scholarly journals The evolution of bacterial shape complexity by a curvature-inducing module

Author(s):  
Nicholas R. Martin ◽  
Edith Blackman ◽  
Benjamin P. Bratton ◽  
Thomas M. Bartlett ◽  
Zemer Gitai

AbstractBacteria can achieve a staggering diversity of cell shapes that promote critical functions like growth, motility, and virulence1-4. Previous studies suggested that bacteria establish complex shapes by co-opting the core machineries essential for elongation and division5,6. In contrast, we discovered a two-protein module, CrvAB, that can curve bacteria autonomously of the major elongation and division machinery by forming a dynamic, asymmetrically-localized structure in the periplasm. CrvAB is essential for curvature in its native species, Vibrio cholerae, and is sufficient to curve multiple heterologous species spanning 2.5 billion years of evolution. Thus, modular shape determinants can promote the evolution of morphological complexity independently of existing cell shape regulation.

2019 ◽  
Author(s):  
Cole Zmurchok ◽  
William R. Holmes

ABSTRACTIt is well known that cells exhibit a variety of morphologically distinct responses to their environments that manifest in their cell shape. Some protrude uniformly to increase substrate contacts, others are broadly contrac-tile, some polarize to facilitate migration, and yet others exhibit mixtures of these responses. Prior imaging studies have identified a discrete collection of shapes that the majority of cells display and have demonstrated links between those shapes and activity levels of the cytoskeletal regulators Rho GTPases. Here we use a novel computational modeling approach to demonstrate that well known Rho GTPase signaling dynamics naturally give rise to this diverse but discrete (rather than continuum) set of morphologies. Specifically, the combination of auto-activation and mutually-antagonistic crosstalk between GTPases along with the conservative membrane (un)binding dynamics readily explain at least 6 of the 7 commonly observed morphologies. We further use this methodology to map the entire parameter space of this model and show that in appropriate regimes, individual parameter sets give rise to a variety of different morphologies. This provides an explanation for how seemingly similar cells of the same fate derived from the same population can exhibit a diverse array of cell shapes in imaging studies. These results thus demonstrate that Rho GTPases form the core of a cytoskeletal regulatory system governing cell shape, further supporting the picture that they act as a central signaling hub determining how cells respond to their environmental context.


1985 ◽  
Vol 74 (1) ◽  
pp. 219-237
Author(s):  
C.L. Lachney ◽  
T.A. Lonergan

The role of cytoplasmic microtubules in a recently reported biological clock-controlled rhythm in cell shape of the alga Euglena gracilis (strain Z) was examined using indirect immunofluorescence microscopy. The resulting fluorescent patterns indicated that, unlike many other cell systems, Euglena cells apparently change from round to long to round cell shape without associated cytoplasmic microtubule assembly and disassembly. Instead, the different cell shapes were correlated with microtubule patterns, which suggested that movement of stable microtubules to accomplish cell shape changes. In live intact cells, these microtubules were demonstrated by immunofluorescence to be stable to lowered temperature and elevated intracellular Ca2+ levels, treatments that are commonly used to depolymerize microtubules. In cells extracted in detergent at low temperature or in the presence of elevated Ca2+ levels, the fluorescent image of the microtubules was disrupted. Transmission electron microscopy confirmed the loss of one subset of pellicle microtubules. The difference in microtubule stability to these agents between live intact cells and cells extracted in detergent suggested the presence of a microtubule-stabilizing factor in live cells, which is released from the cell by extraction with detergent, thereby permitting microtubule depolymerization by Ca2+ or lowered temperature. The calmodulin antagonist trifluoperazine prevented the Ca2+-induced disruption of the fluorescent microtubule pattern in cells extracted in detergent. These results implied the involvement of calmodulin in the sensitivity to Ca2+ of the microtubules of cells extracted in detergent.


mBio ◽  
2019 ◽  
Vol 10 (4) ◽  
Author(s):  
Aurore Fleurie ◽  
Abdelrahim Zoued ◽  
Laura Alvarez ◽  
Kelly M. Hines ◽  
Felipe Cava ◽  
...  

ABSTRACTBolA family proteins are conserved in Gram-negative bacteria and many eukaryotes. While diverse cellular phenotypes have been linked to this protein family, the molecular pathways through which these proteins mediate their effects are not well described. Here, we investigated the roles of BolA family proteins inVibrio cholerae, the cholera pathogen. LikeEscherichia coli,V. choleraeencodes two BolA proteins, BolA and IbaG. However, in marked contrast toE. coli, wherebolAis linked to cell shape andibaGis not, inV. cholerae,bolAmutants lack morphological defects, whereasibaGproved critical for the generation and/or maintenance of the pathogen’s morphology. Notably, the bizarre-shaped, multipolar, elongated, and wide cells that predominated in exponential-phase ΔibaGV. choleraecultures were not observed in stationary-phase cultures. TheV. choleraeΔibaGmutant exhibited increased sensitivity to cell envelope stressors, including cell wall-acting antibiotics and bile, and was defective in intestinal colonization. ΔibaGV. choleraehad reduced peptidoglycan and lipid II and altered outer membrane lipids, likely contributing to the mutant’s morphological defects and sensitivity to envelope stressors. Transposon insertion sequencing analysis ofibaG’s genetic interactions suggested thatibaGis involved in several processes involved in the generation and homeostasis of the cell envelope. Furthermore, copurification studies revealed that IbaG interacts with proteins containing iron-sulfur clusters or involved in their assembly. Collectively, our findings suggest thatV. choleraeIbaG controls cell morphology and cell envelope integrity through its role in biogenesis or trafficking of iron-sulfur cluster proteins.IMPORTANCEBolA-like proteins are conserved across prokaryotes and eukaryotes. These proteins have been linked to a variety of phenotypes, but the pathways and mechanisms through which they act have not been extensively characterized. Here, we unraveled the role of the BolA-like protein IbaG in the cholera pathogenVibrio cholerae. The absence of IbaG was associated with dramatic changes in cell morphology, sensitivity to envelope stressors, and intestinal colonization defects. IbaG was found to be required for biogenesis of several components of theV. choleraecell envelope and to interact with numerous iron-sulfur cluster-containing proteins and factors involved in their assembly. Thus, our findings suggest that IbaG governsV. choleraecell shape and cell envelope homeostasis through its effects on iron-sulfur proteins and associated pathways. The diversity of processes involving iron-sulfur-containing proteins is likely a factor underlying the range of phenotypes associated with BolA family proteins.


2019 ◽  
Vol 98 (11) ◽  
pp. 1253-1261 ◽  
Author(s):  
S. Yamada ◽  
R. Lav ◽  
J. Li ◽  
A.S. Tucker ◽  
J.B.A. Green

Tooth germs undergo a series of dynamic morphologic changes through bud, cap, and bell stages, in which odontogenic epithelium continuously extends into the underlying mesenchyme. During the transition from the bud stage to the cap stage, the base of the bud flattens and then bends into a cap shape whose edges are referred to as “cervical loops.” Although genetic mechanisms for cap formation have been well described, little is understood about the morphogenetic mechanisms. Computer modeling and cell trajectory tracking have suggested that the epithelial bending is driven purely by differential cell proliferation and adhesion in different parts of the tooth germ. Here, we show that, unexpectedly, inhibition of cell proliferation did not prevent bud-to-cap morphogenesis. We quantified cell shapes and actin and myosin distributions in different parts of the tooth epithelium at the critical stages and found that these are consistent with basal relaxation in the forming cervical loops and basal constriction around enamel knot at the center of the cap. Inhibition of focal adhesion kinase, which is required for basal constriction in other systems, arrested the molar explant morphogenesis at the bud stage. Together, these results show that the bud-to-cap transition is largely proliferation independent, and we propose that it is driven by classic actomyosin-driven cell shape–dependent mechanisms. We discuss how these results can be reconciled with the previous models and data.


2016 ◽  
Vol 113 (14) ◽  
pp. E2066-E2072 ◽  
Author(s):  
Knut Drescher ◽  
Jörn Dunkel ◽  
Carey D. Nadell ◽  
Sven van Teeffelen ◽  
Ivan Grnja ◽  
...  

Many bacterial species colonize surfaces and form dense 3D structures, known as biofilms, which are highly tolerant to antibiotics and constitute one of the major forms of bacterial biomass on Earth. Bacterial biofilms display remarkable changes during their development from initial attachment to maturity, yet the cellular architecture that gives rise to collective biofilm morphology during growth is largely unknown. Here, we use high-resolution optical microscopy to image all individual cells in Vibrio cholerae biofilms at different stages of development, including colonies that range in size from 2 to 4,500 cells. From these data, we extracted the precise 3D cellular arrangements, cell shapes, sizes, and global morphological features during biofilm growth on submerged glass substrates under flow. We discovered several critical transitions of the internal and external biofilm architectures that separate the major phases of V. cholerae biofilm growth. Optical imaging of biofilms with single-cell resolution provides a new window into biofilm formation that will prove invaluable to understanding the mechanics underlying biofilm development.


2021 ◽  
Author(s):  
Zelin Li ◽  
Jianfeng Cao ◽  
Zhongying Zhao ◽  
Hong Yan

Abstract Background: The developmental process is featured by fabulous morphogenesis in multicellular organisms. Describing morphological changes quantitatively concretes the way to investigating both intra and inter cell regulations on cell fate. While Caenorhabditis elegans has been used as a model for cell and development studies for a long time, the exploration of how cell shape is precisely controlled keeps obscured by the lack of methods to model morphological features. Currently, in order to characterize the features of cell shape involved in cell migration and differentiation, there is an increasing demand in analyzing cell shape systematically, especially when many works have contributed to cell reconstruction. Results: In this work, Spherical harmonics and Principal component analysis integrated Cell Shape quantification Models (SPCSMs) is proposed to represent cell shapes in a low-dimensional shape space. SPCSMs incorporates a complete pipeline to quantify cell shapes and analyze their morphological phenotypes in three dimensional (3D) reconstructions. Based on the framework, we extract biological patterns in the lineage of C. elegans embryo before 350-cell stage, during which all hypodermis cells deformed like a funnel and can be recognized by this shape pattern. Finally, SPCSMs is compared with two cell shape representation methods, which substantiates the effectiveness and robustness of our method. Conclusion: SPCSMs provides a general method to decribe shapes in low-dimensional shape space with compact parameters. It can quantify the shapes of cells from single-cell resolution images obtained over one-minute intervals, making it possible for the recognition of developmental patterns in cell lineages. SPCSMs is expected to be an effective model for biologists to explore the relationships between the shapes of cells and their fates.


2020 ◽  
Author(s):  
Aliaksei S Vasilevich ◽  
Steven S Vermeulen ◽  
Marloes Kamphuis ◽  
Nadia Roumans ◽  
Said Eroume ◽  
...  

Learning rules by which cell shape impacts cell function would enable control of cell physiology and fate in medical applications, particularly, on the interface of cells and material of the implants. We defined the phenotypic response of human bone marrow-derived mesenchymal stem cells (hMSCs) to 2176 randomly generated surface topographies by probing basic functions such as migration, proliferation, protein synthesis, apoptosis, and differentiation using quantitative image analysis. Clustering the surfaces into 28 archetypical cell shapes, we found a very strict correlation between cell shape and physiological response and selected seven cell shapes to describe the molecular mechanism leading to phenotypic diversity. Transcriptomics analysis revealed a tight link between cell shape, molecular signatures, and phenotype. For instance, proliferation is strongly reduced in cells with limited spreading, resulting in down-regulation of genes involved in the G2/M cycle and subsequent quiescence, whereas cells with large filopodia are related to activation of early response genes and inhibition of the osteogenic process. Thus, we have started to unravel the open question of how cell function follows cell shape. This will allow designing implants that can actively regulate cellular, molecular signalling through cell shape. Here we are proposing an approach to tackle this question.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Aliaksei S. Vasilevich ◽  
Steven Vermeulen ◽  
Marloes Kamphuis ◽  
Nadia Roumans ◽  
Said Eroumé ◽  
...  

Abstract Learning rules by which cell shape impacts cell function would enable control of cell physiology and fate in medical applications, particularly, on the interface of cells and material of the implants. We defined the phenotypic response of human bone marrow-derived mesenchymal stem cells (hMSCs) to 2176 randomly generated surface topographies by probing basic functions such as migration, proliferation, protein synthesis, apoptosis, and differentiation using quantitative image analysis. Clustering the surfaces into 28 archetypical cell shapes, we found a very strict correlation between cell shape and physiological response and selected seven cell shapes to describe the molecular mechanism leading to phenotypic diversity. Transcriptomics analysis revealed a tight link between cell shape, molecular signatures, and phenotype. For instance, proliferation is strongly reduced in cells with limited spreading, resulting in down-regulation of genes involved in the G2/M cycle and subsequent quiescence, whereas cells with large filopodia are related to activation of early response genes and inhibition of the osteogenic process. In this paper we were aiming to identify a universal set of genes that regulate the material-induced phenotypical response of human mesenchymal stem cells. This will allow designing implants that can actively regulate cellular, molecular signalling through cell shape. Here we are proposing an approach to tackle this question.


2019 ◽  
Vol 73 (1) ◽  
pp. 457-480 ◽  
Author(s):  
Jennifer A. Taylor ◽  
Sophie R. Sichel ◽  
Nina R. Salama

Helical cell shape appears throughout the bacterial phylogenetic tree. Recent exciting work characterizing cell shape mutants in a number of curved and helical Proteobacteria is beginning to suggest possible mechanisms and provide tools to assess functional significance. We focus here on Caulobacter crescentus, Vibrio cholerae, Helicobacter pylori, and Campylobacter jejuni, organisms from three classes of Proteobacteria that live in diverse environments, from freshwater and saltwater to distinct compartments within the gastrointestinal tract of humans and birds. Comparisons among these bacteria reveal common themes as well as unique solutions to the task of maintaining cell curvature. While motility appears to be influenced in all these bacteria when cell shape is perturbed, consequences on niche colonization are diverse, suggesting the need to consider additional selective pressures.


2019 ◽  
Vol 115 (1) ◽  
Author(s):  
Payam Haftbaradaran Esfahani ◽  
Zaher ElBeck ◽  
Sven Sagasser ◽  
Xidan Li ◽  
Mohammad Bakhtiar Hossain ◽  
...  

AbstractCardiomyocytes undergo considerable changes in cell shape. These can be due to hemodynamic constraints, including changes in preload and afterload conditions, or to mutations in genes important for cardiac function. These changes instigate significant changes in cellular architecture and lead to the addition of sarcomeres, at the same time or at a later stage. However, it is currently unknown whether changes in cell shape on their own affect gene expression and the aim of this study was to fill that gap in our knowledge. We developed a single-cell morphotyping strategy, followed by single-cell RNA sequencing, to determine the effects of altered cell shape in gene expression. This enabled us to profile the transcriptomes of individual cardiomyocytes of defined geometrical morphotypes and characterize them as either normal or pathological conditions. We observed that deviations from normal cell shapes were associated with significant downregulation of gene expression and deactivation of specific pathways, like oxidative phosphorylation, protein kinase A, and cardiac beta-adrenergic signaling pathways. In addition, we observed that genes involved in apoptosis of cardiomyocytes and necrosis were upregulated in square-like pathological shapes. Mechano-sensory pathways, including integrin and Src kinase mediated signaling, appear to be involved in the regulation of shape-dependent gene expression. Our study demonstrates that cell shape per se affects the regulation of the transcriptome in cardiac myocytes, an effect with possible implications for cardiovascular disease.


Sign in / Sign up

Export Citation Format

Share Document