Dataset Information

Embryo-like features in developing Bacillus subtilis biofilms

ABSTRACT: Correspondence between evolution and development has been discussed for more than two centuries. Recent work reveals that phylogeny-ontogeny correlations are indeed present in developmental transcriptomes of eukaryotic clades with complex multicellularity. Nevertheless, it has been largely ignored that the pervasive presence of phylogeny-ontogeny correlations is likely a hallmark of development in eukaryotes. This perspective opens a possibility to look for similar parallelisms in biological settings where developmental logic and multicellular complexity are more obscure. For instance, it has been increasingly recognized that multicellular behavior underlies biofilm formation in bacteria. However, it remains unclear whether bacterial biofilm growth shares some basic principles with development in complex eukaryotes. Here we show that ontogeny of growing Bacillus subtilis biofilms recapitulates phylogeny at the expression level. Using finely resolved transcriptome and proteome profiles, we found that biofilm ontogeny correlates with the evolutionary measures. Early-stage biofilms expressed older and more conserved genes, while later-stage biofilms progressively used evolutionary younger and more diverged genes. Molecular and morphological signatures also revealed that biofilm growth is highly regulated and organized into discrete ontogenetic stages, similar to those of eukaryotic embryos. In conjunction this suggests that biofilm formation in Bacillus is a bona fide developmental process comparable to organismal development in animals, plants and fungi. Given that most cells on Earth reside in the form of biofilms and that biofilms represent the oldest known fossils, we anticipate that the widely-adopted vision of the first life as a single-cell and free-living organism needs rethinking.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Bacillus Subtilis Subsp. Subtilis Str. Ncib 3610

SUBMITTER: Vaishnavi Ravikumar

LAB HEAD: Tomislav Domazet-Lošo

PROVIDER: PXD016656 | Pride | 2020-10-07

REPOSITORIES: Pride

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Dataset's files

Source:

			Action	DRS
	QEHF_170629_14_12H_BR1_F1_inj1.raw	Raw
	QEHF_170629_15_12H_BR1_F1_inj2.raw	Raw
	QEHF_170629_16_12H_BR1_F1_inj3.raw	Raw
	QEHF_170629_17_12H_BR1_F2_inj1.raw	Raw
	QEHF_170629_18_12H_BR1_F2_inj2.raw	Raw

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Publications

Embryo-Like Features in Developing Bacillus subtilis Biofilms.

Futo Momir M Opašić Luka L Koska Sara S Čorak Nina N Široki Tin T Ravikumar Vaishnavi V Thorsell Annika A Lenuzzi Maša M Kifer Domagoj D Domazet-Lošo Mirjana M Vlahoviček Kristian K Mijakovic Ivan I Domazet-Lošo Tomislav T

Molecular biology and evolution 20210101 1

Correspondence between evolution and development has been discussed for more than two centuries. Recent work reveals that phylogeny-ontogeny correlations are indeed present in developmental transcriptomes of eukaryotic clades with complex multicellularity. Nevertheless, it has been largely ignored that the pervasive presence of phylogeny-ontogeny correlations is a hallmark of development in eukaryotes. This perspective opens a possibility to look for similar parallelisms in biological settings w ...[more]

PMID: 32871001

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Project description:Biofilms are structured communities of tightly associated cells that constitute thepredominant state of bacterial growth in naturaland human-madeenvironments. Although the core genetic circuitry that controls biofilm formation in model bacteria such as Bacillus subtilishas been well characterized, little is known about the role that metabolism plays in this complex developmental process. Here, weperformed a time-resolved analysisof the metabolic changes associated with pellicle biofilm formation and development inB. subtilisby combining metabolomic, transcriptomic, and proteomic analyses. We report a 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 hithertounrecognized 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 generally controlled at the transcriptional level. Our resultsalsoprovide insights into the transcription factors and regulatory networks involved in thiscomplexmetabolic remodeling. Following upon these results, we demonstrate that acetoin production via acetolactate synthase is essential for robust biofilm growthand has the dual role of conservingredox balance and maintaining extracellularpH.This study represents a comprehensive systems-level investigation of the metabolic remodeling occurring during B. subtilisbiofilm development that will serve as a useful roadmap for future studies on biofilm physiology.