Optimization of metabolic capacity and flux through environmental cues to maximize hydrogen production by the Cyanobacterium "Arthrospira (Spirulina) maxima"

Gennady Ananyev, Damian Carrieri, G. Charles Dismukes

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Abstract

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.

Original languageEnglish
Pages (from-to)6102-6113
Number of pages12
JournalApplied and Environmental Microbiology
Volume74
Issue number19
DOIs
Publication statusPublished - Oct 2008

Fingerprint

Spirulina maxima
Arthrospira
Spirulina
environmental cue
hydrogen production
NAD (coenzyme)
Cyanobacteria
NAD
fermentation
Cues
cyanobacterium
Hydrogen
hydrogen
Glycogen
ferredoxin hydrogenase
photosynthesis
glycogen
Fermentation
nitrate
Photosynthesis

ASJC Scopus subject areas

  • Applied Microbiology and Biotechnology
  • Food Science
  • Biotechnology
  • Ecology

Cite this

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abstract = "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.",
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