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Semeniuk, DM, Bundy RM, Payne CD, Barbeau KA, Maldonado MT.  2015.  Acquisition of organically complexed copper by marine phytoplankton and bacteria in the northeast subarctic Pacific Ocean. Marine Chemistry. 173:222-233.   10.1016/j.marchem.2015.01.005   AbstractWebsite

Copper (Cu) is an essential micronutrient for marine phytoplankton, but can cause toxicity at elevated intracellular concentrations. The majority of Cu (>99.9%) in oceanic surface waters is bound to strong organic ligands, presumably produced by prokaryotes to detoxify Cu. Although laboratory studies have demonstrated that organically complexed Cu may be bioavailable to marine eukaryotic phytoplankton, the bioavailability of Cu organic complexes to indigenous marine phytoplankton has not been examined in detail. Using the carrier free radioisotope Cu-67 at an iron limited station in the northeast subarctic Pacific Ocean, we performed size fractionated short-term Cu uptake assays with three Cu(II)-chelates, and Cu-67 bound to the strong in situ ligands, with or without additions of weak Cu(I) ligands. Estimates of the maximum supply of inorganic Cu (Cu') to the cell surface of eukaryotic phytoplankton were unable to account for the observed Cu uptake rates from the in situ ligands and two of the three added Cu(II)-chelates. Addition of 10 nM weak organic Cu(I) ligands enhanced uptake of Cu bound to the in situ ligands. Thus, Cu within the in situ and strong artificial Cu(II) organic ligands was accessible to the phytoplankton community via various possible Cu uptake strategies, including; cell surface enzymatically mediated reduction of Cu(II) to Cu(I), the substrate of the high-affinity Cu transport system in eukaryotes; or ligand exchange between weak Cu-binding ligands and the cellular Cu transporters. During a 14-hour uptake assay, particulate Cu concentrations reached a plateau in most treatments. Losses were observed in some treatments, especially in the small size fractions (<5 mu m), corresponding with faster initial Cu uptake rates. This may indicate that Cu cycling is rapid between particulate and dissolved phases due to cellular efflux or remineralization by micrograzers. The acquisition of Cu from the strong in situ ligands puts into question the historic role attributed to Cu binding ligands in decreasing Cu bioavailability. (C) 2015 Elsevier B.V. All rights reserved.

H
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.