Coupled Positive and Negative Feedbacks Produce Diverse Gene Expression Patterns in Colonies

ABSTRACT Formation of patterns is a common feature in the development of multicellular organism as well as of microbial communities. To investigate the formation of gene expression patterns in colonies, we build a mathematical model of two-dimensional colony growth, where cells carry a coupled posit...

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Autores principales:	Namiko Mitarai, Mogens Høgh Jensen, Szabolcs Semsey
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b39390a8fa15400d86f12eab7390cfad
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spelling	oai:doaj.org-article:b39390a8fa15400d86f12eab7390cfad2021-11-15T15:41:33ZCoupled Positive and Negative Feedbacks Produce Diverse Gene Expression Patterns in Colonies10.1128/mBio.00059-152150-7511https://doaj.org/article/b39390a8fa15400d86f12eab7390cfad2015-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00059-15https://doaj.org/toc/2150-7511ABSTRACT Formation of patterns is a common feature in the development of multicellular organism as well as of microbial communities. To investigate the formation of gene expression patterns in colonies, we build a mathematical model of two-dimensional colony growth, where cells carry a coupled positive-and-negative-feedback circuit. We demonstrate that the model can produce sectored, target (concentric), uniform, and scattered expression patterns of regulators, depending on gene expression dynamics and nutrient diffusion. We reconstructed the same regulatory structure in Escherichia coli cells and found gene expression patterns on the surface of colonies similar to the ones produced by the computer simulations. By comparing computer simulations and experimental results, we observed that very simple rules of gene expression can yield a spectrum of well-defined patterns in a growing colony. Our results suggest that variations of the protein content among cells lead to a high level of heterogeneity in colonies. IMPORTANCE Formation of patterns is a common feature in the development of microbial communities. In this work, we show that a simple genetic circuit composed of a positive-feedback loop and a negative-feedback loop can produce diverse expression patterns in colonies. We obtained similar sets of gene expression patterns in the simulations and in the experiments. Because the combination of positive feedback and negative feedback is common in intracellular molecular networks, our results suggest that the protein content of cells is highly diversified in colonies.Namiko MitaraiMogens Høgh JensenSzabolcs SemseyAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 2 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Namiko Mitarai Mogens Høgh Jensen Szabolcs Semsey Coupled Positive and Negative Feedbacks Produce Diverse Gene Expression Patterns in Colonies
description	ABSTRACT Formation of patterns is a common feature in the development of multicellular organism as well as of microbial communities. To investigate the formation of gene expression patterns in colonies, we build a mathematical model of two-dimensional colony growth, where cells carry a coupled positive-and-negative-feedback circuit. We demonstrate that the model can produce sectored, target (concentric), uniform, and scattered expression patterns of regulators, depending on gene expression dynamics and nutrient diffusion. We reconstructed the same regulatory structure in Escherichia coli cells and found gene expression patterns on the surface of colonies similar to the ones produced by the computer simulations. By comparing computer simulations and experimental results, we observed that very simple rules of gene expression can yield a spectrum of well-defined patterns in a growing colony. Our results suggest that variations of the protein content among cells lead to a high level of heterogeneity in colonies. IMPORTANCE Formation of patterns is a common feature in the development of microbial communities. In this work, we show that a simple genetic circuit composed of a positive-feedback loop and a negative-feedback loop can produce diverse expression patterns in colonies. We obtained similar sets of gene expression patterns in the simulations and in the experiments. Because the combination of positive feedback and negative feedback is common in intracellular molecular networks, our results suggest that the protein content of cells is highly diversified in colonies.
format	article
author	Namiko Mitarai Mogens Høgh Jensen Szabolcs Semsey
author_facet	Namiko Mitarai Mogens Høgh Jensen Szabolcs Semsey
author_sort	Namiko Mitarai
title	Coupled Positive and Negative Feedbacks Produce Diverse Gene Expression Patterns in Colonies
title_short	Coupled Positive and Negative Feedbacks Produce Diverse Gene Expression Patterns in Colonies
title_full	Coupled Positive and Negative Feedbacks Produce Diverse Gene Expression Patterns in Colonies
title_fullStr	Coupled Positive and Negative Feedbacks Produce Diverse Gene Expression Patterns in Colonies
title_full_unstemmed	Coupled Positive and Negative Feedbacks Produce Diverse Gene Expression Patterns in Colonies
title_sort	coupled positive and negative feedbacks produce diverse gene expression patterns in colonies
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/b39390a8fa15400d86f12eab7390cfad
work_keys_str_mv	AT namikomitarai coupledpositiveandnegativefeedbacksproducediversegeneexpressionpatternsincolonies AT mogenshøghjensen coupledpositiveandnegativefeedbacksproducediversegeneexpressionpatternsincolonies AT szabolcssemsey coupledpositiveandnegativefeedbacksproducediversegeneexpressionpatternsincolonies
_version_	1718427664233005056

Coupled Positive and Negative Feedbacks Produce Diverse Gene Expression Patterns in Colonies

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