Abstract
Bacteria belonging to the orders Bacillales and Clostridiales form spores in response to nutrient starvation. From a simplified morphological perspective, the spore can be considered as comprising a central protoplast or core, that is, enveloped sequentially by an inner membrane (IM), a peptidoglycan cortex, an outer membrane, and a proteinaceous coat. All of these structures are characterized by unique morphological and/or structural features, which collectively confer metabolic dormancy and properties of environmental resistance to the quiescent spore. These properties are maintained until the spore is stimulated to germinate, outgrow and form a new vegetative cell. Spore germination comprises a series of partially overlapping biochemical and biophysical events – efflux of ions from the core, rehydration and IM reorganization, disassembly of cortex and coat – all of which appear to take place in the absence of de novo ATP and protein synthesis. If the latter points are correct, why then do spores of all species examined to date contain a diverse range of mRNA molecules deposited within the spore core? Are some of these molecules “functional,” serving as translationally active units that are required for efficient spore germination and outgrowth, or are they just remnants from sporulation whose sole purpose is to provide a reservoir of ribonucleotides for the newly outgrowing cell? What is the fate of these molecules during spore senescence, and indeed, are conditions within the spore core likely to provide any opportunity for changes in the transcriptional profile of the spore during dormancy? This review encompasses a historical perspective of spore ribonucleotide biology, from the earliest biochemical led analyses – some of which in hindsight have proved to be remarkably prescient – through the transcriptomic era at the turn of this century, to the latest next generation sequencing derived insights. We provide an overview of the key literature to facilitate reasoned responses to the aforementioned questions, and many others, prior to concluding by identifying the major outstanding issues in this crucial area of spore biology.
Highlights
Spores are formed by some Firmicutes species, the most wellstudied being those of the Bacillales, studies on spores of Clostridiales species are increasing (Tan and Ramamurthi, 2014; Setlow and Johnson, 2019; Shen et al, 2019)
The overall picture that emerged from the work noted above in 2006–2016 was that: (i) spores appeared to have many 100s of different mRNA species, (ii) some of these spore mRNAs are synthesized late in spore formation, and might be “left over” when the water content in the developing spore drops from 80% of wet wt to
There is the question of when ATP becomes available in the developing spore, and as noted in section The Early Years, this appears to begin at most very late in spore germination, and perhaps not until this process is complete and spore core water content rises to the 80% of wet wt in growing cells
Summary
Spores are formed by some Firmicutes species, the most wellstudied being those of the Bacillales, studies on spores of Clostridiales species are increasing (Tan and Ramamurthi, 2014; Setlow and Johnson, 2019; Shen et al, 2019). There is much applied interest in spore resistance and germination, the latter largely because a germinated spore has lost the high resistance of the dormant spore, and is easy to kill (Setlow and Johnson, 2019; Buhr et al, 2020) Together, both the basic science and applied interests in spores’ formation, properties, and germination has made this one of the best studied developmental system in biology, with definitive work going back many years
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