Structural and functional characterization of IdiA/FutA (Tery_3377), an iron-binding protein from the ocean diazotroph Trichodesmium erythraeum

Polyviou, Despo; Machelett, M.M.; Hitchcock, Andrew; Baylay, Alison J.; MacMillan, Fraser; Moore, C. Mark; Bibby, Thomas S.; Tews, Ivo

doi:10.1074/jbc.ra118.001929

Cited by 21 publications

(25 citation statements)

References 63 publications

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“…3b–d), and possibly hint at specificity in the uptake systems. This observation is supported by studies showing that Trichodesmium indeed has proteins capable of siderophore transport 33 . Interestingly, siderophore additions enhanced Fe-uptake in natural Trichodesmium to a greater extent than for associated bacteria (Fig.…”

Section: Resultsmentioning

confidence: 64%

Colonies of marine cyanobacteria Trichodesmium interact with associated bacteria to acquire iron from dust

et al. 2019

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Iron (Fe) bioavailability limits phytoplankton growth in vast ocean regions. Iron-rich dust uplifted from deserts is transported in the atmosphere and deposited on the ocean surface. However, this dust is a poor source of iron for most phytoplankton since dust-bound Fe is poorly soluble in seawater and dust rapidly sinks out of the photic zone. An exception is Trichodesmium , a globally important, N 2 fixing, colony forming, cyanobacterium, which efficiently captures and shuffles dust to its colony core. Trichodesmium and bacteria that reside within its colonies carry out diverse metabolic interactions. Here we show evidence for mutualistic interactions between Trichodesmium and associated bacteria for utilization of iron from dust, where bacteria promote dust dissolution by producing Fe-complexing molecules (siderophores) and Trichodesmium provides dust and optimal physical settings for dissolution and uptake. Our results demonstrate how intricate relationships between producers and consumers can influence productivity in the nutrient starved open ocean.

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Section: Resultsmentioning

confidence: 64%

Colonies of marine cyanobacteria Trichodesmium interact with associated bacteria to acquire iron from dust

et al. 2019

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“…These siderophores have been shown to solubilize iron from its mineral state in dust and to make it available to Trichodesmium cells (Basu et al, 2019). It is not known whether Trichodesmium takes up siderophores by a reductive or nonreductive mechanism, but the cells may contain proteins capable of siderophore transport (Polyviou et al, 2018). Interactions of this type are typically mutualistic, with the heterotrophic bacteria facilitating Trichodesmium iron acquisition and Trichodesmium colonies providing the carbon and nitrogen substrate for bacterial colonization in the form of exudates (Basu et al, 2019).…”

Section: Trichodesmium and The Use Of Iron From Dustmentioning

confidence: 99%

Iron Uptake Mechanisms in Marine Phytoplankton

2020

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Oceanic phytoplankton species have highly efficient mechanisms of iron acquisition, as they can take up iron from environments in which it is present at subnanomolar concentrations. In eukaryotes, three main models were proposed for iron transport into the cells by first studying the kinetics of iron uptake in different algal species and then, more recently, by using modern biological techniques on the model diatom Phaeodactylum tricornutum. In the first model, the rate of uptake is dependent on the concentration of unchelated Fe species, and is thus limited thermodynamically. Iron is transported by endocytosis after carbonate-dependent binding of Fe(III)' (inorganic soluble ferric species) to phytotransferrin at the cell surface. In this strategy the cells are able to take up iron from very low iron concentration. In an alternative model, kinetically limited for iron acquisition, the extracellular reduction of all iron species (including Fe') is a prerequisite for iron acquisition. This strategy allows the cells to take up iron from a great variety of ferric species. In a third model, hydroxamate siderophores can be transported by endocytosis (dependent on ISIP1) after binding to the FBP1 protein, and iron is released from the siderophores by FRE2-dependent reduction. In prokaryotes, one mechanism of iron uptake is based on the use of siderophores excreted by the cells. Iron-loaded siderophores are transported across the cell outer membrane via a TonB-dependent transporter (TBDT), and are then transported into the cells by an ABC transporter. Open ocean cyanobacteria do not excrete siderophores but can probably use siderophores produced by other organisms. In an alternative model, inorganic ferric species are transported through the outer membrane by TBDT or by porins, and are taken up by the ABC transporter system FutABC. Alternatively, ferric iron of the periplasmic space can be reduced by the alternative respiratory terminal oxidase (ARTO) and the ferrous ions can be transported by divalent metal transporters (FeoB or ZIP). After reoxidation, iron can be taken up by the high-affinity permease Ftr1.

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“…the FeoB system (Fe(II)), the IdiA system (Fe(III)), and uptake via Fe-siderophores 8,21 . The single colony metaproteomes provided evidence for the latter two mechanisms; FeoB is rarely identified in metaproteomes of diazotrophs, possibly due to its low copy number/high efficiency ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Mechanisms and heterogeneity of mineral use by natural colonies of the cyanobacteriumTrichodesmium

Held

Sutherland

Webb

et al. 2020

Preprint

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The keystone marine nitrogen fixer Trichodesmium thrives in high dust environments, and while experimental observations suggest that Trichodesmium colonies can access the essential nutrient iron from dust particles, it is not known the extent to which this occurs in the field. Here we demonstrate that Trichodesmium colonies actively process mineral particles in nature with direct molecular impacts. Microscopy and synchrotron-based imaging demonstrated heterogeneous associations with particles consistent with iron oxide and iron silicate minerals. Metaproteomic analysis of individual colonies revealed enrichment of biogeochemically-relevant proteins including photosynthesis proteins and metalloproteins containing iron, nickel, copper and zinc when particles were present. The iron-storage protein ferritin was particularly enriched implying accumulation of particle-derived iron, and multiple iron acquisition pathways including Fe(II), Fe(III), and Fe-siderophore transporters were engaged, including evidence of superoxide-driven particle dissolution. While the particles clearly provided iron, there was also evidence that the concentrated metals had toxic effects. The molecular mechanisms allowing Trichodesmium to interact with particulate minerals are fundamental to its success and global impact on nitrogen biogeochemistry, and may contribute to the leaching of particulate trace metals with implications for global iron and carbon cycling.

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Structural and functional characterization of IdiA/FutA (Tery_3377), an iron-binding protein from the ocean diazotroph Trichodesmium erythraeum

Cited by 21 publications

References 63 publications

Colonies of marine cyanobacteria Trichodesmium interact with associated bacteria to acquire iron from dust

Colonies of marine cyanobacteria Trichodesmium interact with associated bacteria to acquire iron from dust

Iron Uptake Mechanisms in Marine Phytoplankton

Mechanisms and heterogeneity of mineral use by natural colonies of the cyanobacteriumTrichodesmium

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