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Title: Dinitrogenase-Driven Photobiological Hydrogen Production Combats Oxidative Stress in Cyanothece sp. Strain ATCC 51142

Abstract

ABSTRACT Photobiologically synthesized hydrogen (H 2) gas is carbon neutral to produce and clean to combust, making it an ideal biofuel.Cyanothecesp. strain ATCC 51142 is a cyanobacterium capable of performing simultaneous oxygenic photosynthesis and H 2production, a highly perplexing phenomenon because H 2evolving enzymes are O 2sensitive. We employed a system-levelin vivochemoproteomic profiling approach to explore the cellular dynamics of protein thiol redox and how thiol redox mediates the function of the dinitrogenase NifHDK, an enzyme complex capable of aerobic hydrogenase activity. We found that NifHDK responds to intracellular redox conditions and may act as an emergency electron valve to prevent harmful reactive oxygen species formation in concert with other cell strategies for maintaining redox homeostasis. These results provide new insight into cellular redox dynamics useful for advancing photolytic bioenergy technology and reveal a new understanding for the biological function of NifHDK. IMPORTANCEHere, we demonstrate that high levels of hydrogen synthesis can be induced as a protection mechanism against oxidative stress via the dinitrogenase enzyme complex inCyanothecesp. strain ATCC 51142. This is a previously unknown feature of cyanobacterial dinitrogenase, and we anticipate that it may represent a strategy to exploit cyanobacteria for efficient and scalable hydrogen production. We utilized amore » chemoproteomic approach to capture thein situdynamics of reductant partitioning within the cell, revealing proteins and reactive thiols that may be involved in redox sensing and signaling. Additionally, this method is widely applicable across biological systems to achieve a greater understanding of how cells navigate their environment and how redox chemistry can be utilized to alter metabolism and achieve homeostasis.« less

Authors:
; ORCiD logo; ; ; ; ; ; ; ; ORCiD logo;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1339864
Report Number(s):
PNNL-SA-113160
Journal ID: ISSN 0099-2240; 48680; KP1601010
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Applied and Environmental Microbiology; Journal Volume: 82; Journal Issue: 24
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Environmental Molecular Sciences Laboratory

Citation Formats

Sadler, Natalie C., Bernstein, Hans C., Melnicki, Matthew R., Charania, Moiz A., Hill, Eric A., Anderson, Lindsey N., Monroe, Matthew E., Smith, Richard D., Beliaev, Alexander S., Wright, Aaron T., and Nojiri, H. Dinitrogenase-Driven Photobiological Hydrogen Production Combats Oxidative Stress in Cyanothece sp. Strain ATCC 51142. United States: N. p., 2016. Web. doi:10.1128/AEM.02098-16.
Sadler, Natalie C., Bernstein, Hans C., Melnicki, Matthew R., Charania, Moiz A., Hill, Eric A., Anderson, Lindsey N., Monroe, Matthew E., Smith, Richard D., Beliaev, Alexander S., Wright, Aaron T., & Nojiri, H. Dinitrogenase-Driven Photobiological Hydrogen Production Combats Oxidative Stress in Cyanothece sp. Strain ATCC 51142. United States. doi:10.1128/AEM.02098-16.
Sadler, Natalie C., Bernstein, Hans C., Melnicki, Matthew R., Charania, Moiz A., Hill, Eric A., Anderson, Lindsey N., Monroe, Matthew E., Smith, Richard D., Beliaev, Alexander S., Wright, Aaron T., and Nojiri, H. Fri . "Dinitrogenase-Driven Photobiological Hydrogen Production Combats Oxidative Stress in Cyanothece sp. Strain ATCC 51142". United States. doi:10.1128/AEM.02098-16.
@article{osti_1339864,
title = {Dinitrogenase-Driven Photobiological Hydrogen Production Combats Oxidative Stress in Cyanothece sp. Strain ATCC 51142},
author = {Sadler, Natalie C. and Bernstein, Hans C. and Melnicki, Matthew R. and Charania, Moiz A. and Hill, Eric A. and Anderson, Lindsey N. and Monroe, Matthew E. and Smith, Richard D. and Beliaev, Alexander S. and Wright, Aaron T. and Nojiri, H.},
abstractNote = {ABSTRACT Photobiologically synthesized hydrogen (H2) gas is carbon neutral to produce and clean to combust, making it an ideal biofuel.Cyanothecesp. strain ATCC 51142 is a cyanobacterium capable of performing simultaneous oxygenic photosynthesis and H2production, a highly perplexing phenomenon because H2evolving enzymes are O2sensitive. We employed a system-levelin vivochemoproteomic profiling approach to explore the cellular dynamics of protein thiol redox and how thiol redox mediates the function of the dinitrogenase NifHDK, an enzyme complex capable of aerobic hydrogenase activity. We found that NifHDK responds to intracellular redox conditions and may act as an emergency electron valve to prevent harmful reactive oxygen species formation in concert with other cell strategies for maintaining redox homeostasis. These results provide new insight into cellular redox dynamics useful for advancing photolytic bioenergy technology and reveal a new understanding for the biological function of NifHDK. IMPORTANCEHere, we demonstrate that high levels of hydrogen synthesis can be induced as a protection mechanism against oxidative stress via the dinitrogenase enzyme complex inCyanothecesp. strain ATCC 51142. This is a previously unknown feature of cyanobacterial dinitrogenase, and we anticipate that it may represent a strategy to exploit cyanobacteria for efficient and scalable hydrogen production. We utilized a chemoproteomic approach to capture thein situdynamics of reductant partitioning within the cell, revealing proteins and reactive thiols that may be involved in redox sensing and signaling. Additionally, this method is widely applicable across biological systems to achieve a greater understanding of how cells navigate their environment and how redox chemistry can be utilized to alter metabolism and achieve homeostasis.},
doi = {10.1128/AEM.02098-16},
journal = {Applied and Environmental Microbiology},
number = 24,
volume = 82,
place = {United States},
year = {Fri Oct 14 00:00:00 EDT 2016},
month = {Fri Oct 14 00:00:00 EDT 2016}
}