Glutamate catabolism during sporulation determines the success of the future spore germination

Rao, Lei; Zhou, Bing; Serruya, Raphael; Moussaieff, Arieh; Sinai, Lior; Ben-Yehuda, Sigal

doi:10.1016/j.isci.2022.105242

Cited by 9 publications

(23 citation statements)

References 65 publications

(101 reference statements)

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“…Moreover, molecular events, including dephosphorylation and transcription, precede Ca-DPA release and are critical for its initiation (Zhou et al, 2022(Zhou et al, , 2019, whereas translation plays an important role in promoting germination events following Ca-DPA release (Sinai et al, 2015;Zhou et al, 2022). A recent finding that ATP levels are highly correlated with the speed of Ca-DPA release during germination (Rao et al, 2022) also reinforces the perspective of molecular event occurrence and importance for germination. Although these new findings remain controversial, they provide new insights into the germination process.…”

Section: Concluding Remarks and Future Perspectivesmentioning

confidence: 78%

“…Unfortunately, the mechanism underlying the initiation of these molecular events that regulate Ca‐DPA release remains unclear. Recently, it has been shown that ATP levels in dormant spores are correlated with the speed of Ca‐DPA release during germination (Rao et al., 2022), indicating that ATP may participate in signal transduction from GerA to SpoVA protein channels. As the low ATP level in spores is incapable of directly energizing molecular events, such as transcription, the involvement of ATP in germination is likely related to signal transduction reactions, such as phosphorylation (Shah et al., 2008).…”

Section: Overview Of Germinants‐induced Spore Germination Via Grsmentioning

confidence: 99%

“…Recently, the application of AlphaFold 2 to identify the spatial structure of GRs or Ca‐DPA channel proteins revealed their possible mode of action during germination (Amon et al., 2022; Artzi et al., 2021; Y. Gao, Barajas‐Ornelas, et al., 2022), and the finding that potassium ion release integrates germination signals sheds light on the mystery process of signal transduction following GRs activation (Kikuchi et al., 2022). Moreover, the occurrence of macromolecule synthesis during germination (Sinai & Ben‐Yehuda, 2016; Sinai et al., 2015; Zhou et al., 2022, 2019) and the proposed high correlation between ATP levels and spore germination capability (Rao et al., 2022) have been demonstrated, but these concepts are controversial (Boone & Driks, 2016; Korza et al., 2017, 2023, 2016; Swarge, Abhyankar, et al., 2020; Swarge, Nafid, et al., 2020). Nevertheless, these findings and debates provide new insights into the molecular regulatory mechanisms of germination.…”

Section: Introductionmentioning

confidence: 99%

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The underlying mechanism of bacterial spore germination: An update review

Zhang

Guo

Wang

et al. 2023

Comp Rev Food Sci Food Safe

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Bacterial spores are highly resilient and universally present on earth and can irreversibly enter the food chain to cause food spoilage or foodborne illness once revived to resume vegetative growth. Traditionally, extensive thermal processing has been employed to efficiently kill spores; however, the relatively high thermal load adversely affects food quality attributes. In recent years, the germination-inactivation strategy has been developed to mildly kill spores based on the circumstance that germination can decrease spore-resilient properties.However, the failure to induce all spores to geminate, mainly owing to the heterogeneous germination behavior of spores, hampers the success of applying this strategy in the food industry. Undoubtedly, elucidating the detailed germination pathway and underlying mechanism can fill the gap in our understanding of germination heterogeneity, thereby facilitating the development of full-scale germination regimes to mildly kill spores. In this review, we comprehensively discuss the mechanisms of spore germination of Bacillus and Clostridium species, and update the molecular basis of the early germination events, for example, the activation of germination receptors, ion release, Ca-DPA release, and molecular events, combined with the latest research evidence. Moreover, high hydrostatic pressure (HHP), an advanced non-thermal food processing technology, can also trigger spore germination, providing a basis for the application of a germinationinactivation strategy in HHP processing. Here, we also summarize the diverse germination behaviors and mechanisms of spores of Bacillus and Clostridium species under HHP, with the aim of facilitating HHP as a mild processing technology with possible applications in food sterilization.

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Section: Concluding Remarks and Future Perspectivesmentioning

confidence: 78%

Section: Overview Of Germinants‐induced Spore Germination Via Grsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The underlying mechanism of bacterial spore germination: An update review

Zhang

Guo

Wang

et al. 2023

Comp Rev Food Sci Food Safe

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“…RocG-mediated glutamate metabolism, rather than Ald-mediated alanine metabolism, is essential for ensuring both the sporulation efficiency and the spore quality, likely through energy supply As the Ald and RocG mediated alanine and glutamate metabolisms were proposed as potential energy sources for sporulation (14,15), we hypothesized that these two metabolic pathways contribute to energy support independently. If this was true, excessive complementation of either metabolic pathway should be capable of rescuing the sporulation defect observed in the Δald ΔrocG mutant.…”

Section: Alanine and Glutamate Metabolism Collaboratively Regulate Sp...mentioning

confidence: 99%

“…Sporulation is recognized as an energy-intensive biological process (12), implying the importance of energy supply in promoting its progress. Studies have suggested that amino acid metabolism, such as glutamate and alanine catabolism, may serve as potential energy sources driving sporulation (13)(14)(15). However, the mechanisms regulating these processes during sporulation remain unclear.…”

Section: Introductionmentioning

confidence: 99%

Alanine and glutamate catabolism ensure proper sporulation by preventing premature germination and providing energy respectively

Lyu,

Zhang,

Yang

et al. 2024

Preprint

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Sporulation as a typical bacterial differentiation process has been studied for decades, and the morphological events along with the molecular regulation mechanisms are relatively clear. However, two other important aspects of sporulation, (i) how sporulating cells gain energy sources to fuel sporulation proceeding, and (ii) how generated spores maintain dormancy during the whole sporulation process lack research. Here, we found that RocG-mediated glutamate metabolism was crucial for driving mother cell lysis to succeed sporulation, likely by providing energy metabolites ATP. Interestingly, high-level rocG expression generated excessively high ATP contents in sporulating cells, which caused adverse effects on the properties of the future spores, e.g. faster germination efficiency, lower DPA content along with decreased heat resistance. Moreover, we revealed that Ald-mediated alanine metabolism decreased the typical germinant L-alanine concentration to a certain level in the sporulating environment, thus avoiding premature germination and maintaining spore dormancy. Our data inferred that sporulation was a highly orchestrated and exquisite biological process requiring the balance of diverse metabolism pathways, hence ensuring both the sporulation completion and the high quality of generated spores.

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