A cobalt concentration sensitive Btu-like system facilitates cobalamin uptake in Anabaena sp. PCC 7120

Authors:

Julia Graf1, Leonard Fresenborg1,2, Hans-Michael Seitz2,3, Rafael Pernil1 and Enrico Schleiff1,2,4,5

Affiliations:

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

2 Frankfurt Isotope and Element Research Center, Goethe University Frankfurt, 60438 Frankfurt Germany.

3 Institute for Geoscience, Goethe University Frankfurt, Altenhöferallee 1, 60438 Frankfurt, Germany.

4 Frankfurt Institute for Advanced Studies, Ruth-Moufang-Straße 1, 60438 Frankfurt, Germany.

5 Buchmann Institute for Molecular Life Sciences, Max von Laue Str. 11, 60438 Frankfurt, Germany.

Keywords: 

cyanobacteria, cobalt, cobalamin, riboswitch, metal uptake, TonB-dependent transporter.

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Corresponding Author(s):

Conflict of interest statement:

The authors declare that they have no conflict of interests.

Please cite this article as:

Julia Graf, Leonard Fresenborg, Hans-Michael Seitz, Rafael Pernil and Enrico Schleiff (2024). A cobalt concentration sensi-tive Btu-like system facilitates cobalamin uptake in Anabaena sp. PCC 7120. Microbial Cell 11: 41-56. doi: 10.15698/mic2024.02.814

© 2024 Graf et al. This is an open-access article released under the terms of the Creative Commons Attribution (CC BY) license, which allows the unrestricted use, distribution, and reproduction in any medium, provided the original author and source are acknowledged.

Abstract:

Metal homeostasis is central to all forms of life, as metals are essential micronutrients with toxic effects at elevated levels. Macromolecular machines facilitate metal uptake into the cells and their intracellular level is regulated by multiple means, which can involve RNA elements and proteinaceous components. While the general principles and components for uptake and cellular content regulation of, e.g., cobalt have been identified for proteobacteria, the corresponding mechanism in other Gram-negative bacteria such as cyanobacteria remain to be established. Based on their photosynthetic activity, cyanobacteria are known to exhibit a special metal demand in comparison to other bacteria. Here, the regulation by cobalt and cobalamin as well as their uptake is described for Anabaena sp. PCC 7120, a model filamentous heterocyst-forming cyanobacterium. Anabaena contains at least three cobalamin riboswitches in its genome, for one of which the functionality is confirmed here. Moreover, two outer membrane-localized cobalamin TonB-dependent transporters, namely BtuB1 and BtuB2, were identified. BtuB2 is important for fast uptake of cobalamin under conditions with low external cobalt, whereas BtuB1 appears to function in cobalamin uptake under conditions of sufficient cobalt supply. While the general function is comparable, the specific function of the two genes differs and mutants thereof show distinct phenotypes. The uptake of cobalamin depends further on the TonB and a BtuFCD machinery, as mutants of tonB3 and btuD show reduced cobalamin uptake rates. Thus, our results provide novel information on the uptake of cobalamin and the regulation of the cellular cobalt content in cyanobacteria.

doi: 10.15698/mic2024.02.814
Volume 11, pp. 41 to 56, published 20/02/2024.

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