Iron (Fe) is a paradox in the modern ocean – it is central to many life-critical enzymes but is scarce across most surface waters. The high cellular demand and low bioavailability of Fe likely puts selective pressure on marine microorganisms. Previous observations suggest that heterotrophic bacteria are outcompeted by small diatoms for Fe supply in the subantarctic zone of Southern Ocean, thereby challenging the idea of heterotrophic bacteria being more competitive than phytoplankton in the access to this trace metal. To test this hypothesis, incubation experiments were carried out at the Southern Ocean Time Series site (March–April 2016). We investigated (a) whether dissolved organic carbon (DOC), dissolved Fe, or both limit the growth of heterotrophic bacteria and, (b) if the presence of potential competitors has consequences on the bacterial Fe acquisition. We observed a pronounced increase in both bulk and cell-specific bacterial production in response to single (+C) and combined (+Fe+C) additions, but no changes in these rates when only Fe was added (+Fe). Moreover, we found that +Fe+C additions promoted increases in cell-specific bacterial Fe uptake rates, and these increases were particularly pronounced (by 13-fold) when phytoplankton were excluded from the incubations. These results suggest that auto- and heterotrophs could compete for Fe when DOC limitation of bacterial growth is alleviated. Such interactions between primary producers and nutrient-recyclers are unexpected drivers for the duration and magnitude of phytoplankton blooms in the Southern Ocean.
Dissolved iron (dFe) availability limits the uptake of atmospheric CO 2 by the Southern Ocean (SO) biological pump. Hence, any change in bioavailable dFe in this region can directly influence climate. On the basis of Fe uptake experiments with Phaeocystis antarctica , we show that the range of dFe bioavailability in natural samples is wider (<1 to ~200% compared to free inorganic Fe′) than previously thought, with higher bioavailability found near glacial sources. The degree of bioavailability varied regardless of in situ dFe concentration and depth, challenging the consensus that sole dFe concentrations can be used to predict Fe uptake in modeling studies. Further, our data suggest a disproportionately major role of biologically mediated ligands and encourage revisiting the role of humic substances in influencing marine Fe biogeochemical cycling in the SO. Last, we describe a linkage between in situ dFe bioavailability and isotopic signatures that, we anticipate, will stimulate future research.
Across the Southern Ocean, phytoplankton growth is governed by iron and light, while bacterial growth is regulated by iron and labile dissolved organic carbon (LDOC). We use a mechanistic model to examine how competition for iron between phytoplankton and bacteria responds to changes in iron, light, and LDOC. Consistent with experimental evidence, increasing iron and light encourages phytoplankton dominance, while increasing LDOC and decreasing light favors bacterial dominance. Under elevated LDOC, bacteria can outcompete phytoplankton for iron, most easily under lower iron. Simulations reveal that bacteria are major iron consumers and suggest that luxury storage plays a key role in competitive iron uptake. Under seasonal conditions typical of the Southern Ocean, sources of LDOC besides phytoplankton exudation modulate the strength of competitive interactions. Continued investigations on the competitive fitness of bacteria in driving changes in primary production in iron‐limited systems will be invaluable in refining these results.
Melting sea ice is a seasonal source of iron (Fe) to the Southern Ocean (SO), where Fe levels in surface waters are otherwise generally too low to support phytoplankton growth. However, the effectiveness of sea-ice Fe fertilization in stimulating SO primary production is unknown since no data exist on Fe uptake by microorganisms in the sea-ice environment. This study reports a unique dataset on Fe uptake rates, Fe-to-carbon (C) uptake ratio (Fe uptake normalized to C uptake) and Fe:C uptake rate (Fe uptake normalized to biomass) by in situ microbial communities inhabiting sea ice and the underlying seawater. Radioisotopes55Fe and14C were used in short-term uptake experiments during the 32-day Ice Station POLarstern (ISPOL) time series to evaluate the contributions of small (0.8–10 µm) and large (> 10 µm) microbes to Fe uptake. Overall, results show that over 90% of Fe was bound to the outside of the cells. Intracellular Fe (Feintra) uptake rates reached up to 68, 194, and 203 pmol Fe L−1d− 1in under-ice seawater, bottom ice, and top ice, respectively. Inorganic carbon uptake ranged between 0.03 and 3.2 µmol C L−1d−1, with the lowest rate observed in under-ice seawater. Importantly, between the start and end of ISPOL, we observed a 30-fold increase in Feintranormalized to carbon biomass in bottom sea ice. This trend was likely due to changes in the microbial community from a dominance of large diatoms at the start of the survey to small diatoms later in the season. As the Antarctic icescape and associated ecosystems are changing, this dataset will help inform the parameterisation of sea-ice biogeochemical and ecological models in ice-covered regions.
Iron and carbon are essential for microbial heterotrophic activity, but the bioavailability of these elements is low in surface waters of the Southern Ocean. Whether the access to iron and carbon differs among phylogenetic groups of prokaryotes is barely known. To address this question we used iron (55FeCl3), and the carbon compounds chitin (3H-Diacetylchitobiose) and leucine (3H-leucine) as model substrates in combination with MICRO-CARD-FISH during spring phytoplankton blooms induced by natural iron fertilization off Kerguelen Island (KErguelen Ocean and Plateau compared Study 2 - KEOPS2; October-November 2011). The application of probes at broad phylogenetic levels indicated an overall similar community composition in surface waters at the 8 investigated sites. The relative contributions of the prokaryotic groups to abundance revealed a strong positive relationship with their respective contributions to the leucine-active community (p0.05; r=0.26). These results suggest preferential uptake of iron and chitin by some prokaryotic groups. SAR11 and Cytophaga-Flavobacterium-Bacteroides (CFB) were the dominant contributors to the leucine-active community, while CFB and Archaea had the highest contributions to the chitin-active community. By contrast, Gammaproteobacteria, including SAR86, and CFB revealed the highest contributions to the iron-active community. We found several correlations between the group-specific fractions of active cells for a given substrate and most of them included CFB, pointing to the potential importance of microbial interactions for iron and carbon cycling in the Southern Ocean.
In the Subantarctic sector of the Southern Ocean, vertical entrainment of iron (Fe) triggers the seasonal productivity cycle but diminishing physical supply during the spring to summer transition forces microbial assemblages to rapidly acclimate. Here, we tested how phytoplankton and bacteria within an isolated eddy respond to different dissolved Fe (DFe)/ligand inputs. We used three treatments: one that mimicked the entrainment of new DFe (Fe-NEW), another in which DFe was supplied from bacterial regeneration of particles (Fe-REG), and a control with no addition of DFe (Fe-NO). After 6 days, 3.5 (Fe-NO, Fe-NEW) to 5-fold (Fe-REG) increases in Chlorophyll a were observed. These responses of the phytoplankton community were best explained by the differences between the treatments in the amount of DFe recycled during the incubation (Fe-REG, 15% recycled c.f. 40% Fe-NEW, 60% Fe-NO). This additional recycling was more likely mediated by bacteria. By day 6, bacterial production was comparable between Fe-NO and Fe-NEW but was approximately two-fold higher in Fe-REG. A preferential response of phytoplankton (haptophyte-dominated) relative to high nucleic acid (HNA) bacteria was also found in the Fe-REG treatment while the relative proportion of diatoms increased faster in the Fe-NEW and Fe-NO treatments. Comparisons between light and dark incubations further confirmed the competition between picophytoplankton and HNA for DFe. Overall, our results demonstrate great versatility by microorganisms to use different Fe sources that results in highly efficient Fe recycling within surface waters. This study also encourages future research to further investigate the interactions between functional groups of microbes (e.g. HNA and cyanobacteria) to better constraint modeling in Fe and carbon biogeochemical cycles.