Arginine dephosphorylation propels spore germination in bacteria

Bing Zhou, Maja Semanjski, Natalie Orlovetskie, Saurabh Bhattacharya, Sima Alon, Liron Argaman, Nayef Jarrous, Yan Zhang, Boris Macek, Lior Sinai*, Sigal Ben-Yehuda

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

28 Scopus citations

Abstract

Bacterial spores can remain dormant for years but possess the remarkable ability to germinate, within minutes, once nutrients become available. However, it still remains elusive how such instant awakening of cellular machineries is achieved. Utilizing Bacillus subtilis as a model, we show that YwlE arginine (Arg) phosphatase is crucial for spore germination. Accordingly, the absence of the Arg kinase McsB accelerated the process. Arg phosphoproteome of dormant spores uncovered a unique set of Arg-phosphorylated proteins involved in key biological functions, including translation and transcription. Consequently, we demonstrate that during germination, YwlE dephosphorylates an Arg site on the ribosome-associated chaperone Tig, enabling its association with the ribosome to reestablish translation. Moreover, we show that Arg dephosphorylation of the housekeeping σ factor A (SigA), mediated by YwlE, facilitates germination by activating the transcriptional machinery. Subsequently, we reveal that transcription is reinitiated at the onset of germination and its recommencement precedes that of translation. Thus, Arg dephosphorylation elicits the most critical stages of spore molecular resumption, placing this unusual post-translational modification as a major regulator of a developmental process in bacteria.

Original languageAmerican English
Pages (from-to)14228-14237
Number of pages10
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number28
DOIs
StatePublished - 2019

Bibliographical note

Funding Information:
We thank Silke Wahl for preparing samples for MS measurements. We are grateful to the members of the S.B.-Y. laboratory for valuable discussions and comments. We thank P. Setlow (University of Connecticut) for generously providing antibodies against germination receptors. This work was supported by the European Research Council Advanced Grant (339984) and the Israel Science Foundation (774/16) awarded to S.B.-Y., and by The German-Israeli Foundation (GIF) (Grant I-1464-416.13/2018) awarded to S.B.-Y. and B.M. B.Z. was funded by the Key Project of National Natural Science Foundation of China (NSFC) (31530058) and China Scholarship Council (CSC) scholarship (201606350068).

Funding Information:
ACKNOWLEDGMENTS. We thank Silke Wahl for preparing samples for MS measurements. We are grateful to the members of the S.B.-Y. laboratory for valuable discussions and comments. We thank P. Setlow (University of Connecticut) for generously providing antibodies against germination receptors. This work was supported by the European Research Council Advanced Grant (339984) and the Israel Science Foundation (774/16) awarded to S.B.-Y., and by The German-Israeli Foundation (GIF) (Grant I-1464-416.13/2018) awarded to S.B.-Y. and B.M. B.Z. was funded by the Key Project of National Natural Science Foundation of China (NSFC) (31530058) and China Scholarship Council (CSC) scholarship (201606350068).

Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.

Keywords

  • Arginine phosphorylation
  • Bacillus subtilis
  • Germination
  • Spore dormancy

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