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Journal Article
Roe, KL, Barbeau K, Mann EL, Haygood MG.  2012.  Acquisition of iron by Trichodesmium and associated bacteria in culture. Environmental Microbiology. 14:1681-1695.   10.1111/j.1462-2920.2011.02653.x   AbstractWebsite

Trichodesmium colonies contain an abundant microbial consortium that is likely to play a role in nutrient cycling within the colony. This study used laboratory cultures of Trichodesmium and two genome-sequenced strains of bacteria typical of Trichodesmium-associated microbes to develop an understanding of the cycling of iron, a potentially limiting micronutrient, within Trichodesmium colonies. We found that the ferric siderophores desferrioxamine B and aerobactin were not readily bioavailable to Trichodesmium, relative to ferric chloride or citrate-associated iron. In contrast, the representative bacterial strains we studied were able to acquire iron from all of the iron sources, implying that naturally occurring Trichodesmium-associated bacteria may be capable of utilizing a more diverse array of iron sources than Trichodesmium. From the organism-specific uptake data collected in this study, a theoretical Trichodesmium colony was designed to model whole colony iron uptake. The bacteria accounted for most (> 70%) of the iron acquired by the colony, highlighting the importance of determining organism-specific uptake in a complex environment. Our findings suggest that, although they may share the same micro-environment, Trichodesmium and its colony-associated microbial cohort may differ substantially in terms of iron acquisition strategy.

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.

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.

Hogle, SL, Brahamsha B, Barbeau KA.  2017.  Direct Heme Uptake by Phytoplankton-Associated Roseobacter Bacteria. mSystems. 2(1):e00124-16.   10.1128/mSystems.00124-16   AbstractWebsite

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Dupont, CL, McCrow JP, Valas R, Moustafa A, Walworth N, Goodenough U, Roth R, Hogle SL, Bai J, Johnson ZI, Mann E, Palenik B, Barbeau KA, Craig Venter J, Allen AE.  2015.  Genomes and gene expression across light and productivity gradients in eastern subtropical Pacific microbial communities. ISME J. 9:1076-1092.: International Society for Microbial Ecology   10.1038/ismej.2014.198   Abstract

Transitions in community genomic features and biogeochemical processes were examined in surface and subsurface chlorophyll maximum (SCM) microbial communities across a trophic gradient from mesotrophic waters near San Diego, California to the oligotrophic Pacific. Transect end points contrasted in thermocline depth, rates of nitrogen and CO2 uptake, new production and SCM light intensity. Relative to surface waters, bacterial SCM communities displayed greater genetic diversity and enrichment in putative sulfur oxidizers, multiple actinomycetes, low-light-adapted Prochlorococcus and cell-associated viruses. Metagenomic coverage was not correlated with transcriptional activity for several key taxa within Bacteria. Low-light-adapted Prochlorococcus, Synechococcus, and low abundance gamma-proteobacteria enriched in the>3.0-[mu]m size fraction contributed disproportionally to global transcription. The abundance of these groups also correlated with community functions, such as primary production or nitrate uptake. In contrast, many of the most abundant bacterioplankton, including SAR11, SAR86, SAR112 and high-light-adapted Prochlorococcus, exhibited low levels of transcriptional activity and were uncorrelated with rate processes. Eukaryotes such as Haptophytes and non-photosynthetic Aveolates were prevalent in surface samples while Mamielles and Pelagophytes dominated the SCM. Metatranscriptomes generated with ribosomal RNA-depleted mRNA (total mRNA) coupled to in vitro polyadenylation compared with polyA-enriched mRNA revealed a trade-off in detection eukaryotic organelle and eukaryotic nuclear origin transcripts, respectively. Gene expression profiles of SCM eukaryote populations, highly similar in sequence identity to the model pelagophyte Pelagomonas sp. CCMP1756, suggest that pelagophytes are responsible for a majority of nitrate assimilation within the SCM.

Hogle, SL, Barbeau KA, Gledhill M.  2014.  Heme in the marine environment: from cells to the iron cycle. Metallomics. 6:1107-1120.   10.1039/c4mt00031e   AbstractWebsite

Hemes are iron containing heterocyclic molecules important in many cellular processes. In the marine environment, hemes participate as enzymatic cofactors in biogeochemically significant processes like photosynthesis, respiration, and nitrate assimilation. Further, hemoproteins, hemes, and their analogs appear to be iron sources for some marine bacterioplankton under certain conditions. Current oceanographic analytical methodologies allow for the extraction and measurement of heme b from marine material, and a handful of studies have begun to examine the distribution of heme b in ocean basins. The study of heme in the marine environment is still in its infancy, but some trends can be gleaned from the work that has been published so far. In this review, we summarize what is known or might be inferred about the roles of heme in marine microbes as well as the few studies on heme in the marine environment that have been conducted to date. We conclude by presenting some future questions and challenges for the field.

Hopkinson, BM, Roe KL, Barbeau KA.  2008.  Heme uptake by Microscilla marina and evidence for heme uptake systems in the genomes of diverse marine bacteria. Applied and Environmental Microbiology. 74:6263-6270.   10.1128/aem.00964-08   AbstractWebsite

The ability to acquire diverse and abundant forms of iron would be expected to confer a survival advantage in the marine environment, where iron is scarce. Marine bacteria are known to use siderophores and inorganic iron, but their ability to use heme, an abundant intracellular iron form, has only been examined preliminarily. Microscilla marina, a cultured relative of a bacterial group frequently found on marine particulates, was used as a model organism to examine heme uptake. Searches of the genome revealed analogs to known heme transport proteins, and reverse transcription-quantitative PCR analysis of these genes showed that they were expressed and upregulated under iron stress and during growth on heme. M. marina was found to take up heme-bound iron and could grow on heme as a sole iron source, supporting the genetic evidence for heme transport. Similar putative heme transport components were identified in the genomes of diverse marine bacteria. These systems were found in the genomes of many bacteria thought to be particle associated but were lacking in known free-living organisms (e.g., Pelagibacter ubique and marine cyanobacteria). This distribution of transporters is consistent with the hydrophobic, light-sensitive nature of heme, suggesting that it is primarily available on phytoplankton or detritus or in nutrient-rich environments.

Hopkinson, BM, Barbeau KA.  2008.  Interactive influences of iron and light limitation on phytoplankton at subsurface chlorophyll maxima in the eastern North Pacific. Limnology and Oceanography. 53:1303-1318.   10.4319/lo.2008.53.4.1303   AbstractWebsite

The roles of iron and light as limiting and colimiting factors for phytoplankton growth in subsurface chlorophyll maxima (SCMs) were investigated in mesotrophic to oligotrophic waters of the Southern California Bight and the eastern tropical North Pacific using microcosm manipulation experiments. Phytoplankton responses indicative of iron-light colimitation were found at several SCMs underlying macronutrient-limited surface waters in the eastern Pacific. Iron additions led to a shift in the size and taxonomic structure of the phytoplankton community, where large diatoms dominated what was formerly a diverse community of relatively small phytoplankton. The strongest and most ubiquitous responses of diatoms to iron addition were found under elevated light conditions, indicating that iron availability may have the greatest potential to affect SCM phytoplankton communities when light levels increase rapidly, such as during eddy events or with strong internal waves. The results show that iron influences phytoplankton community structure at SCMs, which would have consequences for nutrient cycling and carbon export within the lower euphotic zone.

Pizeta, I, Sander SG, Hudson RJM, Omanovic D, Baars O, Barbeau KA, Buck KN, Bundy RM, Carrasco G, Croot PL, Garnier C, Gerringa LJA, Gledhill M, Hirose K, Kondo Y, Laglera LM, Nuester J, Rijkenberg MJA, Takeda S, Twining BS, Wells M.  2015.  Interpretation of complexometric titration data: An intercomparison of methods for estimating models of trace metal complexation by natural organic ligands. Marine Chemistry. 173:3-24.   10.1016/j.marchem.2015.03.006   AbstractWebsite

With the common goal of more accurately and consistently quantifying ambient concentrations of free metal ions and natural organic ligands in aquatic ecosystems, researchers from 15 laboratories that routinely analyze trace metal speciation participated in an intercomparison of statistical methods used to model their most common type of experimental dataset, the complexometric titration. All were asked to apply statistical techniques that they were familiar with to model synthetic titration data that are typical of those obtained by applying state-of-the-art electrochemical methods - anodic stripping voltammetry (ASV) and competitive ligand equilibration-adsorptive cathodic stripping voltammetry (CLE-ACSV) - to the analysis of natural waters. Herein, we compare their estimates for parameters describing the natural ligands, examine the accuracy of inferred ambient free metal ion concentrations (]M-f]), and evaluate the influence of the various methods and assumptions used on these results. The ASV-type titrations were designed to test each participant's ability to correctly describe the natural ligands present in a sample when provided with data free of measurement error, i.e., random noise. For the three virtual samples containing just one natural ligand, all participants were able to correctly identify the number of ligand classes present and accurately estimate their parameters. For the four samples containing two or three ligand classes, a few participants detected too few or too many classes and consequently reported inaccurate 'measurements' of ambient [M-f]. Since the problematic results arose from human error rather than any specific method of analyzing the data, we recommend that analysts should make a practice of using one's parameter estimates to generate simulated (back-calculated) titration curves for comparison to the original data. The root-mean-squared relative error between the fitted observations and the simulated curves should be comparable to the expected precision of the analytical method and upon visual inspection the distribution of residuals should not be skewed. Modeling the synthetic, CLE-ACSV-type titration dataset, which comprises 5 titration curves generated at different analytical-windows or levels of competing ligand added to the virtual sample, proved to be more challenging due to the random measurement error that was incorporated. Comparison of the submitted results was complicated by the participants' differing interpretations of their task. Most adopted the provided 'true' instrumental sensitivity in modeling the CLE-ACSV curves, but several estimated sensitivities using internal calibration, exactly as is required for actual samples. Since most fitted sensitivities were biased low, systematic error in inferred ambient [M-f] and in estimated weak ligand (L-2) concentrations resulted. The main distinction between the mathematical approaches taken by participants lies in the functional form of the speciation model equations, with their implicit definition of independent and dependent or manipulated variables. In 'direct modeling', the dependent variable is the measured [M-f] (or I-p) and the total metal concentration ([M](T)) is considered independent In other, much more widely used methods of analyzing titration data - classical linearization, best known as van den Berg/Ruzic and isotherm fitting by nonlinear regression, best known as the langmuir or Gerringa methods - [M-f] is defined as independent and the dependent variable calculated from both [M](T) and [M-f]. Close inspection of the biases and variability in the estimates of ligand parameters and in predictions of ambient [M-f] revealed that the best results were obtained by the direct approach. Linear regression of transformed data yielded the largest bias and greatest variability, while non-linear isotherm fitting generated results with mean bias comparable to direct modeling, but also with greater variability. Participants that performed a unified analysis of ACSV titration curves at multiple detection windows for a sample improved their results regardless of the basic mathematical approach taken. Overall, the three most accurate sets of results were obtained using direct modeling of the unified multiwindow dataset, while the single most accurate set of results also included simultaneous calibration. We therefore recommend that where sample volume and time permit, titration experiments for all natural water samples be designed to include two or more detection windows, especially for coastal and estuarine waters. It is vital that more practical experimental designs for multi-window titrations be developed. Finally, while all mathematical approaches proved to be adequate for some datasets, matrix-based equilibrium models proved to be most naturally suited for the most challenging cases encountered in this work, i.e., experiments where the added ligand in ACSV became titrated. The ProMCC program (Omanovic et al., this issue) as well as the Excel Add-in based KINETEQL Multiwindow Solver spreadsheet (Hudson, 2014) have this capability and have been made available for public use as a result of this intercomparison exercise. (C) 2015 The Authors. Published by Elsevier B.V.

Hopkinson, BM, Mitchell G, Reynolds RA, Wang H, Selph KE, Measures CI, Hewes CD, Holm-Hansen O, Barbeau KA.  2007.  Iron limitation across chlorophyll gradients in the southern Drake Passage: Phytoplankton responses to iron addition and photosynthetic indicators of iron stress. Limnology and Oceanography. 52:2540-2554.   10.4319/lo.2007.52.6.2540   AbstractWebsite

Processes influencing phytoplankton bloom development in the southern Drake Passage were studied using shipboard iron-enrichment incubations conducted across a surface chlorophyll gradient near the Antarctic Peninsula, in a region of water mass mixing. Iron incubation assays showed that Antarctic Circumpolar Current (ACC) waters were severely iron limited, while shelf waters with high ambient iron concentrations (1-2 nmol L-1) were iron replete, demonstrating that mixing of the two water masses is a plausible mechanism for generation of the high phytoplankton biomass observed downstream of the Antarctic Peninsula. In downstream high-chlorophyll mixed waters, phytoplankton growth rates were also iron limited, although responses to iron addition were generally more moderate as compared to ACC waters. Synthesizing results from all experiments, significant correlations were found between the initial measurements of Photosystem II (PSII) parameters (F-v: F-m, sigma(PSII), and p) and the subsequent responses of these waters to iron addition. These correlations indicate that PSII parameters can be used to assess the degree of iron stress experienced in these waters and likely in other regions where photoinhibition and nitrogen stress are not confounding factors.

Hopkinson, BM, Barbeau KA.  2012.  Iron transporters in marine prokaryotic genomes and metagenomes. Environmental Microbiology. 14:114-128.   10.1111/j.1462-2920.2011.02539.x   AbstractWebsite

In the pelagic environment, iron is a scarce but essential micronutrient. The iron acquisition capabilities of selected marine bacteria have been investigated, but the recent proliferation of marine prokaryotic genomes and metagenomes offers a more comprehensive picture of microbial iron uptake pathways in the ocean. Searching these data sets, we were able to identify uptake mechanisms for Fe3+, Fe2+ and iron chelates (e.g. siderophore and haem iron complexes). Transport of iron chelates is accomplished by TonB-dependent transporters (TBDTs). After clustering the TBDTs from marine prokaryotic genomes, we identified TBDT clusters for the transport of hydroxamate and catecholate siderophore iron complexes and haem using gene neighbourhood analysis and co-clustering of TBDTs of known function. The genomes also contained two classes of siderophore biosynthesis genes: NRPS (non-ribosomal peptide synthase) genes and NIS (NRPS Independent Siderophore) genes. The most common iron transporters, in both the genomes and metagenomes, were Fe3+ ABC transporters. Iron uptake-related TBDTs and siderophore biosynthesis genes were less common in pelagic marine metagenomes relative to the genomic data set, in part because Pelagibacter ubique and Prochlorococcus species, which almost entirely lacked these Fe uptake systems, dominate the metagenomes. Our results are largely consistent with current knowledge of iron speciation in the ocean, but suggest that in certain niches the ability to acquire siderophores and/or haem iron chelates is beneficial.

Bundy, RM, Abdulla HAN, Hatcher PG, Biller DV, Buck KN, Barbeau KA.  2015.  Iron-binding ligands and humic substances in the San Francisco Bay estuary and estuarine-influenced shelf regions of coastal California. Marine Chemistry. 173:183-194.   10.1016/j.marchem.2014.11.005   AbstractWebsite

Dissolved iron (dFe) and organic dFe-binding ligands were determined in San Francisco Bay, California by competitive ligand exchange adsorptive cathodic stripping voltammetry (CLE-ACSV) along a salinity gradient from the freshwater endmember of the Sacramento River (salinity <2) to the mouth of the estuary (salinity >26). A range of dFe-binding ligand classes was simultaneously determined using multiple analytical window analysis, involving titrations with multiple concentrations of the added ligand,salicylaldoxime. The highest dFe and ligand concentrations were determined in the low salinity end of the estuary, with dFe equal to 131.5 nmol L-1 and strong ligand (log K-Fel, Fe'(cond) >= 12.0) concentrations equal to 139.5 nmol L-1. The weakest ligands (log K-Fel, Fe'(cond) < 10.0) were always in excess of dFe in low salinity waters, but were rapidly flocculated within the estuary and were not detected at salinities greater than 7. The strongest ligands (log K-Fel, Fe'(cond) > 11.0) were tightly coupled to dFe throughout the estuary, with average excess ligand concentrations ([L]-[dFe]) equal to 0.5 nmol L-1. Humic-like substances analyzed via both CLE-ACSV and proton nuclear magnetic resonance in several samples were found to be a significant portion of the dFe-binding ligand pool in San Francisco Bay, with concentrations ranging from 559.5 mu g L-1 to 67.5 mu g L-1 in the lowest and highest salinity samples, respectively. DFe-binding ligands and humic-like substances were also found in benthic boundary layer samples taken from the shelf near the mouths of San Francisco Bay and Eel River, suggesting estuaries are an important source of dFe-binding ligands to California coastal shelf waters. (C) 2014 Elsevier B.V. All rights reserved.

Hopkinson, BM, Barbeau KA.  2007.  Organic and redox speciation of iron in the eastern tropical North Pacific suboxic zone. Marine Chemistry. 106:2-17.   10.1016/j.marchem.2006.02.008   AbstractWebsite

The organic and redox speciation of iron was examined in the strongly layered upper water column of the eastern tropical North Pacific, including oxic and sub oxic waters, in a region 100- 1300 km offshore. Suboxic conditions ([O-2] < 5 mu M) were found to affect the organic speciation of iron, and reduced dissolved iron, Fc(II), was present in the suboxic zone, but conditions were not sufficiently reducing to convert all iron to Fe(II). Dissolved iron concentrations in the suboxic zone were similar to concentrations found in oxic regions. Using a competitive ligand exchange-adsorptive cathodic stripping voltammetry (CLE-ACSV) method, natural ligands were found to have distinct characteristics in the oxic and suboxic waters with stronger ligands found in the suboxic zone. It is unusual to find stronger ligands below the euphotic zone, but their strength, logK(Fe'L) = 12.1-12.8, is within the range determined for surface ligands in other regions. These strong ligands may be the result of the unique chemistry of the suboxic zone stabilizing reduced or labile compounds, or they may be actively produced by microbes to enhance iron uptake. No onshore-offshore trends in ligand strength or concentration were detected suggesting the ligands may result from the inherent chemistry of the suboxic zone or production from denitrifiers, rather than the resident suboxic zone population of Prochlorococcus which were more abundant nearshore. A luminol-chemiluminescence based flow injection analysis (FIA) technique capable of detecting picomolar concentrations of Fe(II) was used to assess the redox state of iron in the suboxic zone and overlying oxic waters at a station 1300 km offshore. An elevated signal equivalent to 0.12-0.15 nM Fe(II), 21-24% of dissolved iron, was found only in the suboxic waters. Oxidation kinetics suggest that this Fe(II) is most likely produced by an in-situ process, as opposed to being transported from shelf sediment. The luminol-chemiluminescence Fe(II) method was systematically tested for inferences from reduced species potentially present in the suboxic zone to validate our Fe(II) results. Several species, V(IV) and V(111), produced significant signals, but considerations of the reducing state of the suboxic zone make it unlikely that reduced V is present. With additional information on the identity of the suboxic zone species provided by analysis of signal decay rate, it was determined that Fe(II) was the most reasonable source of the signal, and at minimum the chemiluminescence data allows us to set limits on the Fe(II) concentration in the offshore suboxic water column. (C) 2006 Elsevier B.V. All rights reserved.

Hogle, SL, Dupont CL, Hopkinson BM, King AL, Buck KN, Roe KL, Stuart RK, Allen AE, Mann EL, Johnson ZI, Barbeau KA.  2018.  Pervasive iron limitation at subsurface chlorophyll maxima of the California Current. Proceedings of the National Academy of Sciences of the United States of America. 115:13300-13305.   10.1073/pnas.1813192115   AbstractWebsite

Subsurface chlorophyll maximum layers (SCMLs) are nearly ubiquitous in stratified water columns and exist at horizontal scales ranging from the submesoscale to the extent of oligotrophic gyres. These layers of heightened chlorophyll and/or phytoplankton concentrations are generally thought to be a consequence of a balance between light energy from above and a limiting nutrient flux from below, typically nitrate (NO3). Here we present multiple lines of evidence demonstrating that iron (Fe) limits or with light colimits phytoplankton communities in SCMLs along a primary productivity gradient from coastal to oligotrophic offshore waters in the southern California Current ecosystem. SCML phytoplankton responded markedly to added Fe or Fe/light in experimental incubations and transcripts of diatom and picoeukaryote Fe stress genes were strikingly abundant in SCML metatranscriptomes. Using a biogeochemical proxy with data from a 40-y time series, we find that diatoms growing in California Current SCMLs are persistently Fe deficient during the spring and summer growing season. We also find that the spatial extent of Fe deficiency within California Current SCMLs has significantly increased over the last 25 y in line with a regional climate index. Finally, we show that diatom Fe deficiency may be common in the subsurface of major upwelling zones worldwide. Our results have important implications for our understanding of the biogeochemical consequences of marine SCML formation and maintenance.

Hopkinson, BM, Seegers B, Hatta M, Measures CI, Mitchell BG, Barbeau KA.  2013.  Planktonic C:Fe ratios and carrying capacity in the southern Drake Passage. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 90:102-111.   10.1016/j.dsr2.2012.09.001   AbstractWebsite

The carbon to iron (C:Fe) ratio of planktonic biomass constrains net production in iron-limited regions of the ocean and is an important parameter for predicting biomass production from iron inputs. On a cruise to the southern Drake Passage in July-August 2006, we used two approaches to determine the C:Fe ratio of planktonic material: dual-radiotracer labeling and net biomass production in iron-limited grow-out experiments. There was variability in C:Fe ratios among experiments, but values from the two methods overlapped with average values of 1.4 x 10(5) (mol:mol) for the radiotracer method and 1.7 x 10(5) for the net biomass production method. This is notable since the net biomass production method is a new approach to determine C:Fe ratios. Although it has potential issues related to bottle effects and sensitivity to trace contamination, the method avoids some of the questions associated with iron speciation and bioavailability since ambient iron supports production. Because light intensity is known to affect C:Fe ratios in phytoplankton through photosynthetic iron demands, we tested the effect of light level on C:Fe in Antarctic assemblages. In contrast to what is seen in many phytoplankton cultures, C:Fe ratios increased at low-light, but we suspect that this is due to initial photoinhibition of the low-light adapted winter assemblages at higher light levels. (c) 2012 Elsevier Ltd. All rights reserved.

Boiteau, RM, Till CP, Ruacho A, Bundy RM, Hawco NJ, McKenna AM, Barbeau KA, Bruland KW, Saito MA, Repeta DJ.  2016.  Structural characterization of natural nickel and copper binding ligands along the US GEOTRACES Eastern Pacific Zonal Transect. Frontiers in Marine Science. 3:243.   10.3389/fmars.2016.00243   Abstract

Organic ligands form strong complexes with many trace elements in seawater. Various metals can compete for the same ligand chelation sites, and the final speciation of bound metals is determined by relative binding affinities, concentrations of binding sites, uncomplexed metal concentrations, and association/dissociation kinetics. Different ligands have a wide range of metal affinities and specificities. However, the chemical composition of these ligands in the marine environment remains poorly constrained, which has hindered progress in modeling marine metal speciation. In this study, we detected and characterized natural ligands that bind copper (Cu) and nickel (Ni) in the eastern South Pacific Ocean with liquid chromatography tandem inductively coupled plasma mass spectrometry (LC-ICPMS), and high resolution electrospray ionization mass spectrometry (ESIMS). Dissolved Cu, Ni, and ligand concentrations were highest near the coast. Chromatographically unresolved polar compounds dominated ligands isolated near the coast by solid phase extraction. Offshore, metal and ligand concentrations decreased, but several new ligands appeared. One major ligand was detected that bound both Cu2+ and Ni2+. Based on accurate mass and fragmentation measurements, this compound has a molecular formula of [C20H21N4O8S2 + M]+ (M = metal isotope) and contains several azole-like metal binding groups. Additional lipophilic Ni complexes were also present only in oligotrophic waters, with masses of 649, 698, and 712 m/z (corresponding to the 58Ni metal complex). Molecular formulae of [C32H54N3O6S2Ni]+ and [C33H56N3O6S2Ni]+ were determined for two of these compounds. Addition of Cu and Ni to the samples also revealed the presence of additional compounds that can bind both Ni and Cu. Although these specific compounds represent a small fraction of the total dissolved Cu and Ni pool, they highlight the compositional diversity and spatial heterogeneity of marine Ni and Cu ligands, as well as variability in the extent to which different metals in the same environment compete for ligand binding.

Hogle, SL, Thrash JC, Dupont CL, Barbeau KA.  2016.  Trace metal acquisition by marine heterotrophic bacterioplankton with contrasting trophic strategies. Applied and Environmental Microbiology. 82:1613-1624.   10.1128/aem.03128-15   AbstractWebsite

Heterotrophic bacteria in the SAR11 and Roseobacter lineages shape the marine carbon, nitrogen, phosphorous, and sulfur cycles, yet they do so having adopted divergent ecological strategies. Currently, it is unknown whether these globally significant groups partition into specific niches with respect to micronutrients (e.g., trace metals) and how that may affect marine trace metal cycling. Here, we used comparative genomics to identify diverse iron, cobalt, nickel, copper, and zinc uptake capabilities in SAR11 and Roseobacter genomes and uncover surprising unevenness within and between lineages. The strongest predictors for the extent of the metal uptake gene content are the total number of transporters per genome, genome size, total metal transporters, and GC content, but numerous exceptions exist in both groups. Taken together, our results suggest that SAR11 have strongly minimized their trace metal uptake versatility, with high-affinity zinc uptake being a unique exception. The larger Roseobacter genomes have greater trace metal uptake versatility on average, but they also appear to have greater plasticity, resulting in phylogenetically similar genomes having largely different capabilities. Ultimately, phylogeny is predictive of the diversity and extent of 20 to 33% of all metal uptake systems, suggesting that specialization in metal utilization mostly occurred independently from overall lineage diversification in both SAR11 and Roseobacter. We interpret these results as reflecting relatively recent trace metal niche partitioning in both lineages, suggesting that concentrations and chemical forms of metals in the marine environment are important factors shaping the gene content of marine heterotrophic Alphaproteobacteria of the SAR11 and Roseobacter lineages.

Roe, KL, Hogle SL, Barbeau KA.  2013.  Utilization of heme as an iron source by marine alphaproteobacteria in the roseobacter clade. Applied and Environmental Microbiology. 79:5753-5762.   10.1128/aem.01562-13   AbstractWebsite

The bioavailability and utilization of porphyrin-bound iron, specifically heme, by marine microorganisms have rarely been examined. This study used Ruegeria sp. strain TrichCH4B as a model organism to study heme acquisition by a member of the Roseobacter clade. Analogs of known heme transporter proteins were found within the Ruegeria sp. TrichCH4B genome. The identified heme uptake and utilization system appears to be functional, as the heme genes were upregulated under iron stress, the bacterium could grow on ferric-porphyrin complexes as the sole iron source, and internalization of(55) Fe from ferric protoporphyrin IX was observed. The potential ability to utilize heme in the Roseobacter clade appears to be common, as half of the isolates in the RoseoBase database were found to have a complete heme uptake system. A degenerate primer set was designed and successfully used to identify the putative heme oxygenase gene (hmus) in the roseobacter heme uptake system from diverse nonenriched marine environments. This study found that members of the Roseobacter clade are capable of utilizing heme as an iron source and that this capability may be present in all types of marine environments. The results of this study add a new perspective to the current picture of iron cycling in marine systems, whereby relatively refractory intracellular pools of heme-bound iron may be taken up quickly and directly reincorporated into living bacteria without previous degradation or the necessity of a siderophore intermediate.