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Applied and Environmental Microbiology, October 2008, p. 6102-6113, Vol. 74, No. 19
0099-2240/08/$08.00+0     doi:10.1128/AEM.01078-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Optimization of Metabolic Capacity and Flux through Environmental Cues To Maximize Hydrogen Production by the Cyanobacterium "Arthrospira (Spirulina) maxima"{triangledown} ,{dagger}

Gennady Ananyev, Damian Carrieri, and G. Charles Dismukes*

Department of Chemistry, Princeton University, and Princeton Environmental Institute, Princeton, New Jersey 08544

Received 13 May 2008/ Accepted 23 July 2008

Environmental and nutritional conditions that optimize the yield of hydrogen (H2) from water using a two-step photosynthesis/fermentation (P/F) process are reported for the hypercarbonate-requiring cyanobacterium "Arthrospira maxima." Our observations lead to four main conclusions broadly applicable to fermentative H2 production by bacteria: (i) anaerobic H2 production in the dark from whole cells catalyzed by a bidirectional [NiFe] hydrogenase is demonstrated to occur in two temporal phases involving two distinct metabolic processes that are linked to prior light-dependent production of NADPH (photosynthetic) and dark/anaerobic production of NADH (fermentative), respectively; (ii) H2 evolution from these reductants represents a major pathway for energy production (ATP) during fermentation by regenerating NAD+ essential for glycolysis of glycogen and catabolism of other substrates; (iii) nitrate removal during fermentative H2 evolution is shown to produce an immediate and large stimulation of H2, as nitrate is a competing substrate for consumption of NAD(P)H, which is distinct from its slower effect of stimulating glycogen accumulation; (iv) environmental and nutritional conditions that increase anaerobic ATP production, prior glycogen accumulation (in the light), and the intracellular reduction potential (NADH/NAD+ ratio) are shown to be the key variables for elevating H2 evolution. Optimization of these conditions and culture age increases the H2 yield from a single P/F cycle using concentrated cells to 36 ml of H2/g (dry weight) and a maximum 18% H2 in the headspace. H2 yield was found to be limited by the hydrogenase-mediated H2 uptake reaction.

* Corresponding author. Mailing address: Department of Chemistry, Princeton University, Hoyt Laboratory, Princeton, NJ 08544. Phone: (609) 258-3896. Fax: (609) 258-1980. E-mail: dismukes{at}princeton.edu

{triangledown} Published ahead of print on 1 August 2008.

{dagger} Supplemental material for this article may be found at http://aem.asm.org/.

Applied and Environmental Microbiology, October 2008, p. 6102-6113, Vol. 74, No. 19
0099-2240/08/$08.00+0     doi:10.1128/AEM.01078-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.





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