Impact of iron limitation on primary production (dissolved and particulate) and secondary production in cultured Trichodesmium sp.

E Rochelle-Newall,S L’Helguen,C Ridame,C Dimier-Hugueney

doi:10.3354/ame01690

Abstract

Diazotrophic cyanobacteria play an important role in biogeochemical cycles of carbon and nitrogen and, hence, in oceanic productivity in the tropical and subtropical regions of the ocean. Although many studies have examined the impact of iron (Fe) limitation on particulate primary production and dinitrogen (N2) fixation in the colonial cyanobacterium Trichodesmium, none have looked at the impact of Fe limitation on the percentage extracellular release (PER) and secondary production (SP) in Fe-limited cultures of this cyanobacterium. Here, we present the results of a series of culture experiments during which we examined the impact of 3 concentrations of dissolved iron (DFe) on total primary production (TPP = dissolved + particulate primary production, i.e. DPP + PPP), PER and on SP. Under severe Fe limitation (5 nM DFe), biomass, growth rates, TPP and N2 fixation were strongly reduced, while PER increased relative to the rates ob served at the highest Fe concentration. Moreover, reducing Fe concentration induced an increase in the percentage of photosynthetically fixed C used for algal growth, while the percentage of C used to support algal respiration decreased. Reduced Fe concentrations also induced a decrease in SP and in the SP:DPP ratio, indicating that the efficiency of transfer of fixed carbon from autotrophic to heterotrophic processes is reduced. This suggests that Fe, either directly through influencing cellular processes or indirectly through influencing organic matter structure or nitrogen availability, is controlling SP and, thus, microbial carbon utilization. These results suggest that the amount of carbon entering into the microbial loop may be reduced under Fe limitation, thus leading to an accumulation of dissolved organic carbon with potentially important impacts on microbial carbon cycling and, ultimately, on the biological carbon pump

Highlights

In tropical and subtropical nutrient-poor ocean waters, the diazotrophic filamentous cyanobacteria Trichodesmium spp. form extensive blooms and can dominate phytoplankton assemblages
These rates decreased from 1.96 ± 0.28 ng N μg particulate organic carbon (POC)−1 h−1 to 0.40 ± 0.10 ng N μg POC−1 h−1 for dissolved Fe (DFe) concentrations of 100 nM and 5 nM, respectively (p < 0.05)
The impacts of Fe limitation on the production and transfer of organic carbon from Trichodesmium and other diazotrophic cyanobacteria to the microbial loop need to be further investigated, in in situ conditions that take into account the diversity of the associated bacterial heterotrophs

Summary

Introduction

In tropical and subtropical nutrient-poor ocean waters, the diazotrophic filamentous cyanobacteria Trichodesmium spp. form extensive blooms and can dominate phytoplankton assemblages. Diazotrophic cyanobacteria have relatively high Fe requirements and it is estimated that N2-fixing organisms such as Trichodesmium require up to 5 times more Fe than non-diazotrophic phytoplankton (Berman-Frank et al 2001, Kustka et al 2003b). In both cultured and natural populations, reduced N2 fixation has been observed in Trichodesmium at low dissolved Fe concentrations (Berman-Frank et al 2001, Moore et al 2009). In regions of low Fe availability, N2 fixation can be limited by Fe or co-limited by Fe and phosphorus (Mills et al 2004), in large open ocean areas, isolated from continental inputs and weakly impacted by the atmospheric deposition of desert dust

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Discussion

Conclusion