Identification of an iron permease, cFTR1, in cyanobacteria involved in the iron reduction/re‐oxidation uptake pathway

Xu, Ning; Qiu, Guo-Wei; Lou, Wenjing; Li, Zheng‐Ke; Jiang, Haibo; Price, Neil M.; Qiu, Bao‐Sheng

doi:10.1111/1462-2920.13464

Cited by 16 publications

(27 citation statements)

References 44 publications

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“…However, these commonalities weakened at genus level, with respective metal‐related microbes. Previous research suggests that Synechococcus tolerates copper (Stuart et al, ), Exiguobacterium and Cyanobacteria reduce Cr (VI) and Fe (III) (Mohapatra et al, ; Xu et al, ). These bacteria were also present in our surface water and sediment samples.…”

Section: Discussionmentioning

confidence: 99%

Microbial Community Responses to Vanadium Distributions in Mining Geological Environments and Bioremediation Assessment

et al. 2019

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Vanadium mining activities can cause contamination of the surrounding geological environment. Vanadium may exist in multiple matrices due to its migration and transformation, forming interactive relationships; however, the connection between vanadium distributions in multiple matrices and microbial community responses remains largely unknown. Vanadium is a redox‐sensitive metal that can be microbiologically reduced and immobilized. To date, bioremediation of vanadium‐contaminated environments by indigenous microorganisms has rarely been evaluated. This paper reports a systematic investigation into vanadium distributions and microbial communities in soils, water, and sediment from Panzhihua, China. Large vanadium contents of 1130.1 ± 9.8 mg/kg and 0.13 ± 0.02 mg/L were found in surface soil and groundwater. Vanadium in surface water tended to precipitate. Microbial communities isolated from similar environments were alike due to similarity in matrix chemistry whereas communities were distinct when compared to different matrices, with lower richness and diversity in groundwater. Proteobacteria was distributed widely and dominated microbial communities within groundwater. Redundancy analysis shows that vanadium and nutrients significantly affected metal‐tolerant bacteria. Long‐term cultivation (240 days) suggests the possibility of vanadium bioremediation by indigenous microorganisms, within acid‐soluble fraction. This active fraction can potentially release mobile vanadium with shifted redox conditions. Vanadium (V) was bio‐reduced to less toxic, mobile vanadium (IV) primarily by enriched Bacillus and Thauera. This study reveals the biogeochemical fate of vanadium in regional geological environments and suggests a bioremediation pathway via native vanadium‐reducing microbes.

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Section: Discussionmentioning

confidence: 99%

Microbial Community Responses to Vanadium Distributions in Mining Geological Environments and Bioremediation Assessment

et al. 2019

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“…This implies that iron must be reduced before uptake, as in the eukaryotic yeast and Chlamydomonas models. It has been suggested that this reductive iron uptake strategy operates in many cyanobacteria (Kranzler et al, 2011(Kranzler et al, , 2013(Kranzler et al, , 2014Lis et al, 2015a;Rudolf et al, 2015;Xu et al, 2016;Eichner et al, 2019). The outer membrane has no obvious redox activity.…”

Section: Reductive Iron Uptake and Uptake Of Inorganic Ferric Speciesmentioning

confidence: 99%

“…ARTO has been shown to be expressed and upregulated in response to lower iron availability in Trichodesmium (Polyviou et al, 2017). In some cases, iron may be re-oxidized by oxygen and transported through the inner membrane by an FTR1 (cFTR1) permease similar to that found in yeast (Xu et al, 2016). Ferrous iron would then be transported into the cell by the FeoB protein and/or by divalent metal ion transporters (NRAMP or ZIP transporters for picocyanobacteria) (Hopkinson and Barbeau, 2012).…”

Section: Reductive Iron Uptake and Uptake Of Inorganic Ferric Speciesmentioning

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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“…Cells were grown under Fe-replete or Fe-depleted conditions for 4 days prior and then collected and frozen in liquid nitrogen. The excitation wavelength was set at 430 nm, and the resulting spectra were normalized to the intensity at 720 nm, as previously described (37).…”

Section: Methodsmentioning

confidence: 99%

“…Still, many cyanobacteria do not produce siderophores and/or lack siderophore transport capabilities, suggesting that alternative acquisition strategies are in play (32). One such example is that some cyanobacteria use a reductive uptake strategy and reduce Fe(III) to Fe(II) in the periplasmic space via a CM redox system, followed by transport across the CM facilitated by specific transporters (35)(36)(37). Several studies have suggested that some cyanobacteria may be able to combine multiple Fe uptake strategies to increase their access to various Fe substrates (e.g., Fe-organic ligand complexes including siderophores and Fe=), a key capability necessary to thrive in Fe-limited environments (24,35).…”

mentioning

confidence: 99%

Outer Membrane Iron Uptake Pathways in the Model Cyanobacterium Synechocystis sp. Strain PCC 6803

Qiu

Lou

Sun

et al. 2018

Appl Environ Microbiol

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Cyanobacteria are foundational drivers of global nutrient cycling, with high intracellular iron (Fe) requirements. Fe is found at extremely low concentrations in aquatic systems, however, and the ways in which cyanobacteria take up Fe are largely unknown, especially the initial step in Fe transport across the outer membrane. Here, we identified one TonB protein and four TonB-dependent transporters (TBDTs) of the energy-requiring Fe acquisition system and six porins of the passive diffusion Fe uptake system in the model cyanobacterium sp. strain PCC 6803. The results experimentally demonstrated that TBDTs not only participated in organic ferri-siderophore uptake but also in inorganic free Fe (Fe') acquisition.Fe uptake rate measurements showed that a TBDT quadruple mutant acquired Fe at a lower rate than the wild type and lost nearly all ability to take up ferri-siderophores, indicating that TBDTs are critical for siderophore uptake. However, the mutant retained the ability to take up Fe' at 42% of the wild-type Fe' uptake rate, suggesting additional pathways of Fe' acquisition besides TBDTs, likely by porins. Mutations in four of the six porin-encoding genes produced a low-Fe-sensitive phenotype, while a mutation in all six genes was lethal to cell survival. These diverse outer membrane Fe uptake pathways reflect cyanobacterial evolution and adaptation under a range of Fe regimes across aquatic systems. Cyanobacteria are globally important primary producers and contribute about 25% of global CO fixation. Low Fe bioavailability in surface waters is thought to limit the primary productivity in as much as 40% of the global ocean. The Fe acquisition strategies that cyanobacteria have evolved to overcome Fe deficiency remain poorly characterized. We experimentally characterized the key players and the cooperative work mode of two Fe uptake pathways, including an active uptake pathway and a passive diffusion pathway in the model cyanobacterium sp. PCC 6803. Our finding proved that cyanobacteria use ferri-siderophore transporters to take up Fe', and they shed light on the adaptive mechanisms of cyanobacteria to cope with widespread Fe deficiency across aquatic environments.

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Identification of an iron permease, cFTR1, in cyanobacteria involved in the iron reduction/re‐oxidation uptake pathway

Cited by 16 publications

References 44 publications

Microbial Community Responses to Vanadium Distributions in Mining Geological Environments and Bioremediation Assessment

Microbial Community Responses to Vanadium Distributions in Mining Geological Environments and Bioremediation Assessment

Iron Uptake Mechanisms in Marine Phytoplankton

Outer Membrane Iron Uptake Pathways in the Model Cyanobacterium Synechocystis sp. Strain PCC 6803

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