Metabolic Remodeling during Biofilm Development of <named-content content-type="genus-species">Bacillus subtilis</named-content>

ABSTRACT Biofilms are structured communities of tightly associated cells that constitute the predominant state of bacterial growth in natural and human-made environments. Although the core genetic circuitry that controls biofilm formation in model bacteria such as Bacillus subtilis has been well cha...

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Autores principales:	Tippapha Pisithkul, Jeremy W. Schroeder, Edna A. Trujillo, Ponlkrit Yeesin, David M. Stevenson, Tai Chaiamarit, Joshua J. Coon, Jue D. Wang, Daniel Amador-Noguez
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Bacillus subtilis acetoin biofilms metabolism metabolomics proteomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/531ca265dec64ba28248243c75ac6d3f
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spelling	oai:doaj.org-article:531ca265dec64ba28248243c75ac6d3f2021-11-15T15:55:24ZMetabolic Remodeling during Biofilm Development of <named-content content-type="genus-species">Bacillus subtilis</named-content>10.1128/mBio.00623-192150-7511https://doaj.org/article/531ca265dec64ba28248243c75ac6d3f2019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00623-19https://doaj.org/toc/2150-7511ABSTRACT Biofilms are structured communities of tightly associated cells that constitute the predominant state of bacterial growth in natural and human-made environments. Although the core genetic circuitry that controls biofilm formation in model bacteria such as Bacillus subtilis has been well characterized, little is known about the role that metabolism plays in this complex developmental process. Here, we performed a time-resolved analysis of the metabolic changes associated with pellicle biofilm formation and development in B. subtilis by combining metabolomic, transcriptomic, and proteomic analyses. We report surprisingly widespread and dynamic remodeling of metabolism affecting central carbon metabolism, primary biosynthetic pathways, fermentation pathways, and secondary metabolism. Most of these metabolic alterations were hitherto unrecognized as biofilm associated. For example, we observed increased activity of the tricarboxylic acid (TCA) cycle during early biofilm growth, a shift from fatty acid biosynthesis to fatty acid degradation, reorganization of iron metabolism and transport, and a switch from acetate to acetoin fermentation. Close agreement between metabolomic, transcriptomic, and proteomic measurements indicated that remodeling of metabolism during biofilm development was largely controlled at the transcriptional level. Our results also provide insights into the transcription factors and regulatory networks involved in this complex metabolic remodeling. Following upon these results, we demonstrated that acetoin production via acetolactate synthase is essential for robust biofilm growth and has the dual role of conserving redox balance and maintaining extracellular pH. This report represents a comprehensive systems-level investigation of the metabolic remodeling occurring during B. subtilis biofilm development that will serve as a useful road map for future studies on biofilm physiology. IMPORTANCE Bacterial biofilms are ubiquitous in natural environments and play an important role in many clinical, industrial, and ecological settings. Although much is known about the transcriptional regulatory networks that control biofilm formation in model bacteria such as Bacillus subtilis, very little is known about the role of metabolism in this complex developmental process. To address this important knowledge gap, we performed a time-resolved analysis of the metabolic changes associated with bacterial biofilm development in B. subtilis by combining metabolomic, transcriptomic, and proteomic analyses. Here, we report a widespread and dynamic remodeling of metabolism affecting central carbon metabolism, primary biosynthetic pathways, fermentation pathways, and secondary metabolism. This report serves as a unique hypothesis-generating resource for future studies on bacterial biofilm physiology. Outside the biofilm research area, this work should also prove relevant to any investigators interested in microbial physiology and metabolism.Tippapha PisithkulJeremy W. SchroederEdna A. TrujilloPonlkrit YeesinDavid M. StevensonTai ChaiamaritJoshua J. CoonJue D. WangDaniel Amador-NoguezAmerican Society for MicrobiologyarticleBacillus subtilisacetoinbiofilmsmetabolismmetabolomicsproteomicsMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacillus subtilis acetoin biofilms metabolism metabolomics proteomics Microbiology QR1-502
spellingShingle	Bacillus subtilis acetoin biofilms metabolism metabolomics proteomics Microbiology QR1-502 Tippapha Pisithkul Jeremy W. Schroeder Edna A. Trujillo Ponlkrit Yeesin David M. Stevenson Tai Chaiamarit Joshua J. Coon Jue D. Wang Daniel Amador-Noguez Metabolic Remodeling during Biofilm Development of <named-content content-type="genus-species">Bacillus subtilis</named-content>
description	ABSTRACT Biofilms are structured communities of tightly associated cells that constitute the predominant state of bacterial growth in natural and human-made environments. Although the core genetic circuitry that controls biofilm formation in model bacteria such as Bacillus subtilis has been well characterized, little is known about the role that metabolism plays in this complex developmental process. Here, we performed a time-resolved analysis of the metabolic changes associated with pellicle biofilm formation and development in B. subtilis by combining metabolomic, transcriptomic, and proteomic analyses. We report surprisingly widespread and dynamic remodeling of metabolism affecting central carbon metabolism, primary biosynthetic pathways, fermentation pathways, and secondary metabolism. Most of these metabolic alterations were hitherto unrecognized as biofilm associated. For example, we observed increased activity of the tricarboxylic acid (TCA) cycle during early biofilm growth, a shift from fatty acid biosynthesis to fatty acid degradation, reorganization of iron metabolism and transport, and a switch from acetate to acetoin fermentation. Close agreement between metabolomic, transcriptomic, and proteomic measurements indicated that remodeling of metabolism during biofilm development was largely controlled at the transcriptional level. Our results also provide insights into the transcription factors and regulatory networks involved in this complex metabolic remodeling. Following upon these results, we demonstrated that acetoin production via acetolactate synthase is essential for robust biofilm growth and has the dual role of conserving redox balance and maintaining extracellular pH. This report represents a comprehensive systems-level investigation of the metabolic remodeling occurring during B. subtilis biofilm development that will serve as a useful road map for future studies on biofilm physiology. IMPORTANCE Bacterial biofilms are ubiquitous in natural environments and play an important role in many clinical, industrial, and ecological settings. Although much is known about the transcriptional regulatory networks that control biofilm formation in model bacteria such as Bacillus subtilis, very little is known about the role of metabolism in this complex developmental process. To address this important knowledge gap, we performed a time-resolved analysis of the metabolic changes associated with bacterial biofilm development in B. subtilis by combining metabolomic, transcriptomic, and proteomic analyses. Here, we report a widespread and dynamic remodeling of metabolism affecting central carbon metabolism, primary biosynthetic pathways, fermentation pathways, and secondary metabolism. This report serves as a unique hypothesis-generating resource for future studies on bacterial biofilm physiology. Outside the biofilm research area, this work should also prove relevant to any investigators interested in microbial physiology and metabolism.
format	article
author	Tippapha Pisithkul Jeremy W. Schroeder Edna A. Trujillo Ponlkrit Yeesin David M. Stevenson Tai Chaiamarit Joshua J. Coon Jue D. Wang Daniel Amador-Noguez
author_facet	Tippapha Pisithkul Jeremy W. Schroeder Edna A. Trujillo Ponlkrit Yeesin David M. Stevenson Tai Chaiamarit Joshua J. Coon Jue D. Wang Daniel Amador-Noguez
author_sort	Tippapha Pisithkul
title	Metabolic Remodeling during Biofilm Development of <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_short	Metabolic Remodeling during Biofilm Development of <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_full	Metabolic Remodeling during Biofilm Development of <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_fullStr	Metabolic Remodeling during Biofilm Development of <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_full_unstemmed	Metabolic Remodeling during Biofilm Development of <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_sort	metabolic remodeling during biofilm development of <named-content content-type="genus-species">bacillus subtilis</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/531ca265dec64ba28248243c75ac6d3f
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Metabolic Remodeling during Biofilm Development of <named-content content-type="genus-species">Bacillus subtilis</named-content>

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