Sustained H<sub>2</sub> Production Driven by Photosynthetic Water Splitting in a Unicellular Cyanobacterium

ABSTRACT The relationship between dinitrogenase-driven H2 production and oxygenic photosynthesis was investigated in a unicellular cyanobacterium, Cyanothece sp. ATCC 51142, using a novel custom-built photobioreactor equipped with advanced process control. Continuously illuminated nitrogen-deprived...

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Autores principales:	Matthew R. Melnicki, Grigoriy E. Pinchuk, Eric A. Hill, Leo A. Kucek, Jim K. Fredrickson, Allan Konopka, Alexander S. Beliaev
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2012
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/89594524346f4d8fa0e72a88ded7a117
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spelling	oai:doaj.org-article:89594524346f4d8fa0e72a88ded7a1172021-11-15T15:39:09ZSustained H<sub>2</sub> Production Driven by Photosynthetic Water Splitting in a Unicellular Cyanobacterium10.1128/mBio.00197-122150-7511https://doaj.org/article/89594524346f4d8fa0e72a88ded7a1172012-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00197-12https://doaj.org/toc/2150-7511ABSTRACT The relationship between dinitrogenase-driven H2 production and oxygenic photosynthesis was investigated in a unicellular cyanobacterium, Cyanothece sp. ATCC 51142, using a novel custom-built photobioreactor equipped with advanced process control. Continuously illuminated nitrogen-deprived cells evolved H2 at rates up to 400 µmol ⋅ mg Chl−1 ⋅ h−1 in parallel with uninterrupted photosynthetic O2 production. Notably, sustained coproduction of H2 and O2 occurred over 100 h in the presence of CO2, with both gases displaying inverse oscillations which eventually dampened toward stable rates of 125 and 90 µmol ⋅ mg Chl−1 ⋅ h−1, respectively. Oscillations were not observed when CO2 was omitted, and instead H2 and O2 evolution rates were positively correlated. The sustainability of the process was further supported by stable chlorophyll content, maintenance of baseline protein and carbohydrate levels, and an enhanced capacity for linear electron transport as measured by chlorophyll fluorescence throughout the experiment. In situ light saturation analyses of H2 production displayed a strong dose dependence and lack of O2 inhibition. Inactivation of photosystem II had substantial long-term effects but did not affect short-term H2 production, indicating that the process is also supported by photosystem I activity and oxidation of endogenous glycogen. However, mass balance calculations suggest that carbohydrate consumption in the light may, at best, account for no more than 50% of the reductant required for the corresponding H2 production over that period. Collectively, our results demonstrate that uninterrupted H2 production in unicellular cyanobacteria can be fueled by water photolysis without the detrimental effects of O2 and have important implications for sustainable production of biofuels. IMPORTANCE The study provides an important insight into the photophysiology of light-driven H2 production by the nitrogen-fixing cyanobacterium Cyanothece sp. strain ATCC 51142. This work is also of significance for biotechnology, supporting the feasibility of “direct biophotolysis.” The sustainability of the process, highlighted by prolonged gas evolution with no clear sign of significant decay or apparent photodamage, provides a foundation for the future development of an effective, renewable, and economically efficient bio-H2 production process.Matthew R. MelnickiGrigoriy E. PinchukEric A. HillLeo A. KucekJim K. FredricksonAllan KonopkaAlexander S. BeliaevAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 4 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Matthew R. Melnicki Grigoriy E. Pinchuk Eric A. Hill Leo A. Kucek Jim K. Fredrickson Allan Konopka Alexander S. Beliaev Sustained H<sub>2</sub> Production Driven by Photosynthetic Water Splitting in a Unicellular Cyanobacterium
description	ABSTRACT The relationship between dinitrogenase-driven H2 production and oxygenic photosynthesis was investigated in a unicellular cyanobacterium, Cyanothece sp. ATCC 51142, using a novel custom-built photobioreactor equipped with advanced process control. Continuously illuminated nitrogen-deprived cells evolved H2 at rates up to 400 µmol ⋅ mg Chl−1 ⋅ h−1 in parallel with uninterrupted photosynthetic O2 production. Notably, sustained coproduction of H2 and O2 occurred over 100 h in the presence of CO2, with both gases displaying inverse oscillations which eventually dampened toward stable rates of 125 and 90 µmol ⋅ mg Chl−1 ⋅ h−1, respectively. Oscillations were not observed when CO2 was omitted, and instead H2 and O2 evolution rates were positively correlated. The sustainability of the process was further supported by stable chlorophyll content, maintenance of baseline protein and carbohydrate levels, and an enhanced capacity for linear electron transport as measured by chlorophyll fluorescence throughout the experiment. In situ light saturation analyses of H2 production displayed a strong dose dependence and lack of O2 inhibition. Inactivation of photosystem II had substantial long-term effects but did not affect short-term H2 production, indicating that the process is also supported by photosystem I activity and oxidation of endogenous glycogen. However, mass balance calculations suggest that carbohydrate consumption in the light may, at best, account for no more than 50% of the reductant required for the corresponding H2 production over that period. Collectively, our results demonstrate that uninterrupted H2 production in unicellular cyanobacteria can be fueled by water photolysis without the detrimental effects of O2 and have important implications for sustainable production of biofuels. IMPORTANCE The study provides an important insight into the photophysiology of light-driven H2 production by the nitrogen-fixing cyanobacterium Cyanothece sp. strain ATCC 51142. This work is also of significance for biotechnology, supporting the feasibility of “direct biophotolysis.” The sustainability of the process, highlighted by prolonged gas evolution with no clear sign of significant decay or apparent photodamage, provides a foundation for the future development of an effective, renewable, and economically efficient bio-H2 production process.
format	article
author	Matthew R. Melnicki Grigoriy E. Pinchuk Eric A. Hill Leo A. Kucek Jim K. Fredrickson Allan Konopka Alexander S. Beliaev
author_facet	Matthew R. Melnicki Grigoriy E. Pinchuk Eric A. Hill Leo A. Kucek Jim K. Fredrickson Allan Konopka Alexander S. Beliaev
author_sort	Matthew R. Melnicki
title	Sustained H<sub>2</sub> Production Driven by Photosynthetic Water Splitting in a Unicellular Cyanobacterium
title_short	Sustained H<sub>2</sub> Production Driven by Photosynthetic Water Splitting in a Unicellular Cyanobacterium
title_full	Sustained H<sub>2</sub> Production Driven by Photosynthetic Water Splitting in a Unicellular Cyanobacterium
title_fullStr	Sustained H<sub>2</sub> Production Driven by Photosynthetic Water Splitting in a Unicellular Cyanobacterium
title_full_unstemmed	Sustained H<sub>2</sub> Production Driven by Photosynthetic Water Splitting in a Unicellular Cyanobacterium
title_sort	sustained h<sub>2</sub> production driven by photosynthetic water splitting in a unicellular cyanobacterium
publisher	American Society for Microbiology
publishDate	2012
url	https://doaj.org/article/89594524346f4d8fa0e72a88ded7a117
work_keys_str_mv	AT matthewrmelnicki sustainedhsub2subproductiondrivenbyphotosyntheticwatersplittinginaunicellularcyanobacterium AT grigoriyepinchuk sustainedhsub2subproductiondrivenbyphotosyntheticwatersplittinginaunicellularcyanobacterium AT ericahill sustainedhsub2subproductiondrivenbyphotosyntheticwatersplittinginaunicellularcyanobacterium AT leoakucek sustainedhsub2subproductiondrivenbyphotosyntheticwatersplittinginaunicellularcyanobacterium AT jimkfredrickson sustainedhsub2subproductiondrivenbyphotosyntheticwatersplittinginaunicellularcyanobacterium AT allankonopka sustainedhsub2subproductiondrivenbyphotosyntheticwatersplittinginaunicellularcyanobacterium AT alexandersbeliaev sustainedhsub2subproductiondrivenbyphotosyntheticwatersplittinginaunicellularcyanobacterium
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Sustained H<sub>2</sub> Production Driven by Photosynthetic Water Splitting in a Unicellular Cyanobacterium

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