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McQuaid, JB, Kustka AB, Obornik M, Horak A, McCrow JR, Karas BJ, Zheng H, Kindeberg T, Andersson AJ, Barbeau KA, Allen AE.  2018.  Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms. Nature. 555:534-537.   10.1038/nature25982   AbstractWebsite

In vast areas of the ocean, the scarcity of iron controls the growth and productivity of phytoplankton(1,2). Although most dissolved iron in the marine environment is complexed with organic molecules(3), picomolar amounts of labile inorganic iron species (labile iron) are maintained within the euphotic zone(4) and serve as an important source of iron for eukaryotic phytoplankton and particularly for diatoms(5). Genome-enabled studies of labile iron utilization by diatoms have previously revealed novel iron responsive transcripts(6,7), including the ferric iron-concentrating protein ISIP2A(8), but the mechanism behind the acquisition of picomolar labile iron remains unknown. Here we show that ISIP2A is a phytotransferrin that independently and convergently evolved carbonate ion-coordinated ferric iron binding. Deletion of ISIP2A disrupts high-affinity iron uptake in the diatom Phaeodactylum tricornutum, and uptake is restored by complementation with human transferrin. ISIP2A is internalized by endocytosis, and manipulation of the seawater carbonic acid system reveals a second order dependence on the concentrations of labile iron and carbonate ions. In P. tricornutum, the synergistic interaction of labile iron and carbonate ions occurs at environmentally relevant concentrations, revealing that carbonate availability co-limits iron uptake. Phytotransferrin sequences have a broad taxonomic distribution(8) and are abundant in marine environmental genomic datasets(9,10), suggesting that acidification-driven declines in the concentration of seawater carbonate ions will have a negative effect on this globally important eukaryotic iron acquisition mechanism.

Fitzsimmons, JN, Bundy RM, Al-Subiai SN, Barbeau KA, Boyle EA.  2015.  The composition of dissolved iron in the dusty surface ocean: An exploration using size-fractionated iron-binding ligands. Marine Chemistry. 173:125-135.   10.1016/j.marchem.2014.09.002   AbstractWebsite

The size partitioning of dissolved iron and organic iron-binding ligands into soluble and colloidal phases was investigated in the upper 150 m of two stations along the GA03 U.S. GEOTRACES North Atlantic transect. The size fractionation was completed using cross-flow filtration methods, followed by analysis by isotope dilution inductively-coupled plasma mass spectrometry (ID-ICP-MS) for iron and competitive ligand exchange-adsorptive cathodic stripping voltammetry (CLE-ACSV) for iron-binding ligands. On average, 80% of the 0.1-0.65 nM dissolved iron (<0.2 mu m) was partitioned into the colloidal iron (cFe) size fraction (10 kDa < cFe <0.2 gm), as expected for areas of the ocean underlying a dust plume. The 1.3-2.0 nM strong organic iron-binding ligands, however, overwhelmingly (75-77%) fell into the soluble size fraction (<10 kDa). As a result, modeling the dissolved iron size fractionation at equilibrium using the observed ligand partitioning did not accurately predict the iron partitioning into colloidal and soluble pools. This suggests that either a portion of colloidal ligands is missed by current electrochemical methods because they react with iron more slowly than the equilibration time of our CLE-ACSV method, or part of the observed colloidal iron is actually inorganic in composition and thus cannot be predicted by our model of unbound iron-binding ligands. This potentially contradicts the prevailing view that greater than >99% of dissolved iron in the ocean is organically complexed. Disentangling the chemical form of iron in the upper ocean has important implications for surface ocean biogeochemistry and may affect iron uptake by phytoplankton. (C) 2014 Elsevier B.V. All rights reserved.

Hogle, SL, Bundy RM, Blanton JM, Allen EE, Barbeau KA.  2016.  Copiotrophic marine bacteria are associated with strong iron-binding ligand production during phytoplankton blooms. Limnology and Oceanography Letters. 1:36-43.   10.1002/lol2.10026   Abstract

Although marine bacteria were identified nearly two decades ago as potential sources for strong iron-binding organic ligands detected in seawater, specific linkages between ligands detected in natural water and the microbial community remain unclear. We compared the production of different classes of iron-binding ligands, dissolved iron and macronutrient concentrations, and phytoplankton and bacterioplankton assemblages in a series of iron amended 6-d incubations. Incubations with high iron additions had near complete macronutrient consumption and higher phytoplankton biomass compared with incubations with low iron additions, but both iron treatments were dominated by diatoms. However, we only detected the strongest ligands in high-iron treatments, and strong iron-binding ligands were generally correlated with an increased abundance of copiotrophic bacteria, particularly Alteromonas strains. Ultimately, these robust correlations suggest a potential linkage between copiotrophic bacteria and strong iron-binding ligand production after iron fertilization events in the marine environment.

Stuart, RK, Bundy R, Buck K, Ghassemain M, Barbeau K, Palenik B.  2017.  Copper toxicity response influences mesotrophic Synechococcus community structure. Environmental Microbiology. 19:756-769.   10.1111/1462-2920.13630   AbstractWebsite

Picocyanobacteria from the genus Synechococcus are ubiquitous in ocean waters. Their phylogenetic and genomic diversity suggests ecological niche differentiation, but the selective forces influencing this are not well defined. Marine picocyanobacteria are sensitive to Cu toxicity, so adaptations to this stress could represent a selective force within, and between, species', also known as clades. Here, we compared Cu stress responses in cultures and natural populations of marine Synechococcus from two co-occurring major mesotrophic clades (I and IV). Using custom microarrays and proteomics to characterize expression responses to Cu in the lab and field, we found evidence for a general stress regulon in marine Synechococcus. However, the two clades also exhibited distinct responses to copper. The Clade I representative induced expression of genomic island genes in cultures and Southern California Bight populations, while the Clade IV representative downregulated Fe-limitation proteins. Copper incubation experiments suggest that Clade IV populations may harbour stress-tolerant subgroups, and thus fitness tradeoffs may govern Cu-tolerant strain distributions. This work demonstrates that Synechococcus has distinct adaptive strategies to deal with Cu toxicity at both the clade and subclade level, implying that metal toxicity and stress response adaptations represent an important selective force for influencing diversity within marine Synechococcus populations.

Moffett, JW, Brand LE, Croot PL, Barbeau KA.  1997.  Cu Speciation and Cyanobacterial Distribution in Harbors Subject to Anthropogenic Cu Inputs. Limnology and Oceanography. 42:789-799.: American Society of Limnology and Oceanography   10.2307/2838883   AbstractWebsite

Cu speciation was studied in four harbors on the south coast of Cape Cod, Massachusetts, that are exposed to varying degress of Cu contamination from anthropogenic sources. Copper in waters outside the harbors was complexed by ∼ 10 nM of very strong chelators, twofold higher than ambient Cu concentrations. In Eel Pond (Woods Hole) and Falmouth Inner Harbor, total dissolved Cu concentrations were 7-10-fold higher. However, because the strong chelators were saturated in these two harbors, the free Cu increased by 1,000-fold, from $\thicksim 10^13 M$ to $\thicksim 10^-10 M$ . There was no evidence for any enhanced biological production of chelators in response to the elevated Cu concentrations. However, cell densities of cyanobacteria, which have been proposed as a source of strong Cu chelators in seawater, decline drastically in the high Cu harbors. These trends are consistent with culture studies showing that Synechococcus sp., the predominant cyanophyte in these waters, shows a dramatic decrease in growth rates above a free Cu2+ level of 10-11 M. In Great Pond and Waquoit Bay, which showed no significant Cu contamination or saturation of strong ligands, cyanobacterial cell densities showed little or no decrease. Results suggest that significant anthropogenic inputs of Cu may overwhelm processes occurring in seawater that lead Cu and strong chelator concentrations to approach comparable levels.