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Researchers Discover How Oxygen Attacks Hydrogen-Producing Enzymes in Photosynthetic Organisms; Insight Could Assist Identification of New Pathways for Bio-Hydrogen Production
29 September 2009
An international team of scientists from the UK, Germany and France have discovered how oxygen stops photosynthetic organisms such as green algae from producing hydrogen. The findings could help advance development of the microbial production of hydrogen from sunlight and water. They reported their results in two papers, one last week in the Journal of the American Chemical Society and one in the Proceedings of the National Academy of Sciences, published this week.
One promising approach to the renewable production of hydrogen is the use of microorganisms. Enzymes called hydrogenases are responsible for evolving hydrogen in biological processes ranging from fermentation to photosynthesis. There are two main classes of hydrogenases: nickel-iron [NiFE]- and iron-iron [FeFe]-. These are highly efficient enzymes, and have been shown to function as superb electrocatalysts of hydrogen oxidation and production. However, the [FeFe]-hydrogenases, considered the most active in hydrogen production, are irreparably damaged when exposed to oxygen.
The hydrogen-producing enzyme found in green algae, known as an iron-iron hydrogenase, has evolved a structure that makes it particularly susceptible to attacking oxygen molecules. Because oxygen is a major by-product of the hydrogen-making photosynthetic process in such organisms, the build-up of oxygen, which rapidly attacks the active site of the enzyme, quickly brings the hydrogen-making process to an irreversible halt. Our work has revealed the mechanism of this process.—Professor Fraser Armstrong, Oxford University, co-author
The team used electrochemical kinetic methods to determine the order of events in which oxygen attacks the active site of an iron-iron hydrogenase found in the green algae Chlamydomonas reinhardtii. They combined their observations with data obtained from X-ray absorption spectroscopy. By measuring ripples in the photoelectron energy spectrum of the enzyme under X-ray bombardment they were able to deduce the nature of the damage caused to the active site following attack by oxygen.
Yet while the research reported in PNAS shows just how destructive oxygen is to the enzyme powering green algae’s hydrogen-making process, the team’s research reported in JACS shows that similar hydrogenases produced by other microorganisms may possess greater tolerance to oxygen, sufficient perhaps to survive in the presence of oxygen released during photosynthetic hydrogen production.
It shows that whilst we may have found a major obstacle along one route to the biological production of hydrogen, this knowledge could help us to identify new routes where nature could suggest an answer to the problem of oxygen’s destructive effect on hydrogen-producing enzymes.—Professor Armstrong
The team will shortly be publishing the results of similar research into nickel-iron hydrogenases, enzymes related to those that enable blue-green algae to produce hydrogen.
Gabrielle Goldet, Caterina Brandmayr, Sven T. Stripp, Thomas Happe, Christine Cavazza, Juan C. Fontecilla-Camps and Fraser A. Armstrong (2009) Electrochemical Kinetic Investigations of the Reactions of [FeFe]-Hydrogenases with Carbon Monoxide and Oxygen: Comparing the Importance of Gas Tunnels and Active-Site Electronic/Redox Effects. J. Am. Chem. Soc., Article ASAP doi: 10.1021/ja905388j
Sven T. Stripp, Gabrielle Goldet, Caterina Brandmayr, Oliver Sanganas, Kylie A. Vincent, Michael Haumann, Fraser A. Armstrong and Thomas Happe (2009) How oxygen attacks [FeFe] hydrogenases from photosynthetic organisms. PNAS, doi: 10.1073/pnas.0905343106
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