The outer membrane of a heterocyst-forming cyanobacterium is a permeability barrier for uptake of metabolites that are exchanged between cells

Authors

  • Kerstin Nicolaisen,

    1. JWGU Frankfurt am Main, Center of Membrane Proteomics, Cluster of Excellence Macromolecular Complexes, Department of Biosciences, Molecular Cell Biology, Max-von-Laue Str. 9, 60439 Frankfurt, Germany.
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  • Vicente Mariscal,

    1. Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, Américo Vespucio 49, E-41092 Seville, Spain.
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  • Rolf Bredemeier,

    1. JWGU Frankfurt am Main, Center of Membrane Proteomics, Cluster of Excellence Macromolecular Complexes, Department of Biosciences, Molecular Cell Biology, Max-von-Laue Str. 9, 60439 Frankfurt, Germany.
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  • Rafael Pernil,

    1. Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, Américo Vespucio 49, E-41092 Seville, Spain.
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  • Sunčana Moslavac,

    1. JWGU Frankfurt am Main, Center of Membrane Proteomics, Cluster of Excellence Macromolecular Complexes, Department of Biosciences, Molecular Cell Biology, Max-von-Laue Str. 9, 60439 Frankfurt, Germany.
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  • Rocío López-Igual,

    1. Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, Américo Vespucio 49, E-41092 Seville, Spain.
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  • Iris Maldener,

    1. Microbiology and Organismic Interactions, Department of Biology at University Tübingen, 72076 Tübingen, Germany.
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  • Antonia Herrero,

    1. Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, Américo Vespucio 49, E-41092 Seville, Spain.
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  • Enrico Schleiff,

    Corresponding author
    1. JWGU Frankfurt am Main, Center of Membrane Proteomics, Cluster of Excellence Macromolecular Complexes, Department of Biosciences, Molecular Cell Biology, Max-von-Laue Str. 9, 60439 Frankfurt, Germany.
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  • Enrique Flores

    Corresponding author
    1. Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, Américo Vespucio 49, E-41092 Seville, Spain.
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*E-mail schleiff@bio.uni-frankfurt.de; Tel. (+49) 69 79829285; Fax (+49) 69 79829286;

**E-mail eflores@ibvf.csic.es; Tel. (+34) 95 4489523; Fax (+34) 95 4460065.

Summary

The multicellular Anabaena sp. strain PCC 7120 is a filamentous cyanobacterium that can fix N2 in differentiated cells called heterocysts, which exchange nutritional and regulatory compounds with the neighbour photosynthetic vegetative cells. The outer membrane of this bacterium is continuous along the filament defining a continuous periplasmic space. The Anabaena alr0075, alr2269 and alr4893 gene products were characterized as Omp85-like proteins, which are generally involved in outer membrane protein biogenesis. Open reading frame alr2269 is the first gene of an operon that also carries genes for lipopolysaccharide lipid A biosynthesis including alr2270 (an lpxC homologue). Strains carrying inactivating alr2269 or alr2270 constructs showed enhanced sensitivity to erythromycin, SDS, lysozyme and proteinase K suggesting that they produce an outer membrane with increased permeability. These strains further exhibited increased uptake of sucrose, glutamate and, to a lesser extent, a few other amino acids. Increased uptake of the same metabolites was obtained by mechanical fragmentation of wild-type Anabaena filaments. These results document that the outer membrane is a permeability barrier for metabolites such as sucrose and glutamate, which are subjected to intercellular exchange in the diazotrophic filament of heterocyst-forming cyanobacteria.

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