The wall of bacteria serves the roles that mechano-proteins do in eukaryotes

Koch, A L

doi:10.1016/0168-6445(91)90003-z

Cited by 13 publications

(15 citation statements)

References 27 publications

(35 reference statements)

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“…The actin-based cytoskeleton is the major shape-determining component of animal cells, but the cell wall performs this role in bacteria (20,22). This difference suggests that although the effect on cytoskeletal structure may be appropriate for galvanotropic animal cells, it is not relevant for bacteria, which lack microfilaments.…”

Section: Discussionmentioning

confidence: 86%

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Electric fields induce curved growth of Enterobacter cloacae, Escherichia coli, and Bacillus subtilis cells: implications for mechanisms of galvanotropism and bacterial growth

1994

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(18,19,21,24). Its basic assumption is that osmotically derived hydrostatic pressure causes tension within the plane of the wall. The wall is not uniformly rigid, and so expansion occurs at regions that are most plastic. Conceptually, growth should be especially problematic for gramnegative bacteria, in which the load-bearing peptidoglycan of the cell wall is extremely thin (19,23) and the bonds within it are stressed greatly by the cell's high (3 to 5 atm) internal osmotic pressure (20,21). In the case of gram-negative enteric bacteria, the prevailing form of the surface stress theory is the variable T model, which suggests that cell shape is determined by regional variation of T, the analog of surface tension (23). Although new murein is inserted all over the surface of gram-negative rods (30), localized variations in T lead to regional differences in the bond stresses within the sacculus, which in turn dictate the rate of cell wall growth. Growth is slow where T is high (at the old poles and on the side walls) and is faster where T is lower (at the developing division sites).This study illustrates that bacteria curve as they grow in applied electric fields. Our data suggest that this striking morphology arises from field-induced regional variation in wall growth rates on the anode-and cathode-facing sides of cells. The ability to manipulate T locally may therefore be a valuable tool in the effort to understand the process of normal growth. Our data also imply that the mechanism for galvanotropism is not the same for all cell types. Specifically, actin is not an 702

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Section: Discussionmentioning

confidence: 86%

“…Despite recent evidence that homologs of eukaryotic mechanopro,teins exist in bacteria (3,31), it is generally accepted that bacteria are naturally devoid of actin (22). We have therefore exploited the serendipitous discovery of a galvanotropic bacterium to explore the mechanisms that elicit fieldinduced directional growth.…”

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confidence: 99%

Electric fields induce curved growth of Enterobacter cloacae, Escherichia coli, and Bacillus subtilis cells: implications for mechanisms of galvanotropism and bacterial growth

1994

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“…There is a third class of models that assume the existence of mechano-proteins that could exert forces, causing extension over the length of the cell or contraction over the width of a cell (Norris et al, 1994). This is in spite of the fact that there is no evidence of force-generating proteins in bacteria (Koch, 1991(Koch, , 1998 and in addition although clearly FtsZ and FtsA have a homology to tubulin and actin and are involved in cell division they cannot have a role in constraining the diameter of the cell because of their small numbers and their distribution within the bulk of the cell throughout the cell cycle.…”

Section: Consequence Of Our Observations For Previously Proposed Theomentioning

confidence: 86%

“…The surface stress theory (Koch, 1983(Koch, , 1988(Koch, , 1991(Koch, , 1998(Koch, , 2000a(Koch, , b, 2001 explains the extension of the sidewall of rod-shaped cells by physical forces akin to surface tension acting as the wall grows.…”

Section: Consequence Of Our Observations For Previously Proposed Theomentioning

confidence: 99%

Patchiness of murein insertion into the sidewall of Escherichia coli

2003

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This paper extends, with computer techniques, the authors' previous work on the kinetics of pole wall and sidewall synthesis in Escherichia coli. These findings extend the conclusion that the nascent poles are made of entirely new material and that no new material is inserted into old poles. This requires re-evaluation of ideas in the literature about wall growth and cell division. Mechanisms of various types have been suggested for the growth of Gram-negative rod-shaped bacteria and these will also require major re-evaluation because of the finding, reported here, that the sidewall is made in several modes: patches of new murein, bands of new material largely going circumferentially around the cell, and areas of the sidewall that are enlarged by an intimate and regular admixture of new with the old muropeptides.

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“…Further progress in under- (43), presumably because of the extreme ionic strength of both their intracellular and extracellular environments. Therefore, these cells do not have obvious turgorbased shape constraints (22) and instead use their S-layer glycoprotein array (25) (for a review, see reference 4) and possibly a cytoskeleton to define cell shape. Since overproducing FtsZ in H. salinarium mimics the loss of rod shape observed with lowered external salt concentration, it is reasonable to propose that altered FtsZ levels, and hence altered interactions between the FtsZ division polymer and the cell wall, could perturb the shape-determining features of the S-layer without causing lysis.…”

Section: Fig 4 Morphology Of H Salinarium Pho81wrmentioning

confidence: 99%

Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarium: implications for the evolution of FtsZ and tubulin

Margolin¹,

Wang²,

Kumar³

1996

J Bacteriol

108

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We have isolated a homolog of the cell division gene ftsZ from the extremely halophilic archaebacterium Halobacterium salinarium. The predicted protein of 39 kDa is divergent relative to eubacterial homologs, with 32% identity to Escherichia coli FtsZ. No other eubacterial cell division gene homologs were found adjacent to H. salinarium ftsZ. Expression of the ftsZ gene region in H. salinarium induced significant morphological changes leading to the loss of rod shape. Phylogenetic analysis demonstrated that the H. salinarium FtsZ protein is more related to tubulins than are the FtsZ proteins of eubacteria, supporting the hypothesis that FtsZ may have evolved into eukaryotic tubulin.FtsZ is an essential cell division protein in Escherichia coli and Bacillus subtilis (3, 9) and appears to be conserved among eubacteria (8). It polymerizes to form a circumferential ring at the division site, constricting at the leading edge of the invaginating septum that will eventually separate the two daughter cells (6,26). FtsZ both shares biochemical properties with and has structural similarities to eukaryotic tubulins. Both bind and hydrolyze GTP, polymerize to form tubules in a GTP-dependent manner, and are involved in cytoskeletal processes in the cell during cell division (7,10,31,32,37). All identified FtsZ proteins from eubacteria contain a conserved N terminus that carries the tubulin-like GTP-binding motif and a hydrophilic, variable C terminus.Although the role of FtsZ in cytokinesis differs from the actin-mediated cytokinesis in eukaryotic cells, the biochemical and amino acid sequence data have led to the proposal that FtsZ is a prokaryotic version of tubulin (14). Since the origins of the eukaryotic cytoskeleton are unknown, an intriguing hypothesis is that FtsZ evolved into tubulin. Since it is believed that the archaea and eucarya diverged after the divergence of archaea from bacteria, then identification of an FtsZ protein in an archaebacterial species might shed light on this evolutionary question (18,21). Because archaebacteria in general have a prokaryotic cellular organization similar to that of eubacteria, it is reasonable to propose that their cell division requires an FtsZ homolog derived from the common ancestor of all living cells (44).To gain insight into FtsZ evolution and diversity, we have isolated and determined the nucleotide sequence of an ftsZ gene from the extremely halophilic archaebacterium Halobacterium salinarium, which grows as long, rod-shaped cells. We show that H. salinarium ftsZ is remarkably similar to the eubacterial versions, particularly in the region most similar to tubulins. An alignment of the H. salinarium FtsZ sequence with those of eubacterial FtsZ proteins and tubulins suggests that H. salinarium FtsZ is more related to tubulin than are the eubacterial FtsZs, supporting the idea that tubulin may have evolved from FtsZ. We also show that H. salinarium ftsZ is not flanked by genes normally found adjacent to several known eubacterial ftsZ genes. Finally, we show that expression...

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The wall of bacteria serves the roles that mechano-proteins do in eukaryotes

Cited by 13 publications

References 27 publications

Electric fields induce curved growth of Enterobacter cloacae, Escherichia coli, and Bacillus subtilis cells: implications for mechanisms of galvanotropism and bacterial growth

Electric fields induce curved growth of Enterobacter cloacae, Escherichia coli, and Bacillus subtilis cells: implications for mechanisms of galvanotropism and bacterial growth

Patchiness of murein insertion into the sidewall of Escherichia coli

Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarium: implications for the evolution of FtsZ and tubulin

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