Carboxysome Mispositioning Alters Growth, Morphology, and Rubisco Level of the Cyanobacterium <named-content content-type="genus-species">Synechococcus elongatus</named-content> PCC 7942

ABSTRACT Cyanobacteria are the prokaryotic group of phytoplankton responsible for a significant fraction of global CO2 fixation. Like plants, cyanobacteria use the enzyme ribulose 1,5-bisphosphate carboxylase/oxidase (Rubisco) to fix CO2 into organic carbon molecules via the Calvin-Benson-Bassham cy...

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Autores principales:	Rees Rillema, Y Hoang, Joshua S. MacCready, Anthony G. Vecchiarelli
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Rubisco carbon dioxide assimilation carbon dioxide concentration mechanism carbon dioxide fixation carboxysome cell division Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6718653b4e514d0f8a9f6512d49e119c
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spelling	oai:doaj.org-article:6718653b4e514d0f8a9f6512d49e119c2021-11-10T18:37:52ZCarboxysome Mispositioning Alters Growth, Morphology, and Rubisco Level of the Cyanobacterium <named-content content-type="genus-species">Synechococcus elongatus</named-content> PCC 794210.1128/mBio.02696-202150-7511https://doaj.org/article/6718653b4e514d0f8a9f6512d49e119c2021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02696-20https://doaj.org/toc/2150-7511ABSTRACT Cyanobacteria are the prokaryotic group of phytoplankton responsible for a significant fraction of global CO2 fixation. Like plants, cyanobacteria use the enzyme ribulose 1,5-bisphosphate carboxylase/oxidase (Rubisco) to fix CO2 into organic carbon molecules via the Calvin-Benson-Bassham cycle. Unlike plants, cyanobacteria evolved a carbon-concentrating organelle called the carboxysome—a proteinaceous compartment that encapsulates and concentrates Rubisco along with its CO2 substrate. In the rod-shaped cyanobacterium Synechococcus elongatus PCC 7942, we recently identified the McdAB system responsible for uniformly distributing carboxysomes along the cell length. It remains unknown what role carboxysome positioning plays with respect to cellular physiology. Here, we show that a failure to distribute carboxysomes leads to slower cell growth, cell elongation, asymmetric cell division, and elevated levels of cellular Rubisco. Unexpectedly, we also report that even wild-type S. elongatus undergoes cell elongation and asymmetric cell division when grown at the cool, but environmentally relevant, growth temperature of 20°C or when switched from a high- to ambient-CO2 environment. The findings suggest that carboxysome positioning by the McdAB system functions to maintain the carbon fixation efficiency of Rubisco by preventing carboxysome aggregation, which is particularly important under growth conditions where rod-shaped cyanobacteria adopt a filamentous morphology. IMPORTANCE Photosynthetic cyanobacteria are responsible for almost half of global CO2 fixation. Due to eutrophication, rising temperatures, and increasing atmospheric CO2 concentrations, cyanobacteria have gained notoriety for their ability to form massive blooms in both freshwater and marine ecosystems across the globe. Like plants, cyanobacteria use the most abundant enzyme on Earth, Rubisco, to provide the sole source of organic carbon required for its photosynthetic growth. Unlike plants, cyanobacteria have evolved a carbon-concentrating organelle called the carboxysome that encapsulates and concentrates Rubisco with its CO2 substrate to significantly increase carbon fixation efficiency and cell growth. We recently identified the positioning system that distributes carboxysomes in cyanobacteria. However, the physiological consequence of carboxysome mispositioning in the absence of this distribution system remains unknown. Here, we find that carboxysome mispositioning triggers changes in cell growth and morphology as well as elevated levels of cellular Rubisco.Rees RillemaY HoangJoshua S. MacCreadyAnthony G. VecchiarelliAmerican Society for MicrobiologyarticleRubiscocarbon dioxide assimilationcarbon dioxide concentration mechanismcarbon dioxide fixationcarboxysomecell divisionMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Rubisco carbon dioxide assimilation carbon dioxide concentration mechanism carbon dioxide fixation carboxysome cell division Microbiology QR1-502
spellingShingle	Rubisco carbon dioxide assimilation carbon dioxide concentration mechanism carbon dioxide fixation carboxysome cell division Microbiology QR1-502 Rees Rillema Y Hoang Joshua S. MacCready Anthony G. Vecchiarelli Carboxysome Mispositioning Alters Growth, Morphology, and Rubisco Level of the Cyanobacterium <named-content content-type="genus-species">Synechococcus elongatus</named-content> PCC 7942
description	ABSTRACT Cyanobacteria are the prokaryotic group of phytoplankton responsible for a significant fraction of global CO2 fixation. Like plants, cyanobacteria use the enzyme ribulose 1,5-bisphosphate carboxylase/oxidase (Rubisco) to fix CO2 into organic carbon molecules via the Calvin-Benson-Bassham cycle. Unlike plants, cyanobacteria evolved a carbon-concentrating organelle called the carboxysome—a proteinaceous compartment that encapsulates and concentrates Rubisco along with its CO2 substrate. In the rod-shaped cyanobacterium Synechococcus elongatus PCC 7942, we recently identified the McdAB system responsible for uniformly distributing carboxysomes along the cell length. It remains unknown what role carboxysome positioning plays with respect to cellular physiology. Here, we show that a failure to distribute carboxysomes leads to slower cell growth, cell elongation, asymmetric cell division, and elevated levels of cellular Rubisco. Unexpectedly, we also report that even wild-type S. elongatus undergoes cell elongation and asymmetric cell division when grown at the cool, but environmentally relevant, growth temperature of 20°C or when switched from a high- to ambient-CO2 environment. The findings suggest that carboxysome positioning by the McdAB system functions to maintain the carbon fixation efficiency of Rubisco by preventing carboxysome aggregation, which is particularly important under growth conditions where rod-shaped cyanobacteria adopt a filamentous morphology. IMPORTANCE Photosynthetic cyanobacteria are responsible for almost half of global CO2 fixation. Due to eutrophication, rising temperatures, and increasing atmospheric CO2 concentrations, cyanobacteria have gained notoriety for their ability to form massive blooms in both freshwater and marine ecosystems across the globe. Like plants, cyanobacteria use the most abundant enzyme on Earth, Rubisco, to provide the sole source of organic carbon required for its photosynthetic growth. Unlike plants, cyanobacteria have evolved a carbon-concentrating organelle called the carboxysome that encapsulates and concentrates Rubisco with its CO2 substrate to significantly increase carbon fixation efficiency and cell growth. We recently identified the positioning system that distributes carboxysomes in cyanobacteria. However, the physiological consequence of carboxysome mispositioning in the absence of this distribution system remains unknown. Here, we find that carboxysome mispositioning triggers changes in cell growth and morphology as well as elevated levels of cellular Rubisco.
format	article
author	Rees Rillema Y Hoang Joshua S. MacCready Anthony G. Vecchiarelli
author_facet	Rees Rillema Y Hoang Joshua S. MacCready Anthony G. Vecchiarelli
author_sort	Rees Rillema
title	Carboxysome Mispositioning Alters Growth, Morphology, and Rubisco Level of the Cyanobacterium <named-content content-type="genus-species">Synechococcus elongatus</named-content> PCC 7942
title_short	Carboxysome Mispositioning Alters Growth, Morphology, and Rubisco Level of the Cyanobacterium <named-content content-type="genus-species">Synechococcus elongatus</named-content> PCC 7942
title_full	Carboxysome Mispositioning Alters Growth, Morphology, and Rubisco Level of the Cyanobacterium <named-content content-type="genus-species">Synechococcus elongatus</named-content> PCC 7942
title_fullStr	Carboxysome Mispositioning Alters Growth, Morphology, and Rubisco Level of the Cyanobacterium <named-content content-type="genus-species">Synechococcus elongatus</named-content> PCC 7942
title_full_unstemmed	Carboxysome Mispositioning Alters Growth, Morphology, and Rubisco Level of the Cyanobacterium <named-content content-type="genus-species">Synechococcus elongatus</named-content> PCC 7942
title_sort	carboxysome mispositioning alters growth, morphology, and rubisco level of the cyanobacterium <named-content content-type="genus-species">synechococcus elongatus</named-content> pcc 7942
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/6718653b4e514d0f8a9f6512d49e119c
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Carboxysome Mispositioning Alters Growth, Morphology, and Rubisco Level of the Cyanobacterium <named-content content-type="genus-species">Synechococcus elongatus</named-content> PCC 7942

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