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Light‐dependent oxygen consumption in nitrogen‐fixing cyanobacteria plays a key role in nitrogenase protection 1
Author(s) -
Milligan Allen J.,
BermanFrank Ilana,
Gerchman Yoram,
Dismukes G. Charles,
Falkowski Paul G.
Publication year - 2007
Publication title -
journal of phycology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 0.85
H-Index - 127
eISSN - 1529-8817
pISSN - 0022-3646
DOI - 10.1111/j.1529-8817.2007.00395.x
Subject(s) - heterocyst , nitrogenase , trichodesmium , cyanobacteria , biology , nitrogen fixation , photosynthesis , diazotroph , anabaena , photosystem i , oxygen , biochemistry , botany , photosystem ii , biophysics , bacteria , chemistry , genetics , organic chemistry
All colonial diazotrophic cyanobacteria are capable of simultaneously evolving O 2 through oxygenic photosynthesis and fixing nitrogen via nitrogenase. Since nitrogenase is irreversibly inactivated by O 2 , accommodation of the two metabolic pathways has led to biochemical and/or structural adaptations that protect the enzyme from O 2 . In some species, differentiated cells (heterocysts) are produced within the filaments. PSII is absent in the heterocysts, while PSI activity is maintained. In other, nonheterocystous species, however, a “division of labor” occurs whereby individual cells within a colony appear to ephemerally fix nitrogen while others evolve oxygen. Using membrane inlet mass spectrometry (MIMS) in conjunction with tracer 18 O 2 and inhibitors of photosynthetic and respiratory electron transport, we examined the light dependence of O 2 consumption in Trichodesmium sp. IMS 101, a nonheterocystous, colonial cyanobacterium, and Anabaena flos‐aquae (Lyngb.) Bréb. ex Bornet et Flahault, a heterocystous species. Our results indicate that in both species, intracellular O 2 concentrations are maintained at low levels by the light‐dependent reduction of oxygen via the Mehler reaction. In N 2 ‐fixing Trichodesmium colonies, Mehler activity can consume ∼75% of gross O 2 production, while in Trichodesmium utilizing nitrate, Mehler activity declines and consumes ∼10% of gross O 2 production. Moreover, evidence for the coupling between N 2 fixation and Mehler activity was observed in purified heterocysts of Anabaena, where light accelerated O 2 consumption by 3‐fold. Our results suggest that a major role for PSI in N 2 ‐fixing cyanobacteria is to effectively act as a photon‐catalyzed oxidase, consuming O 2 through pseudocyclic electron transport while simultaneously supplying ATP in both heterocystous and nonheterocystous taxa.