Abstract
Iron (Fe) is widely suspected as a key controlling factor of N2 fixation due to the high Fe content of nitrogenase and photosynthetic enzymes complex, and to its low concentrations in oceanic surface seawaters. The influence of Fe limitation on the recently discovered unicellular diazotrophic cyanobacteria (UCYN) is poorly understood despite their biogeochemical importance in the carbon and nitrogen cycles. To address this knowledge gap, we conducted culture experiments on Crocosphaera watsonii WH8501 growing under a range of dissolved Fe concentrations (from 3.3 to 403 nM). Overall, severe Fe limitation led to significant decreases in growth rate (2.6-fold), C, N and chlorophyll a contents per cell (up to 4.1-fold), N2 and CO2 fixation rates per cell (17- and 7-fold) as well as biovolume (2.2-fold). We highlighted a two phased response depending on the degree of limitation: (i) under a moderate Fe limitation, the biovolume of C. watsonii was strongly reduced, allowing the cells to keep sufficient energy to maintain an optimal growth, volume-normalized contents and N2 and CO2 fixation rates; (ii) with increasing Fe deprivation, biovolume remained unchanged but the entire cell metabolism was affected, as shown by a strong decrease in the growth rate, volume-normalized contents and N2 and CO2 fixation rates. The half-saturation constant for growth of C. watsonii with respect to Fe is twice as low as that of the filamentous Trichodesmium indicating a better adaptation of C. watsonii to poor Fe environments than filamentous diazotrophs. The physiological response of C. watsonii to Fe limitation was different from that previously shown on the UCYN Cyanothece sp, suggesting potential differences in Fe requirements and/or Fe acquisition within the UCYN community. These results contribute to a better understanding of how Fe bioavailability can control the activity of UCYN and explain the biogeography of diverse N2 fixers in ocean.
Highlights
In oligotrophic oceanic regions, bioavailable nitrogen (N) concentrations are sufficiently low that they set a constraint on primary productivity [1]
Field measurements have highlighted that N2 fixation rates associated with unicellular diazotrophic cyanobacteria (UCYN) probably equal or exceed those associated with Trichodesmium sp. at regional scale [4]
Decreases in the N2 fixation and growth rates of C. watsonii have been observed in one Felimited culture [32] and recent field enrichment experiments in the tropical Atlantic and Pacific have revealed that abundance of UCYN-B could be Fe limited in their natural habitats [27,28,33]
Summary
Bioavailable nitrogen (N) concentrations are sufficiently low that they set a constraint on primary productivity [1]. Decreases in the N2 fixation and growth rates of C. watsonii have been observed in one Felimited culture [32] and recent field enrichment experiments in the tropical Atlantic and Pacific have revealed that abundance of UCYN-B could be Fe limited in their natural habitats [27,28,33]. In order to improve our knowledge and understanding of the impact of Fe limitation on UCYN, we conducted trace-metal clean culture experiments of C. watsonii WH8501 cultivated under a range of dFe concentrations to quantify for the first time the impact of Fe limitation on the growth, N2 fixation rate, primary productivity, elemental contents, and cell size of an open ocean UCYN
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