The Inorganic Nutrient Regime and the <italic toggle="yes">mre</italic> Genes Regulate Cell and Filament Size and Morphology in the Phototrophic Multicellular Bacterium <italic toggle="yes">Anabaena</italic>

ABSTRACT The model cyanobacterium Anabaena sp. PCC 7120 exhibits a phototrophic metabolism relying on oxygenic photosynthesis and a complex morphology. The organismic unit is a filament of communicated cells that may include cells specialized in different nutritional tasks, thus representing a parad...

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Autores principales:	Cristina Velázquez-Suárez, Ignacio Luque, Antonia Herrero
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	bacterial multicellularity cell size cell aspect filament length NtcA regulation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1aa1f4740b644158a583a1766ca90ef6
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spelling	oai:doaj.org-article:1aa1f4740b644158a583a1766ca90ef62021-11-15T15:30:58ZThe Inorganic Nutrient Regime and the <italic toggle="yes">mre</italic> Genes Regulate Cell and Filament Size and Morphology in the Phototrophic Multicellular Bacterium <italic toggle="yes">Anabaena</italic>10.1128/mSphere.00747-202379-5042https://doaj.org/article/1aa1f4740b644158a583a1766ca90ef62020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00747-20https://doaj.org/toc/2379-5042ABSTRACT The model cyanobacterium Anabaena sp. PCC 7120 exhibits a phototrophic metabolism relying on oxygenic photosynthesis and a complex morphology. The organismic unit is a filament of communicated cells that may include cells specialized in different nutritional tasks, thus representing a paradigm of multicellular bacteria. In Anabaena, the inorganic carbon and nitrogen regime influenced not only growth, but also cell size, cell shape, and filament length, which also varied through the growth cycle. When using combined nitrogen, especially with abundant carbon, cells enlarged and elongated during active growth. When fixing N2, which imposed lower growth rates, shorter and smaller cells were maintained. In Anabaena, gene homologs to mreB, mreC, and mreD form an operon that was expressed at higher levels during the phase of fastest growth. In an ntcA mutant, mre transcript levels were higher than in the wild type and, consistently, cells were longer. Negative regulation by NtcA can explain that Anabaena cells were longer in the presence of combined nitrogen than in diazotrophic cultures, in which the levels of NtcA are higher. mreB, mreC, and mreD mutants could grow with combined nitrogen, but only the latter mutant could grow diazotrophically. Cells were always larger and shorter than wild-type cells, and their orientation in the filament was inverted. Consistent with increased peptidoglycan width and incorporation in the intercellular septa, filaments were longer in the mutants, suggesting a role for MreB, MreC, and MreD in the construction of septal peptidoglycan that could affect intercellular communication required for diazotrophic growth. IMPORTANCE Most studies on the determination of bacterial cell morphology have been conducted in heterotrophic organisms. Here, we present a study of how the availability of inorganic nitrogen and carbon sources influence cell size and morphology in the context of a phototrophic metabolism, as found in the multicellular cyanobacterium Anabaena. In Anabaena, the expression of the MreB, MreC, and MreD proteins, which influence cell size and length, are regulated by NtcA, a transcription factor that globally coordinates cellular responses to the C-to-N balance of the cells. Moreover, MreB, MreC, and MreD also influence septal peptidoglycan construction, thus affecting filament length and, possibly, intercellular molecular exchange that is required for diazotrophic growth. Thus, here we identified new roles for Mre proteins in relation to the phototrophic and multicellular character of a cyanobacterium, Anabaena.Cristina Velázquez-SuárezIgnacio LuqueAntonia HerreroAmerican Society for Microbiologyarticlebacterial multicellularitycell sizecell aspectfilament lengthNtcA regulationMicrobiologyQR1-502ENmSphere, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacterial multicellularity cell size cell aspect filament length NtcA regulation Microbiology QR1-502
spellingShingle	bacterial multicellularity cell size cell aspect filament length NtcA regulation Microbiology QR1-502 Cristina Velázquez-Suárez Ignacio Luque Antonia Herrero The Inorganic Nutrient Regime and the <italic toggle="yes">mre</italic> Genes Regulate Cell and Filament Size and Morphology in the Phototrophic Multicellular Bacterium <italic toggle="yes">Anabaena</italic>
description	ABSTRACT The model cyanobacterium Anabaena sp. PCC 7120 exhibits a phototrophic metabolism relying on oxygenic photosynthesis and a complex morphology. The organismic unit is a filament of communicated cells that may include cells specialized in different nutritional tasks, thus representing a paradigm of multicellular bacteria. In Anabaena, the inorganic carbon and nitrogen regime influenced not only growth, but also cell size, cell shape, and filament length, which also varied through the growth cycle. When using combined nitrogen, especially with abundant carbon, cells enlarged and elongated during active growth. When fixing N2, which imposed lower growth rates, shorter and smaller cells were maintained. In Anabaena, gene homologs to mreB, mreC, and mreD form an operon that was expressed at higher levels during the phase of fastest growth. In an ntcA mutant, mre transcript levels were higher than in the wild type and, consistently, cells were longer. Negative regulation by NtcA can explain that Anabaena cells were longer in the presence of combined nitrogen than in diazotrophic cultures, in which the levels of NtcA are higher. mreB, mreC, and mreD mutants could grow with combined nitrogen, but only the latter mutant could grow diazotrophically. Cells were always larger and shorter than wild-type cells, and their orientation in the filament was inverted. Consistent with increased peptidoglycan width and incorporation in the intercellular septa, filaments were longer in the mutants, suggesting a role for MreB, MreC, and MreD in the construction of septal peptidoglycan that could affect intercellular communication required for diazotrophic growth. IMPORTANCE Most studies on the determination of bacterial cell morphology have been conducted in heterotrophic organisms. Here, we present a study of how the availability of inorganic nitrogen and carbon sources influence cell size and morphology in the context of a phototrophic metabolism, as found in the multicellular cyanobacterium Anabaena. In Anabaena, the expression of the MreB, MreC, and MreD proteins, which influence cell size and length, are regulated by NtcA, a transcription factor that globally coordinates cellular responses to the C-to-N balance of the cells. Moreover, MreB, MreC, and MreD also influence septal peptidoglycan construction, thus affecting filament length and, possibly, intercellular molecular exchange that is required for diazotrophic growth. Thus, here we identified new roles for Mre proteins in relation to the phototrophic and multicellular character of a cyanobacterium, Anabaena.
format	article
author	Cristina Velázquez-Suárez Ignacio Luque Antonia Herrero
author_facet	Cristina Velázquez-Suárez Ignacio Luque Antonia Herrero
author_sort	Cristina Velázquez-Suárez
title	The Inorganic Nutrient Regime and the <italic toggle="yes">mre</italic> Genes Regulate Cell and Filament Size and Morphology in the Phototrophic Multicellular Bacterium <italic toggle="yes">Anabaena</italic>
title_short	The Inorganic Nutrient Regime and the <italic toggle="yes">mre</italic> Genes Regulate Cell and Filament Size and Morphology in the Phototrophic Multicellular Bacterium <italic toggle="yes">Anabaena</italic>
title_full	The Inorganic Nutrient Regime and the <italic toggle="yes">mre</italic> Genes Regulate Cell and Filament Size and Morphology in the Phototrophic Multicellular Bacterium <italic toggle="yes">Anabaena</italic>
title_fullStr	The Inorganic Nutrient Regime and the <italic toggle="yes">mre</italic> Genes Regulate Cell and Filament Size and Morphology in the Phototrophic Multicellular Bacterium <italic toggle="yes">Anabaena</italic>
title_full_unstemmed	The Inorganic Nutrient Regime and the <italic toggle="yes">mre</italic> Genes Regulate Cell and Filament Size and Morphology in the Phototrophic Multicellular Bacterium <italic toggle="yes">Anabaena</italic>
title_sort	inorganic nutrient regime and the <italic toggle="yes">mre</italic> genes regulate cell and filament size and morphology in the phototrophic multicellular bacterium <italic toggle="yes">anabaena</italic>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/1aa1f4740b644158a583a1766ca90ef6
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The Inorganic Nutrient Regime and the <italic toggle="yes">mre</italic> Genes Regulate Cell and Filament Size and Morphology in the Phototrophic Multicellular Bacterium <italic toggle="yes">Anabaena</italic>

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