A Comparative Study of Iron Uptake Rates and Mechanisms amongst Marine and Fresh Water Cyanobacteria: Prevalence of Reductive Iron Uptake

Lis, Hagar; Kranzler, Chana; Keren, Nir; Shaked, Yeala

doi:10.3390/life5010841

Cited by 59 publications

(74 citation statements)

References 63 publications

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“…A). This resembles findings observed for Anabaena UTEX 2576 (Lis et al ., ), while in other cyanobacteria species, the complexed iron is reduced and released from the siderophore prior its assimilation into the cytoplasm (Kranzler et al ., ; Lis et al ., ). FeSchizokinen uptake increases when iron is limiting (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…It has been established that the iron uptake rate constant (k in ) of Fe′ uptake is higher than k in of ferric iron siderophore uptake throughout the phytoplankton kingdom (Lis et al ., 2014; 2015). This is in line with the higher uptake rate at 0.05 nM substrate concentration for Fe′ than for FeSchizokinen observed for moderately starved Anabaena sp.…”

Section: Discussionmentioning

confidence: 99%

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Multiple modes of iron uptake by the filamentous, siderophore‐producing cyanobacterium, Anabaena sp. PCC 7120

Rudolf

Kranzler

Lis

et al. 2015

Molecular Microbiology

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SummaryIron is a member of a small group of nutrients that limits aquatic primary production. Mechanisms for utilizing iron have to be efficient and adapted according to the ecological niche. In respect to iron acquisition cyanobacteria, prokaryotic oxygen evolving photosynthetic organisms can be divided into siderophore-and non-siderophore-producing strains. The results presented in this paper suggest that the situation is far more complex. To understand the bioavailability of different iron substrates and the advantages of various uptake strategies, we examined iron uptake mechanisms in the siderophore-producing cyanobacterium Anabaena sp. PCC 7120. Comparison of the uptake of iron complexed with exogenous (desferrioxamine B, DFB) or to self-secreted (schizokinen) siderophores by Anabaena sp. revealed that uptake of the endogenous produced siderophore complexed to iron is more efficient. In addition, Anabaena sp. is able to take up dissolved, ferric iron hydroxide species (Fe′) via a reductive mechanism. Thus, Anabaena sp. exhibits both, siderophore-and non-siderophore-mediated iron uptake. While assimilation of Fe′ and FeDFB are not induced by iron starvation, FeSchizokinen uptake rates increase with increasing iron starvation. Consequently, we suggest that Fe′ reduction and uptake is advantageous for low-density cultures, while at higher densities siderophore uptake is preferred.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Multiple modes of iron uptake by the filamentous, siderophore‐producing cyanobacterium, Anabaena sp. PCC 7120

Rudolf

Kranzler

Lis

et al. 2015

Molecular Microbiology

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“…[31][32][33] However, many cyanobacteria do not produce siderophores, therefore reductive mechanisms are being sought and evidence of possible reductive iron uptake pathways is growing. [34][35][36][37] New insight on cyanobacterial iron acquisition has revealed ferric reduction due to the action of the Alternate Respiratory Terminal Oxidase (ARTO) in the plasma membrane with the subsequent uptake of ferrous, particularly described for the model cyanobacterium Synechocystis sp. PCC6803, 34,38,39 a common strain used in biophotovoltaics.…”

Section: 29mentioning

confidence: 99%

Tapping into cyanobacteria electron transfer for higher exoelectrogenic activity by imposing iron limited growth

et al. 2018

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The exoelectrogenic capacity of the cyanobacterium Synechococcus elongatus PCC7942 was studied in iron limited growth in order to establish conditions favouring extracellular electron transfer in cyanobacteria for photo-bioelectricity generation. Investigation into extracellular reduction of ferricyanide by Synechococcus elongatus PCC7942 demonstrated enhanced capability for the iron limited conditions in comparison to the iron sufficient conditions. Furtheremore, the significance of pH showed that higher rates of ferricyanide reduction occurred at pH 7, with a 2.7-fold increase with respect to pH 9.5 for iron sufficient cultures and 24-fold increase for iron limited cultures. The strategy presented induced exoelectrogenesis driven mainly by photosynthesis and an estimated redirection of the 28% of electrons from photosynthetic activity was achieved by the iron limited conditions. In addition, ferricyanide reduction in the dark by iron limited cultures also presented a significant improvement, with a 6-fold increase in comparison to iron sufficient cultures. Synechococcus elongatus PCC7942 ferricyanide reduction rates are unprecedented for cyanobacteria and they are comparable to those of microalgae. The redox activity of biofilms directly on ITO-coated glass, in the absence of any artificial mediator, was also enhanced under the iron limited conditions, implying that iron limitation increased exoelectrogenesis at the outer membrane level. Cyclic voltammetry of Synechococcus elongatus PCC7942 biofilms on ITO-coated glass showed a midpoint potential around 0.22 V vs. Ag/ AgCl and iron limited biofilms had the capability to sustain currents in a saturated-like fashion. The present work proposes an iron related exoelectrogenic capacity of Synechococcus elongatus PCC7942 and sets a starting point for the study of this strain in order to improve photo-bioelectricity and darkbioelectricity generation by cyanobacteria, including more sustainable mediatorless systems.

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“…in a siderophore-independent manner, which involves a reduction step (Rudolf et al 2015). It is known that reductive iron uptake of both Fe′ and ferrisiderophores is used by several other cyanobacterial species to sequester iron (Kranzler et al 2011;Lis et al 2014Lis et al , 2015. The inner membrane Fe(II) transporter FeoB and the alternate respiratory terminal oxidase (ARTO) were suggested to be involved in this pathway .…”

Section: Introductionmentioning

confidence: 99%

Multiplicity and specificity of siderophore uptake in the cyanobacterium Anabaena sp. PCC 7120

et al. 2016

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Many cyanobacteria secrete siderophores to sequester iron. Alternatively, mechanisms to utilize xenosiderophores have evolved. The overall uptake systems are comparable to that of other bacteria involving outer membrane transporters energized by TonB as well as plasma membrane-localized transporters. However, the function of the bioinformatically-inferred components is largely not established and recent studies showed a high diversity of the complexity of the uptake systems in different cyanobacteria. Thus, we approached the systems of the filamentous Anabaena sp. PCC 7120 as a model of a siderophore-secreting cyanobacterium. Anabaena sp. produces schizokinen and uptake of Fe-schizokinen involves the TonB-dependent transporter, schizokinen transporter (SchT), and the ABC-type transport system FhuBCD. We confirm that this system is also relevant for the uptake of structurally similar Fe-siderophore complexes like Fe-aerobactin. Moreover, we demonstrate a function of the TonB-dependent transporter IutA2 in Fe-schizokinen uptake in addition to SchT. The iutA2 mutant shows growth defects upon iron limitation, alterations in Fe-schizokinen uptake and in the transcription profile of the Fe-schizokinen uptake system. The physiological properties of the mutant confirm the importance of iron uptake for cellular function, e.g. for the Krebs cycle. Based on the relative relation of expression of schT and iutA2 as well as of the iron uptake rate to the degree of starvation, a model for the need of the co-existence of two different outer membrane transporters for the same substrate is discussed.

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A Comparative Study of Iron Uptake Rates and Mechanisms amongst Marine and Fresh Water Cyanobacteria: Prevalence of Reductive Iron Uptake

Cited by 59 publications

References 63 publications

Multiple modes of iron uptake by the filamentous, siderophore‐producing cyanobacterium, Anabaena sp. PCC 7120

Multiple modes of iron uptake by the filamentous, siderophore‐producing cyanobacterium, Anabaena sp. PCC 7120

Tapping into cyanobacteria electron transfer for higher exoelectrogenic activity by imposing iron limited growth

Multiplicity and specificity of siderophore uptake in the cyanobacterium Anabaena sp. PCC 7120

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