Peptidoglycan transformations during <i><scp>B</scp>acillus subtilis</i> sporulation

Tocheva, Elitza I.; López‐Garrido, Javier; Hughes, H. Velocity; Fredlund, Jennifer; Kuru, Erkin; VanNieuwenhze, Michael S.; Brun, Yves V.; Pogliano, Kit; Jensen, Grant J.

doi:10.1111/mmi.12201

Cited by 109 publications

(129 citation statements)

References 70 publications

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“…4. The structural components of the spore section, including the core, cortex, and coat, were identified based upon current knowledge about the spore architecture (6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20). It has been well documented that the core is located at the center of the ellipsoidshaped spore of about 1 to 2 m in size.…”

Section: Resultsmentioning

confidence: 99%

“…The current knowledge of spore structures has been obtained largely using transmission electron microscopy (TEM) methods in various forms (6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20). A mature spore usually shows a concentric multilayer structure, consisting of the core, inner membrane, germ cell wall, cortex, outer membrane, and coat assembly.…”

mentioning

confidence: 99%

“…TEM studies of Gan et al (19) showed that the PG strands were circumferential, parallel to the cell membrane, and perpendicular to the long axis of the cell. More recently, the electron cryotomography study of Tocheva et al (15) showed that vegetative Bacillus subtilis cells and mature spores both are surrounded by a thick layer of peptidoglycan, revealing the presence of a PG-like layer throughout engulfment. Two thick layers of cortex were apparent between the inner and outer spore membranes.…”

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confidence: 99%

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Nanomechanical Characterization of Bacillus anthracis Spores by Atomic Force Microscopy

Burggraf

Xing

2016

Appl Environ Microbiol

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The study of structures and properties of bacterial spores is important to understanding spore formation and biological responses to environmental stresses. While significant progress has been made over the years in elucidating the multilayer architecture of spores, the mechanical properties of the spore interior are not known. Here, we present a thermal atomic force microscopy (AFM) study of the nanomechanical properties of internal structures of Bacillus anthracis spores. We developed a nanosurgical sectioning method in which a stiff diamond AFM tip was used to cut an individual spore, exposing its internal structure, and a soft AFM tip was used to image and characterize the spore interior on the nanometer scale. We observed that the elastic modulus and adhesion force, including their thermal responses at elevated temperatures, varied significantly in different regions of the spore section. Our AFM images indicated that the peptidoglycan (PG) cortex of Bacillus anthracis spores consisted of rod-like nanometer-sized structures that are oriented in the direction perpendicular to the spore surface. Our findings may shed light on the spore architecture and properties. IMPORTANCEA nanosurgical AFM method was developed that can be used to probe the structure and properties of the spore interior. The previously unknown ultrastructure of the PG cortex of Bacillus anthracis spores was observed to consist of nanometer-sized rodlike structures that are oriented in the direction perpendicular to the spore surface. The variations in the nanomechanical properties of the spore section were largely correlated with its chemical composition. Different components of the spore materials showed different thermal responses at elevated temperatures. Structures and material properties of bacterial spores play an important role in protecting them against a variety of environmental stresses, such as toxic chemicals (1), radiation (2, 3), and heat (3-5). The current knowledge of spore structures has been obtained largely using transmission electron microscopy (TEM) methods in various forms (6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20). A mature spore usually shows a concentric multilayer structure, consisting of the core, inner membrane, germ cell wall, cortex, outer membrane, and coat assembly. For Bacillus anthracis spores, there is an exosporium layer that loosely encases the spore. The spore core, which contains mostly DNA, RNA, enzymes, and dipicolinic acid (DPA), is in a dehydrated and metabolically dormant state (21-25). The ability of bacterial spores to survive for long durations, sometimes in harsh environments, has been attributed to the immobilization of essential DNA, RNA, and enzymes by small, acid-soluble spore proteins (SASP) (28-30). It was suggested that the DPA can be intercalated with spore DNA and RNA through covalent bonds, forming a gel-like polymer matrix (26,27). It is worth mentioning that the DPA structure in the spore core is not well understood. The germ cell wall (e.g., inner cortex) and ...

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

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Nanomechanical Characterization of Bacillus anthracis Spores by Atomic Force Microscopy

Burggraf

Xing

2016

Appl Environ Microbiol

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“…The basic topology of sporulation in all species produces two membranes, both of which originate from the cytoplasmic membrane of the mother cell and then later surround the mature spore (11,35). When Gram-positive cells germinate, the second membrane dissociates together with the spore coat and is lost.…”

Section: Discussionmentioning

confidence: 99%

Polyphosphate Storage during Sporulation in the Gram-Negative Bacterium Acetonema longum

Tocheva

Dekas

McGlynn

et al. 2013

Journal of Bacteriology

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Using electron cryotomography, we show that the Gram-negative sporulating bacterium Acetonema longum synthesizes highdensity storage granules at the leading edges of engulfing membranes. The granules appear in the prespore and increase in size and number as engulfment proceeds. Typically, a cluster of 8 to 12 storage granules closely associates with the inner spore membrane and ultimately accounts for ϳ7% of the total volume in mature spores. Energy-dispersive X-ray spectroscopy (EDX) analyses show that the granules contain high levels of phosphorus, oxygen, and magnesium and therefore are likely composed of polyphosphate (poly-P). Unlike the Gram-positive Bacilli and Clostridia, A. longum spores retain their outer spore membrane upon germination. To explore the possibility that the granules in A. longum may be involved in this unique process, we imaged purified Bacillus cereus, Bacillus thuringiensis, Bacillus subtilis, and Clostridium sporogenes spores. Even though B. cereus and B. thuringiensis contain the ppk and ppx genes, none of the spores from Gram-positive bacteria had granules. We speculate that poly-P in A. longum may provide either the energy or phosphate metabolites needed for outgrowth while retaining an outer membrane. Bacteria have the ability to store energy and nutrients such as carbon, phosphate, and nitrogen in the form of granules (1). Inorganic phosphorus (P i ) is stored in the form of polyphosphate (poly-P), chains of tens to hundreds of P i residues, linked by high-energy phosphoanhydride bonds (2). A variety of roles for poly-P granules have been suggested in cell membrane formation, transcriptional and enzymatic regulation, stress and stationary-phase responses, and cation sequestration (3). Even though the mechanism underlying poly-P accumulation is not clearly understood, the principal enzymes involved in the metabolism of poly-P in bacteria have been identified: two classes of poly-P kinases (PPK1 and PPK2) polymerize the terminal phosphate of ATP onto a poly-P chain and can also work in reverse to generate ATP from poly-P, and exopolyphosphatase (PPX) hydrolyzes the terminal phosphate from linear poly-P (4). Genes encoding PPK are present in many bacteria, including various human pathogens (5). Deletion of ppk affects growth, motility, quorum sensing, biofilm formation, and virulence (4, 6, 7). In the opportunistic pathogen Bacillus cereus, the ⌬ppx mutant was also impaired in sporulation (8).Sporulation is a complex morphological process performed by some members of the phylum Firmicutes when nutrients are limited (9). The process begins with an asymmetric cell division, followed by the engulfment of the smaller compartment by the bigger, mother cell (10). At the end of sporulation, two membranes and numerous protective layers surround the mature spore. When the conditions are favorable again, the spore germinates and a new cell is released via outgrowth (10). Our previous studies on sporulation revealed that, unlike Bacilli and Clostridia, the noncanonical Gram-negative organism ...

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“…1): during DNA replication, septation is initiated asymmetrically by FtsZ (a), followed by pumping of one of the DNA molecules through the forespore's closing septum by ATP hydrolysis (b) [2][3][4][5]. Subsequently, the septum (made of PG) is remodeled and grows around the forespore (c), allowing the mother cell to engulf the forespore by its membrane for spore maturation (d) [6][7][8]. This remodeling process is highly complicated, involving penicillin binding proteins (PBPs) to synthesize PG [9], the PG-degradation enzymes SpoIID/M/P [10], the SpoIIQ-SpoIIIAH backup mechanism [10], and many other proteins [11].…”

Section: Introductionmentioning

confidence: 99%

A model of cell-wall dynamics during sporulation inBacillus subtilis

Yap

Endres

2017

Soft Matter

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To survive starvation, Bacillus subtilis forms durable spores. After asymmetric cell division, the septum grows around the forespore in a process called engulfment, but the mechanism of force generation is unknown. Here, we derived a novel biophysical model for the dynamics of cell-wall remodeling during engulfment based on a balancing of dissipative, active, and mechanical forces. By plotting phase diagrams, we predict that sporulation is promoted by a line tension from the attachment of the septum to the outer cell wall, as well as by an imbalance in turgor pressures in the mother-cell and forespore compartments. We also predict that significant mother-cell growth hinders engulfment. Hence, relatively simple physical principles may guide this complex biological process.

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Peptidoglycan transformations during Bacillus subtilis sporulation

Cited by 109 publications

References 70 publications

Nanomechanical Characterization of Bacillus anthracis Spores by Atomic Force Microscopy

Nanomechanical Characterization of Bacillus anthracis Spores by Atomic Force Microscopy

Polyphosphate Storage during Sporulation in the Gram-Negative Bacterium Acetonema longum

A model of cell-wall dynamics during sporulation inBacillus subtilis

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