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

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Abstract

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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Acknowledgments

This work was supported by the Deutsche Forschungsgemeinschaft (SCHL 585-6) to ES and by an Israeli Science Foundation grant (806/11) awarded to NK.

Author contributions

ES designed research; MR performed uptake experiments and mutant analysis; MR, MS and RP performed qRT-PCR; ES, MR, RP and NK analysed data; ES and MR wrote the manuscript; all authors were involved in final editing and all approved the manuscript.

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Authors and Affiliations

  1. Institute for Molecular Biosciences, Goethe University Frankfurt, Max von Laue Str. 9, 60438, Frankfurt, Germany

    Mareike Rudolf, Mara Stevanovic, Rafael Pernil & Enrico Schleiff

  2. Department of Plant and Environmental Science, The Alexander Silberman Institute of Life Sciences, The Hebrew University in Jerusalem, Jerusalem, Israel

    Chana Kranzler & Nir Keren

  3. Cluster of Excellence Macromolecular Complexes, Goethe University Frankfurt, 60438, Frankfurt, Germany

    Enrico Schleiff

  4. Buchman Institute for Molecular Life Sciences, Goethe University Frankfurt, Max von Laue Str. 9, N200/3.02, 60438, Frankfurt, Germany

    Enrico Schleiff

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  1. Mareike Rudolf
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  2. Mara Stevanovic
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  3. Chana Kranzler
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  4. Rafael Pernil
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  5. Nir Keren
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Correspondence to Enrico Schleiff.

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Rudolf, M., Stevanovic, M., Kranzler, C. et al. Multiplicity and specificity of siderophore uptake in the cyanobacterium Anabaena sp. PCC 7120. Plant Mol Biol 92, 57–69 (2016). https://doi.org/10.1007/s11103-016-0495-2

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