Integrative Analysis of Proteome and Transcriptome Dynamics during <named-content content-type="genus-species">Bacillus subtilis</named-content> Spore Revival

ABSTRACT Bacillus subtilis spores can reactivate their metabolism through germination upon contact with germinants and can develop into vegetative cells upon outgrowth. However, the mechanisms at the basis of the molecular machinery that triggers the spore germination and outgrowth processes are sti...

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Autores principales:	Bhagyashree Swarge, Wishwas Abhyankar, Martijs Jonker, Huub Hoefsloot, Gertjan Kramer, Peter Setlow, Stanley Brul, Leo J. de Koning
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Bacillus subtilis spore germination proteomics protein synthesis transcriptomics metabolic labeling Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2b386024339c4aa7b358bb6b2c8531fb
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spelling	oai:doaj.org-article:2b386024339c4aa7b358bb6b2c8531fb2021-11-15T15:30:51ZIntegrative Analysis of Proteome and Transcriptome Dynamics during <named-content content-type="genus-species">Bacillus subtilis</named-content> Spore Revival10.1128/mSphere.00463-202379-5042https://doaj.org/article/2b386024339c4aa7b358bb6b2c8531fb2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00463-20https://doaj.org/toc/2379-5042ABSTRACT Bacillus subtilis spores can reactivate their metabolism through germination upon contact with germinants and can develop into vegetative cells upon outgrowth. However, the mechanisms at the basis of the molecular machinery that triggers the spore germination and outgrowth processes are still largely unclear. To gain further insights into these processes, the transcriptome and proteome changes occurring during the conversion of spores to vegetative cells were analyzed in the present study. For each time point sampled, the changes in the spore proteome were quantitatively monitored relative to the proteome of metabolically 15N-labeled vegetative cells. Of the quantified proteins, 60% are shared by vegetative cells and spores, indicating that the spores have a minimal protein set, sufficient to resume metabolism upon completion of germination. These shared proteins thus represent the most basic “survival kit” for spore-based life. We observed no significant change in the proteome or the transcriptome until the spore’s completion of germination. Our analysis identified 34 abundant mRNA transcripts in the dormant spores, 31 of which are rapidly degraded after germination. In outgrowing spores, we identified 3,152 differentially expressed genes and have demonstrated the differential expression of 322 proteins with our mass spectrometry analyses. Our data also showed that 173 proteins from dormant spores, including both proteins unique to spores and proteins shared with vegetative cells, were lost after completion of germination. The observed diverse timings of synthesis of different protein sets in spore outgrowth revealed a putative core strategy underlying the revival of ‘life’ from the B. subtilis spore. IMPORTANCE This study demonstrated the progress of macromolecular synthesis during Bacillus subtilis spore germination and outgrowth. The transcriptome analysis has additionally allowed us to trace gene expression during this transformation process. For the first time, the basic survival kit for spore-based life has been identified. In addition, in this analysis based on monitoring of protein levels in germinating and outgrowing spores, the transition from (ribo)nucleotide and amino acid biosynthesis to the restoration of all metabolic pathways can be clearly seen. The integrative multi-omics approach applied in this study thus has helped us to achieve a comprehensive overview of the molecular mechanisms at the basis of spore germination and outgrowth as well as to identify important knowledge gaps in need of further study.Bhagyashree SwargeWishwas AbhyankarMartijs JonkerHuub HoefslootGertjan KramerPeter SetlowStanley BrulLeo J. de KoningAmerican Society for MicrobiologyarticleBacillus subtilisspore germinationproteomicsprotein synthesistranscriptomicsmetabolic labelingMicrobiologyQR1-502ENmSphere, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacillus subtilis spore germination proteomics protein synthesis transcriptomics metabolic labeling Microbiology QR1-502
spellingShingle	Bacillus subtilis spore germination proteomics protein synthesis transcriptomics metabolic labeling Microbiology QR1-502 Bhagyashree Swarge Wishwas Abhyankar Martijs Jonker Huub Hoefsloot Gertjan Kramer Peter Setlow Stanley Brul Leo J. de Koning Integrative Analysis of Proteome and Transcriptome Dynamics during <named-content content-type="genus-species">Bacillus subtilis</named-content> Spore Revival
description	ABSTRACT Bacillus subtilis spores can reactivate their metabolism through germination upon contact with germinants and can develop into vegetative cells upon outgrowth. However, the mechanisms at the basis of the molecular machinery that triggers the spore germination and outgrowth processes are still largely unclear. To gain further insights into these processes, the transcriptome and proteome changes occurring during the conversion of spores to vegetative cells were analyzed in the present study. For each time point sampled, the changes in the spore proteome were quantitatively monitored relative to the proteome of metabolically 15N-labeled vegetative cells. Of the quantified proteins, 60% are shared by vegetative cells and spores, indicating that the spores have a minimal protein set, sufficient to resume metabolism upon completion of germination. These shared proteins thus represent the most basic “survival kit” for spore-based life. We observed no significant change in the proteome or the transcriptome until the spore’s completion of germination. Our analysis identified 34 abundant mRNA transcripts in the dormant spores, 31 of which are rapidly degraded after germination. In outgrowing spores, we identified 3,152 differentially expressed genes and have demonstrated the differential expression of 322 proteins with our mass spectrometry analyses. Our data also showed that 173 proteins from dormant spores, including both proteins unique to spores and proteins shared with vegetative cells, were lost after completion of germination. The observed diverse timings of synthesis of different protein sets in spore outgrowth revealed a putative core strategy underlying the revival of ‘life’ from the B. subtilis spore. IMPORTANCE This study demonstrated the progress of macromolecular synthesis during Bacillus subtilis spore germination and outgrowth. The transcriptome analysis has additionally allowed us to trace gene expression during this transformation process. For the first time, the basic survival kit for spore-based life has been identified. In addition, in this analysis based on monitoring of protein levels in germinating and outgrowing spores, the transition from (ribo)nucleotide and amino acid biosynthesis to the restoration of all metabolic pathways can be clearly seen. The integrative multi-omics approach applied in this study thus has helped us to achieve a comprehensive overview of the molecular mechanisms at the basis of spore germination and outgrowth as well as to identify important knowledge gaps in need of further study.
format	article
author	Bhagyashree Swarge Wishwas Abhyankar Martijs Jonker Huub Hoefsloot Gertjan Kramer Peter Setlow Stanley Brul Leo J. de Koning
author_facet	Bhagyashree Swarge Wishwas Abhyankar Martijs Jonker Huub Hoefsloot Gertjan Kramer Peter Setlow Stanley Brul Leo J. de Koning
author_sort	Bhagyashree Swarge
title	Integrative Analysis of Proteome and Transcriptome Dynamics during <named-content content-type="genus-species">Bacillus subtilis</named-content> Spore Revival
title_short	Integrative Analysis of Proteome and Transcriptome Dynamics during <named-content content-type="genus-species">Bacillus subtilis</named-content> Spore Revival
title_full	Integrative Analysis of Proteome and Transcriptome Dynamics during <named-content content-type="genus-species">Bacillus subtilis</named-content> Spore Revival
title_fullStr	Integrative Analysis of Proteome and Transcriptome Dynamics during <named-content content-type="genus-species">Bacillus subtilis</named-content> Spore Revival
title_full_unstemmed	Integrative Analysis of Proteome and Transcriptome Dynamics during <named-content content-type="genus-species">Bacillus subtilis</named-content> Spore Revival
title_sort	integrative analysis of proteome and transcriptome dynamics during <named-content content-type="genus-species">bacillus subtilis</named-content> spore revival
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/2b386024339c4aa7b358bb6b2c8531fb
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Integrative Analysis of Proteome and Transcriptome Dynamics during <named-content content-type="genus-species">Bacillus subtilis</named-content> Spore Revival

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