Carbon Fate and Flux in <italic toggle="yes">Prochlorococcus</italic> under Nitrogen Limitation

ABSTRACT Primary production by Prochlorococcus, the smallest known free-living photosynthetic organism in terms of both physical and genomic size, is thought to have a significant role in global carbon cycles. Despite its small size and low growth rate, Prochlorococcus numerically dominates the phyt...

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Autores principales:	Martin J. Szul, Stephen P. Dearth, Shawn R. Campagna, Erik R. Zinser
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Prochlorococcus carbon cyanobacteria metabolomics nitrogen Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6d7f21a1ae9e41cba001cd0460ab3c9b
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spelling	oai:doaj.org-article:6d7f21a1ae9e41cba001cd0460ab3c9b2021-12-02T18:15:45ZCarbon Fate and Flux in <italic toggle="yes">Prochlorococcus</italic> under Nitrogen Limitation10.1128/mSystems.00254-182379-5077https://doaj.org/article/6d7f21a1ae9e41cba001cd0460ab3c9b2019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00254-18https://doaj.org/toc/2379-5077ABSTRACT Primary production by Prochlorococcus, the smallest known free-living photosynthetic organism in terms of both physical and genomic size, is thought to have a significant role in global carbon cycles. Despite its small size and low growth rate, Prochlorococcus numerically dominates the phytoplankton community in the nutrient-poor oligotrophic ocean, the largest biome of the Earth’s surface. How nutrient limitation, and nitrogen limitation in particular, affects the fate and flux of carbon fixed by Prochlorococcus is currently unknown. To address this gap in knowledge, we compared the bulk rates of photosynthesis and organic carbon release, the concentrations of intracellular metabolites, and the rates of assimilated carbon into the metabolite pools between replete and N-limited chemostat cultures. Total photosynthesis of our N-limited cultures was less than half of those observed in replete cultures, and nitrogen limitation also appears to cause a larger proportion of total fixed carbon to be released to the environment. Our data suggest this occurs in concert with the maintenance of large slow-moving pools of metabolites, including nitrogen-rich molecules such as glutamate. Additionally, we report field data suggesting metabolisms of Prochlorococcus are comparable to results we observe in our laboratory studies. Accounting for these observations, potential metabolic mechanisms utilized by Prochlorococcus are discussed as we build upon our understanding of nutrient-limited photosynthesis and carbon metabolism. IMPORTANCE Photosynthetic microbes are the predominant sources of organic carbon in the sunlit regions of the ocean. During photosynthesis, nitrogen and carbon metabolism are coordinated to synthesize nitrogen-containing organics such as amino acids and nucleic acids. In large regions of the ocean, nitrogen is thought to limit the growth of phytoplankton. The impact of nitrogen limitation on the synthesis of organic carbon is not well understood, especially for the most abundant photosynthetic organism in the nitrogen-limited regions of the ocean, Prochlorococcus. This study compares the carbon metabolism of nitrogen-replete and nitrogen-limited Prochlorococcus spp. to determine how nitrogen availability influences inorganic carbon assimilation into an organic form. Metabolomics and physiological data revealed that cells under nitrogen limitation have reduced metabolic flux and total carbon fixation rates while maintaining elevated metabolite pool levels and releasing a larger proportion of total fixed carbon to the environment.Martin J. SzulStephen P. DearthShawn R. CampagnaErik R. ZinserAmerican Society for MicrobiologyarticleProchlorococcuscarboncyanobacteriametabolomicsnitrogenMicrobiologyQR1-502ENmSystems, Vol 4, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Prochlorococcus carbon cyanobacteria metabolomics nitrogen Microbiology QR1-502
spellingShingle	Prochlorococcus carbon cyanobacteria metabolomics nitrogen Microbiology QR1-502 Martin J. Szul Stephen P. Dearth Shawn R. Campagna Erik R. Zinser Carbon Fate and Flux in <italic toggle="yes">Prochlorococcus</italic> under Nitrogen Limitation
description	ABSTRACT Primary production by Prochlorococcus, the smallest known free-living photosynthetic organism in terms of both physical and genomic size, is thought to have a significant role in global carbon cycles. Despite its small size and low growth rate, Prochlorococcus numerically dominates the phytoplankton community in the nutrient-poor oligotrophic ocean, the largest biome of the Earth’s surface. How nutrient limitation, and nitrogen limitation in particular, affects the fate and flux of carbon fixed by Prochlorococcus is currently unknown. To address this gap in knowledge, we compared the bulk rates of photosynthesis and organic carbon release, the concentrations of intracellular metabolites, and the rates of assimilated carbon into the metabolite pools between replete and N-limited chemostat cultures. Total photosynthesis of our N-limited cultures was less than half of those observed in replete cultures, and nitrogen limitation also appears to cause a larger proportion of total fixed carbon to be released to the environment. Our data suggest this occurs in concert with the maintenance of large slow-moving pools of metabolites, including nitrogen-rich molecules such as glutamate. Additionally, we report field data suggesting metabolisms of Prochlorococcus are comparable to results we observe in our laboratory studies. Accounting for these observations, potential metabolic mechanisms utilized by Prochlorococcus are discussed as we build upon our understanding of nutrient-limited photosynthesis and carbon metabolism. IMPORTANCE Photosynthetic microbes are the predominant sources of organic carbon in the sunlit regions of the ocean. During photosynthesis, nitrogen and carbon metabolism are coordinated to synthesize nitrogen-containing organics such as amino acids and nucleic acids. In large regions of the ocean, nitrogen is thought to limit the growth of phytoplankton. The impact of nitrogen limitation on the synthesis of organic carbon is not well understood, especially for the most abundant photosynthetic organism in the nitrogen-limited regions of the ocean, Prochlorococcus. This study compares the carbon metabolism of nitrogen-replete and nitrogen-limited Prochlorococcus spp. to determine how nitrogen availability influences inorganic carbon assimilation into an organic form. Metabolomics and physiological data revealed that cells under nitrogen limitation have reduced metabolic flux and total carbon fixation rates while maintaining elevated metabolite pool levels and releasing a larger proportion of total fixed carbon to the environment.
format	article
author	Martin J. Szul Stephen P. Dearth Shawn R. Campagna Erik R. Zinser
author_facet	Martin J. Szul Stephen P. Dearth Shawn R. Campagna Erik R. Zinser
author_sort	Martin J. Szul
title	Carbon Fate and Flux in <italic toggle="yes">Prochlorococcus</italic> under Nitrogen Limitation
title_short	Carbon Fate and Flux in <italic toggle="yes">Prochlorococcus</italic> under Nitrogen Limitation
title_full	Carbon Fate and Flux in <italic toggle="yes">Prochlorococcus</italic> under Nitrogen Limitation
title_fullStr	Carbon Fate and Flux in <italic toggle="yes">Prochlorococcus</italic> under Nitrogen Limitation
title_full_unstemmed	Carbon Fate and Flux in <italic toggle="yes">Prochlorococcus</italic> under Nitrogen Limitation
title_sort	carbon fate and flux in <italic toggle="yes">prochlorococcus</italic> under nitrogen limitation
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/6d7f21a1ae9e41cba001cd0460ab3c9b
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Carbon Fate and Flux in <italic toggle="yes">Prochlorococcus</italic> under Nitrogen Limitation

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