Abstract
ABSTRACTDividing cells of the coccoid Gram-positive bacterium Staphylococcus aureus undergo extremely rapid (millisecond) daughter cell separation (DCS) driven by mechanical crack propagation, a strategy that is very distinct from the gradual, enzymatically driven cell wall remodeling process that has been well described in several rod-shaped model bacteria. To determine if other bacteria, especially those in the same phylum (Firmicutes) or with similar coccoid shapes as S. aureus, might use a similar mechanically driven strategy for DCS, we used high-resolution video microscopy to examine cytokinesis in a phylogenetically wide range of species with various cell shapes and sizes. We found that fast mechanically driven DCS is rather rare in the Firmicutes (low G+C Gram positives), observed only in Staphylococcus and its closest coccoid relatives in the Macrococcus genus, and we did not observe this division strategy among the Gram-negative Proteobacteria. In contrast, several members of the high-G+C Gram-positive phylum Actinobacteria (Micrococcus luteus, Brachybacterium faecium, Corynebacterium glutamicum, and Mycobacterium smegmatis) with diverse shapes ranging from coccoid to rod all undergo fast mechanical DCS during cell division. Most intriguingly, similar fast mechanical DCS was also observed during the sporulation of the actinobacterium Streptomyces venezuelae.
Highlights
Dividing cells of the coccoid Gram-positive bacterium Staphylococcus aureus undergo extremely rapid daughter cell separation (DCS) driven by mechanical crack propagation, a strategy that is very distinct from the gradual, enzymatically driven cell wall remodeling process that has been well described in several rod-shaped model bacteria
In many well-characterized bacteria, including Escherichia coli and Caulobacter crescentus, DCS is achieved by gradual symmetric constriction coupled with construction of new hemispherical poles at the junction between the presumptive daughters [1, 2], while other bacteria such as Bacillus subtilis initially build a flat septum that undergoes gradual resolution around the periphery to allow symmetric DCS [3]
In order to determine whether this mechanism of fast mechanical DCS is unique to S. aureus or found among other bacterial species, we surveyed representative species across three major bacterial phyla, including the Firmicutes, Actinobacteria, and Proteobacteria (Gram negatives), with particular attention to include diverse species that share the coccoid shape of S. aureus [6] (Fig. 1; see Table S1 in the supplemental material)
Summary
Fast Mechanically Driven Daughter Cell Separation Is Widespread in Actinobacteria. Theriota,b,c Department of Biochemistry, Stanford University School of Medicine, Stanford, California, USAa; Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, California, USAb; Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, California, USAc
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