Editorial: The Bacterial Cell: Coupling between Growth, Nucleoid Replication, Cell Division, and Shape

摘要

Introduction The nucleoid and cell envelope are two unique macromolecules that define a bacterium. To ensure that the essential genetic information is carried faithfully from one generation to the next their duplications must be coupled. Research dating back more than half a century established that this is realized at the level of replication-initiation and cell division. These seminal investigations demonstrated that cell size determines when replication starts and that, in turn, the progress in replication determines when cell division processes occur. Moreover, cell division was later established to be spatially controlled by the structure and position of the nucleoid. Despite extensive research over the past 60 years, detailed understanding on how these spatio-temporal couplings are realized at the molecular level is yet to emerge. The aim in creating this e-book has been to bring together scientists from different backgrounds spanning biology, chemistry and physics to address these fundamental mechanisms in a bacterial cell. The book starts with a historical overview of the research that has established the field. It then advances through series of reviews and research articles devoted to the nucleoid, cell envelope, and their temporary hyper-structures, the orisome, replisome, and divisome. Finally, coupling between them is discussed in the last set of contributions. Historical overview The first evidence of coupling between duplications of the bacterial cell envelope and the nucleoid was revealed in the 1950s and 1960s. Milestones in this research were demonstrations of replication initiation at a constant cell mass per oriC and constant C and D , dissociated from growth dynamics, where C denotes replication time and D time from replication–termination to the separation between the subsequent daughter cells. These findings form the basis of our understanding of physiology of bacterial cell duplication and guide the current research. Historical accounts of how these ideas came about are covered in the e-book by the scientists who were instrumental in developing these concepts ( Hanawalt ; Helmstetter ; Schaechter ; Zaritsky and Woldringh ). The articles dwell on scientific achievements and personal experiences, which endows the new generation of scientists valuable perspective. The nucleoid The nucleoid as a central macromolecular complex of bacterial cell harbors several hyper-structures that are essential to its organization and coupling to the envelope. These hyperstructures include orisomes, replisomes, transcriptional assemblies, and transertional linkages that connect DNA through transcribed mRNA and coupled translated membrane protein to the plasma membrane of the cell. Leonard and Grimwade describe how a timing mechanism, based on unwinding of oriC by the highly conserved DnaA, starts the orisome assembly. Next, the composition and architecture of the replisome is discussed with emphasis on dynamics and stability during its “journey” from origin to terminus ( Beattie and Reyes-Lamothe ). Despite detailed knowledge of the orisome and replisome components from both in vivo and in vitro studies, we have little understanding of how these structures are spatially correlated and physically positioned in the cell. Regarding this aspect, Woldringh et al. present new data on movement and positioning of fluorescently tagged chromosome arms in slow-growing Escherichia coli cells. Remarkably, the observed segregation patterns were similar to those obtained during run-off DNA replication in rifampicin-inhibited cells, suggesting that segregation is passively driven by de novo DNA synthesis.Analysis of super-resolution fluorescence images of ribosomes and RNA polymerase in rapidly growing E. coli cells enabled Bakshi et al. to propose a “translation-centric” view of the compartmentalization of cytoplasm and nucleoid. Their observations are supported by time-dependent effects of rifampicin and chloramphenicol inhibition on nucleoid-ribosome morphology and could be simulated by a physical model assuming entropic contributions and excluded volume interactions between ribosomal subunits and DNA. In a more “transcription-centric” view of nucleoid morphology, Jin et al. describe how multiple ribosomal RNA operons form a nucleolus-like structure at the periphery of the nucleoid.How these cytological observations of nucleoid behavior can be understood in a more quantitative, physical perspective remains to be seen. For instance, following a well-known concept in material science, Scolari et al. provoke us to think of the bacterial nucleoid as a smart polymer—a gel-like substance that shows a variety of responsive behaviors to external stimuli such as temperature, pH, and ionic strength.Coupling between mass growth and chromosome replication has been studied for six decades using mutants defective in thymine biosynthesis ( Guzmán and Martín ). Yet, what leads to thymineless death and whether this process is active