Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth

ABSTRACT Harnessing the metabolic potential of photosynthetic microbes for next-generation biotechnology objectives requires detailed scientific understanding of the physiological constraints and regulatory controls affecting carbon partitioning between biomass, metabolite storage pools, and bioprod...

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Autores principales:	Hans C. Bernstein, Ryan S. McClure, Eric A. Hill, Lye Meng Markillie, William B. Chrisler, Margie F. Romine, Jason E. McDermott, Matthew C. Posewitz, Donald A. Bryant, Allan E. Konopka, James K. Fredrickson, Alexander S. Beliaev
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/147264692d7f4291b7e292c6fd168e35
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spelling	oai:doaj.org-article:147264692d7f4291b7e292c6fd168e352021-11-15T15:50:18ZUnlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth10.1128/mBio.00949-162150-7511https://doaj.org/article/147264692d7f4291b7e292c6fd168e352016-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00949-16https://doaj.org/toc/2150-7511ABSTRACT Harnessing the metabolic potential of photosynthetic microbes for next-generation biotechnology objectives requires detailed scientific understanding of the physiological constraints and regulatory controls affecting carbon partitioning between biomass, metabolite storage pools, and bioproduct synthesis. We dissected the cellular mechanisms underlying the remarkable physiological robustness of the euryhaline unicellular cyanobacterium Synechococcus sp. strain PCC 7002 (Synechococcus 7002) and identify key mechanisms that allow cyanobacteria to achieve unprecedented photoautotrophic productivities (~2.5-h doubling time). Ultrafast growth of Synechococcus 7002 was supported by high rates of photosynthetic electron transfer and linked to significantly elevated transcription of precursor biosynthesis and protein translation machinery. Notably, no growth or photosynthesis inhibition signatures were observed under any of the tested experimental conditions. Finally, the ultrafast growth in Synechococcus 7002 was also linked to a 300% expansion of average cell volume. We hypothesize that this cellular adaptation is required at high irradiances to support higher cell division rates and reduce deleterious effects, corresponding to high light, through increased carbon and reductant sequestration. IMPORTANCE Efficient coupling between photosynthesis and productivity is central to the development of biotechnology based on solar energy. Therefore, understanding the factors constraining maximum rates of carbon processing is necessary to identify regulatory mechanisms and devise strategies to overcome productivity constraints. Here, we interrogate the molecular mechanisms that operate at a systems level to allow cyanobacteria to achieve ultrafast growth. This was done by considering growth and photosynthetic kinetics with global transcription patterns. We have delineated putative biological principles that allow unicellular cyanobacteria to achieve ultrahigh growth rates through photophysiological acclimation and effective management of cellular resource under different growth regimes.Hans C. BernsteinRyan S. McClureEric A. HillLye Meng MarkillieWilliam B. ChrislerMargie F. RomineJason E. McDermottMatthew C. PosewitzDonald A. BryantAllan E. KonopkaJames K. FredricksonAlexander S. BeliaevAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 4 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Hans C. Bernstein Ryan S. McClure Eric A. Hill Lye Meng Markillie William B. Chrisler Margie F. Romine Jason E. McDermott Matthew C. Posewitz Donald A. Bryant Allan E. Konopka James K. Fredrickson Alexander S. Beliaev Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth
description	ABSTRACT Harnessing the metabolic potential of photosynthetic microbes for next-generation biotechnology objectives requires detailed scientific understanding of the physiological constraints and regulatory controls affecting carbon partitioning between biomass, metabolite storage pools, and bioproduct synthesis. We dissected the cellular mechanisms underlying the remarkable physiological robustness of the euryhaline unicellular cyanobacterium Synechococcus sp. strain PCC 7002 (Synechococcus 7002) and identify key mechanisms that allow cyanobacteria to achieve unprecedented photoautotrophic productivities (~2.5-h doubling time). Ultrafast growth of Synechococcus 7002 was supported by high rates of photosynthetic electron transfer and linked to significantly elevated transcription of precursor biosynthesis and protein translation machinery. Notably, no growth or photosynthesis inhibition signatures were observed under any of the tested experimental conditions. Finally, the ultrafast growth in Synechococcus 7002 was also linked to a 300% expansion of average cell volume. We hypothesize that this cellular adaptation is required at high irradiances to support higher cell division rates and reduce deleterious effects, corresponding to high light, through increased carbon and reductant sequestration. IMPORTANCE Efficient coupling between photosynthesis and productivity is central to the development of biotechnology based on solar energy. Therefore, understanding the factors constraining maximum rates of carbon processing is necessary to identify regulatory mechanisms and devise strategies to overcome productivity constraints. Here, we interrogate the molecular mechanisms that operate at a systems level to allow cyanobacteria to achieve ultrafast growth. This was done by considering growth and photosynthetic kinetics with global transcription patterns. We have delineated putative biological principles that allow unicellular cyanobacteria to achieve ultrahigh growth rates through photophysiological acclimation and effective management of cellular resource under different growth regimes.
format	article
author	Hans C. Bernstein Ryan S. McClure Eric A. Hill Lye Meng Markillie William B. Chrisler Margie F. Romine Jason E. McDermott Matthew C. Posewitz Donald A. Bryant Allan E. Konopka James K. Fredrickson Alexander S. Beliaev
author_facet	Hans C. Bernstein Ryan S. McClure Eric A. Hill Lye Meng Markillie William B. Chrisler Margie F. Romine Jason E. McDermott Matthew C. Posewitz Donald A. Bryant Allan E. Konopka James K. Fredrickson Alexander S. Beliaev
author_sort	Hans C. Bernstein
title	Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth
title_short	Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth
title_full	Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth
title_fullStr	Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth
title_full_unstemmed	Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth
title_sort	unlocking the constraints of cyanobacterial productivity: acclimations enabling ultrafast growth
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/147264692d7f4291b7e292c6fd168e35
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Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth

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