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Special Issue "Novel Principles and Methods in Bacterial Cell Cycle Physiology: Celebrating the Charles E. Helmstetter Prize in 2022"

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A special issue of Life (ISSN 2075-1729). This special issue belongs to the section "Biochemistry, Biophysics and Computational Biology".

Deadline for manuscript submissions: closed (30 April 2023) | Viewed by 4542

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Special Issue Editors

Prof. Dr. Arieh Zaritsky

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Guest Editor

Ben-Gurion University of the Negev, Life/Natural Sciences, Be’er-Sheva, Israel
Interests: Bacterial Cell-Cycle Physiology; Biological Control of Insect Pests

Prof. Dr. Vic Norris

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Guest Editor

Theoretical Biology Unit, EA 4312, University of Rouen, 76821 Mont-Saint-Aignan, France
Interests: integrative approaches to the bacterial cell cycle, origins of life; biotechnology; systems biology

Prof. Dr. Itzhak Fishov

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Guest Editor

Department of Life Sciences, Ben-Gurion University of the Negev, Be'er Sheva, Israel
Interests: bacterial cell cycle; membrane domains; protein-membrane interactions; nucleoid morphology and dynamics

Special Issue Information

Dear Colleagues,

Understanding the bacterial cell cycle is fundamental to understanding the physiology of the cell and, hence, to all the fields that depend on microbial physiology, such as clinical microbiology, industrial biotechnology, the origins of life, xenobiology, environmental microbiology, and synthetic biology.

Charles E. Helmstetter is widely acknowledged as the person who provided the experimental and theoretical bases for our understanding of the bacterial cell cycle. Indeed, the ensemble of his ingenious investigations, designed and performed by himself from the 1960s to the end of the century, is considered to have defined the field, which is exceptional in science.

A group of specialists in this field collaborated to create The Charles E Helmstetter Prize for Groundbreaking Research in Bacterial Cell Cycle Physiology. The Prize will be awarded every two years. The aim of the present Special Issue is to celebrate the The Charles E Helmstetter Prize in 2022. The first three recipients have been selected and will be awarded the Prize in the opening session of the EMBO Workshop “Bacterial cell biophysics: DNA replication, growth, division, size and shape” https://meetings.embo.org/event/22-bacteria-biophysics, to be held in Israel, 11–15 December 2022.

The first session of this workshop (entitled "Bacterial Physiology Comes of Age at 60") will be devoted to the Prize, to the achievements of Dr. Helmstetter and the three laureates, and to the implications stemming from their pioneering investigations. A number of scientists in the field, selected for their relationships to Helmstetter and his work, have been invited to contribute chapters; other colleagues are also welcome to submit relevant chapters.

Prof. Dr. Arieh Zaritsky
Prof. Dr. Vic Norris
Prof. Dr. Itzhak Fishov
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

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Keywords

synchrony for bacterial cell cycle
DNA replication and I-BCD periods
cell dimensions, orisome, replisome and divisome
overlapping rounds of replication
nucleoid structure and membrane domains
cell variability and individuality
thymine limitation, unbalanced growth, and thymine-less death

Published Papers (7 papers)

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Research

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Open AccessArticle

The Replicative DnaE Polymerase of Bacillus subtilis Recruits the Glycolytic Pyruvate Kinase (PykA) When Bound to Primed DNA Templates

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Life 2023, 13(4), 965; https://doi.org/10.3390/life13040965 - 07 Apr 2023

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Abstract

The glycolytic enzyme PykA has been reported to drive the metabolic control of replication through a mechanism involving PykA moonlighting functions on the essential DnaE polymerase, the DnaC helicase and regulatory determinants of PykA catalytic activity in Bacillus subtilis. The mutants of this control suffer from critical replication and cell cycle defects, showing that the metabolic control of replication plays important functions in the overall rate of replication. Using biochemical approaches, we demonstrate here that PykA interacts with DnaE for modulating its activity when the replication enzyme is bound to a primed DNA template. This interaction is mediated by the CAT domain of PykA and possibly allosterically regulated by its PEPut domain, which also operates as a potent regulator of PykA catalytic activity. Furthermore, using fluorescence microscopy we show that the CAT and PEPut domains are important for the spatial localization of origins and replication forks, independently of their function in PykA catalytic activity. Collectively, our data suggest that the metabolic control of replication depends on the recruitment of PykA by DnaE at sites of DNA synthesis. This recruitment is likely highly dynamic, as DnaE is frequently recruited to and released from replication machineries to extend the several thousand RNA primers generated from replication initiation to termination. This implies that PykA and DnaE continuously associate and dissociate at replication machineries for ensuring a highly dynamic coordination of the replication rate with metabolism. Full article

(This article belongs to the Special Issue Novel Principles and Methods in Bacterial Cell Cycle Physiology: Celebrating the Charles E. Helmstetter Prize in 2022)

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Recollections of a Helmstetter Disciple

Alan C. Leonard

Life 2023, 13(5), 1114; https://doi.org/10.3390/life13051114 - 30 Apr 2023

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Abstract

Nearly fifty years ago, it became possible to construct E. coli minichromosomes using recombinant DNA technology. These very small replicons, comprising the unique replication origin of the chromosome oriC coupled to a drug resistance marker, provided new opportunities to study the regulation of bacterial chromosome replication, were key to obtaining the nucleotide sequence information encoded into oriC and were essential for the development of a ground-breaking in vitro replication system. However, true authenticity of the minichromosome model system required that they replicate during the cell cycle with chromosome-like timing specificity. I was fortunate enough to have the opportunity to construct E. coli minichromosomes in the laboratory of Charles Helmstetter and, for the first time, measure minichromosome cell cycle regulation. In this review, I discuss the evolution of this project along with some additional studies from that time related to the DNA topology and segregation properties of minichromosomes. Despite the significant passage of time, it is clear that large gaps in our understanding of oriC regulation still remain. I discuss some specific topics that continue to be worthy of further study. Full article

(This article belongs to the Special Issue Novel Principles and Methods in Bacterial Cell Cycle Physiology: Celebrating the Charles E. Helmstetter Prize in 2022)

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Open AccessReview

Fifty-Five Years of Research on B, C and D in Escherichia coli

Charles E. Helmstetter

Life 2023, 13(4), 977; https://doi.org/10.3390/life13040977 - 10 Apr 2023

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Abstract

The basic properties of the Escherichia coli duplication process can be defined by two time periods: C, the time for a round of chromosome replication, and D, the time between the end of a round of replication and cell division. Given the durations of these periods, the pattern of chromosome replication during the cell cycle can be determined for cells growing with any doubling time. In the 55 years since these parameters were identified, there have been numerous investigations into their durations and into the elements that determine their initiations. In this review, I discuss the history of our involvement in these studies from the very beginning, some of what has been learned over the years by measuring the durations of C and D, and what might be learned with additional investigations. Full article

(This article belongs to the Special Issue Novel Principles and Methods in Bacterial Cell Cycle Physiology: Celebrating the Charles E. Helmstetter Prize in 2022)

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Open AccessReview

The Bacterial Nucleoid: From Electron Microscopy to Polymer Physics—A Personal Recollection

Conrad L. Woldringh

Life 2023, 13(4), 895; https://doi.org/10.3390/life13040895 - 28 Mar 2023

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Abstract

In the 1960s, electron microscopy did not provide a clear answer regarding the compact or dispersed organization of the bacterial nucleoid. This was due to the necessary preparation steps of fixation and dehydration (for embedding) and freezing (for freeze-fracturing). Nevertheless, it was possible to measure the lengths of nucleoids in thin sections of slow-growing Escherichia coli cells, showing their gradual increase along with cell elongation. Later, through application of the so-called agar filtration method for electron microscopy, we were able to perform accurate measurements of cell size and shape. The introduction of confocal and fluorescence light microscopy enabled measurements of size and position of the bacterial nucleoid in living cells, inducing the concepts of “nucleoid occlusion” for localizing cell division and of “transertion” for the final step of nucleoid segregation. The question of why the DNA does not spread throughout the cytoplasm was approached by applying polymer-physical concepts of interactions between DNA and proteins. This gave a mechanistic insight in the depletion of proteins from the nucleoid, in accordance with its low refractive index observed by phase-contrast microscopy. Although in most bacterial species, the widely conserved proteins of the ParABS-system play a role in directing the segregation of newly replicated DNA strands, the basis for the separation and opposing movement of the chromosome arms was proposed to lie in preventing intermingling of nascent daughter strands already in the early replication bubble. E. coli, lacking the ParABS system, may be suitable for investigating this basic mechanism of DNA strand separation and segregation. Full article

(This article belongs to the Special Issue Novel Principles and Methods in Bacterial Cell Cycle Physiology: Celebrating the Charles E. Helmstetter Prize in 2022)

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Open AccessOpinion

The Quantification of Bacterial Cell Size: Discrepancies Arise from Varied Quantification Methods

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Life 2023, 13(6), 1246; https://doi.org/10.3390/life13061246 - 24 May 2023

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Abstract

The robust regulation of the cell cycle is critical for the survival and proliferation of bacteria. To gain a comprehensive understanding of the mechanisms regulating the bacterial cell cycle, it is essential to accurately quantify cell-cycle-related parameters and to uncover quantitative relationships. In this paper, we demonstrate that the quantification of cell size parameters using microscopic images can be influenced by software and by the parameter settings used. Remarkably, even if the consistent use of a particular software and specific parameter settings is maintained throughout a study, the type of software and the parameter settings can significantly impact the validation of quantitative relationships, such as the constant-initiation-mass hypothesis. Given these inherent characteristics of microscopic image-based quantification methods, it is recommended that conclusions be cross-validated using independent methods, especially when the conclusions are associated with cell size parameters that were obtained under different conditions. To this end, we presented a flexible workflow for simultaneously quantifying multiple bacterial cell-cycle-related parameters using microscope-independent methods. Full article

(This article belongs to the Special Issue Novel Principles and Methods in Bacterial Cell Cycle Physiology: Celebrating the Charles E. Helmstetter Prize in 2022)

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Open AccessPerspective

Unbalanced Growth, the DNA Replication Cycle and Discovery of Repair Replication

Philip C. Hanawalt

Life 2023, 13(4), 1052; https://doi.org/10.3390/life13041052 - 20 Apr 2023

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Abstract

This article recounts my graduate research at Yale University (1954–1958) on unbalanced growth in Eschericia coli during thymine deprivation or following ultraviolet (UV) irradiation, with early evidence for the repair of UV-induced DNA damage. Follow-up studies in Copenhagen (1958–1960) in the laboratory of Ole Maaløe led to my discovery that the DNA replication cycle can be synchronized by inhibiting protein and RNA syntheses and that an RNA synthesis step is essential for initiation of the cycle, but not for its completion. This work set the stage for my subsequent research at Stanford University, where the repair replication of damaged DNA was documented, to provide compelling evidence for an excision-repair pathway. That universal pathway validates the requirement for the redundant information in the complementary strands of duplex DNA to ensure genomic stability. Full article

(This article belongs to the Special Issue Novel Principles and Methods in Bacterial Cell Cycle Physiology: Celebrating the Charles E. Helmstetter Prize in 2022)

Open AccessOpinion

Extending Validity of the Bacterial Cell Cycle Model through Thymine Limitation: A Personal View

Arieh Zaritsky

Life 2023, 13(4), 906; https://doi.org/10.3390/life13040906 - 29 Mar 2023

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Abstract

The contemporary view of bacterial physiology was established in 1958 at the “Copenhagen School”, culminating a decade later in a detailed description of the cell cycle based on four parameters. This model has been subsequently supported by numerous studies, nicknamed BCD (The Bacterial Cell-Cycle Dogma). It readily explains, quantitatively, the coupling between chromosome replication and cell division, size and DNA content. An important derivative is the number of replication positions n, the ratio between the time C to complete a round of replication and the cell mass doubling time τ; the former is constant at any temperature and the latter is determined by the medium composition. Changes in cell width W are highly correlated to n through the equation for so-called nucleoid complexity NC (=(2ⁿ − 1)/(ln2

\times

n)), the amount of DNA per terC (i.e., chromosome) in genome equivalents. The narrow range of potential n can be dramatically extended using the method of thymine limitation of thymine-requiring mutants, which allows a more rigorous testing of the hypothesis that the nucleoid structure is the primary source of the signal that determines W during cell division. How this putative signal is relayed from the nucleoid to the divisome is still highly enigmatic. The aim of this Opinion article is to suggest the possibility of a new signaling function for nucleoid DNA. Full article

(This article belongs to the Special Issue Novel Principles and Methods in Bacterial Cell Cycle Physiology: Celebrating the Charles E. Helmstetter Prize in 2022)

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