses. YC, JS, and GJJ conducted the electron cryo-tomography studies. LS and UK carried out the synthesis of HADA. MT designed the study. EC and MT wrote the paper, with input from all other authors. The authors have no conflicts of interest related to this work.
Funders:
Funding AgencyGrant Number
Philipps-Universität MarburgUNSPECIFIED
Deutsche Forschungsgemeinschaft (DFG)1216
Max Planck SocietyUNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:Polar growth, stalked bacteria, morphogenesis, Agrobacterium, Caulobacter
Issue or Number:5
Record Number:CaltechAUTHORS:20170104-102831596
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20170104-102831596
Official Citation:Cserti, E., Rosskopf, S., Chang, Y.-W., Eisheuer, S., Selter, L., Shi, J., Regh, C., Koert, U., Jensen, G. J. and Thanbichler, M. (2017), Dynamics of the peptidoglycan biosynthetic machinery in the stalked budding bacterium Hyphomonas neptunium. Molecular Microbiology, 103: 875–895. doi:10.1111/mmi.13593
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:73201
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:04 Jan 2017 18:39
Last Modified:03 Oct 2019 16:25

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