Control of nitrogen fixation by oxygen depletion in surface-associated microzones

Abstract

Chronic deficiencies in biologically utilizable nitrogen control primary production in vast segments of the world's oceans1–3. A priori, it would appear that these conditions offer selective advantages to N2-fixing microorganisms (eubacteria and cyanobacteria). Most studies, however, concur that ecologically insignificant rates of N2 fixation are found in such waters4–6. We have addressed this paradox by identifying some environmental factors that may control the development and growth of marine N2 fixers and experimentally manipulating them in nitrogen-depleted North Carolina coastal Atlantic Ocean water. The availability of phosphorus, iron and molybdenum, required for both synthesis and function of the N2-fixing enzyme complex nitrogenase7, was sufficient to support the growth of N2-fixers. However, colonizable inorganic and organic surfaces were important for the development and proliferation of N2-fixing microbial consortia (mixtures of eubacteria, and cyanobacteria plus eubacteria). Surface-associated N2 fixation potentials were much more dependent on organic than on inorganic nutrient enrichment, and were affected by the incidence and magnitude of localized O2 depletion in the surface-associated micro-zones. As molecular O2 is a potent inhibitor of N2 fixation in many marine microorganisms, the extent to which biological nitrogen demands can be met by N2 fixation depends on the presence and maintenance of O2 depleted microzones.