Timing of swarmer cell cycle morphogenesis and macromolecular synthesis by Hyphomicrobium neptunium in synchronous culture

Wali, Tonu; Hudson, Gavin; Danald, D A; Weiner, Ronald M.

doi:10.1128/jb.144.1.406-412.1980

Cited by 33 publications

(22 citation statements)

References 16 publications

(29 reference statements)

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“…Culture synchronization. A modification of the size-sorting procedure of Wali et al (32) was used to synchronize VP-6 cultures. One liter of early-to midlogarithmic-phase culture was centrifuged at 13,000 ϫ g for 5 min.…”

Section: Methodsmentioning

confidence: 99%

Spatial and Temporal Deposition of Hyphomonas Strain VP-6 Capsules Involved in Biofilm Formation

Langille

Weiner

1998

Appl Environ Microbiol

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Hyphomonas strain VP-6 is a prosthecate bacterium isolated from the Guayamas vent region and is a member of a genus of primary and common colonizers of marine surfaces. It adheres to solid substrata as a first step in biofilm formation. Fine-structure microscopy and the use of specific stains and lectins reveal that it synthesizes two different extracellular polymeric substances (EPS). One is a temporally synthesized, polar holdfast EPS, and the other is a capsular EPS that is present during the complete life cycle and surrounds the entire cell, including the prosthecum. The timing and location of Hyphomonas strain VP-6 EPS elaboration correlate with adhesion to surfaces, suggesting that the EPS serves not only as the biofilm matrix but also as a primary adhesin. The temporality and polarity of VP-6 EPS expression substantially differ from those properties of Hyphomonas strain MHS-3 EPS expression.

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Section: Methodsmentioning

confidence: 99%

Spatial and Temporal Deposition of Hyphomonas Strain VP-6 Capsules Involved in Biofilm Formation

Langille

Weiner

1998

Appl Environ Microbiol

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“…The node at which MreB and the associated proteins MreCD, RodA, RodZ and PBP2 are predicted to have been lost is labeled with a red dot. structure (Wali et al, 1980;Moore, 1981). Cell division then occurs highly asymmetrically at the bud neck, giving rise to a stalked mother cell and a non-stalked daughter cell.…”

Section: Introductionmentioning

confidence: 99%

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

Cserti

Rosskopf

Chang

et al. 2017

Molecular Microbiology

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SUMMARYMost 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.

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“…Even among closely related species there are phenotypic differences, such as the number and placement of stalks, as well as differences in the genes involved in stalk synthesis. Furthermore, in many stalked marine species, the stalk serves a reproductive function, with a budding daughter cell produced from the tip of the stalk [41][42][43][44]. How have these stalk synthesis pathways evolved?…”

Section: Discussionmentioning

confidence: 99%

A Division of Labor in the Recruitment and Topological Organization of a Bacterial Morphogenic Complex

Caccamo

Jacq

VanNieuwenhze

et al. 2019

Preprint

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17Bacteria come in an array of shapes and sizes, but the mechanisms underlying diverse 18 morphologies are poorly understood. The peptidoglycan (PG) cell wall is the primary 19 determinant of cell shape. At the molecular level, much of the studied morphological 20 variation results from the regulation of PG synthesis enzymes involved in elongation 21 and division. These enzymes are spatially controlled by cytoskeletal scaffolding 22 hydrolase. How then does a non-cytoskeletal protein, SpmX, define and constrain PG 30 synthesis to form stalks? Here we report that SpmX and the bactofilin BacA act in 31 concert to regulate stalk synthesis in Asticcacaulis biprosthecum. We show that SpmX 32 acts to recruit BacA to the site of stalk synthesis. BacA then serves as a stalk-specific 33 topological organizer that anchors the PG synthesis complex, including its recruiter 34 SpmX, to the base of the stalk, where stalk PG synthesis occurs. In the absence of 35BacA, cells produce "pseudostalks" that are the result of unconstrained PG synthesis 36 correlated with the mislocalization of SpmX. Finally, we show that BacA is required to 37 inhibit the default function of PG synthesis machinery in cell elongation/division and to 38 prevent DNA entry at the site of stalk synthesis defined by SpmX. Therefore, the protein 39 responsible for recruitment of a morphogenic PG remodeling complex is uncoupled from 40 the protein that topologically organizes the complex. 41 42 to play a role in nutrient uptake [8, 9]. Stalk synthesis requires PG synthesis in a 60 spatially constrained zone in order to extend a thin cylindrical projection of the cell 61 envelope. The stalk is compartmentalized from the cytoplasm, as it is devoid of DNA 62 and ribosomes and excludes even small cytoplasmic proteins such as GFP [9]. 63Asticcacaulis biprosthecum, a gram negative Alphaproteobacterium from the 64 Caulobacteraceae family [10], produces two bilateral stalks whose synthesis depends 65 on PG synthesis at the base of the incipient stalk structures (red arrows in Figure 1A) 66 4 [11]. How do cells harness PG synthesis machinery to produce stalks while preventing 67 its typical function of cell elongation or division? 68 Here we report how a recently identified class of bacterial cytoskeletal protein, known as 69 "bactofilin", plays a dual role by defining the topography of PG synthesis for the 70 synthesis of stalks and by inhibiting a default cell elongation mode at that same site in 71 A. biprosthecum. Bactofilins are conserved throughout the bacterial kingdom and are 72 characterized by the presence of a central conserved DUF583 (or "bactofilin") domain 73 flanked by N-and C-terminal regions of variable length and sequence (Figure 1B) [12]. 74Bactofilins are involved in cell shape determination in a number of species. For 75 example, in the helical Helicobacter pylori and Leptospira biflexa, bactofilins are 76 required for proper helical shape generation [13, 14]. In Caulobacter crescentus, 77 bactofilins optimize the rate of stalk synthesis at the ce...

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Timing of swarmer cell cycle morphogenesis and macromolecular synthesis by Hyphomicrobium neptunium in synchronous culture

Cited by 33 publications

References 16 publications

Spatial and Temporal Deposition of Hyphomonas Strain VP-6 Capsules Involved in Biofilm Formation

Spatial and Temporal Deposition of Hyphomonas Strain VP-6 Capsules Involved in Biofilm Formation

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

A Division of Labor in the Recruitment and Topological Organization of a Bacterial Morphogenic Complex

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