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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


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.

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.

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.

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.

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.  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.

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.

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.  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.

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.