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Title: Cu Transport by the Extended Family of CcoA-like Transporters (CalT) in Proteobacteria

Abstract

Comparative genomic studies of the bacterial MFS-type copper importer CcoA, required for cbb3-type cytochrome c oxidase (cbb3-Cox) biogenesis, revealed a widespread CcoA-like transporters (CalT) family, containing the conserved CcoA Cu-binding MxxxM and HxxxM motifs. Surprisingly, this family also included the RfnT-like proteins, earlier suggested to transport riboflavin. However, presence of the Cu-binding motifs in these proteins raised the possibility that they might be Cu transporters. To test this hypothesis, the genomic context of the corresponding genes was examined, and three of such genes from Ochrobactrum anthropi, Rhodopseudomonas palustris and Agrobacterium tumefaciens were expressed in Escherichia coli (ΔribB) and Rhodobacter capsulatus (ΔccoA) mutants. Copper and riboflavin uptake abilities of these strains were compared with those expressing R. capsulatus CcoA and Rhizobium leguminosarum RibN as bona fide copper and riboflavin importers, respectively. Altogether data demonstrated that the “RfnT-like” CalT proteins are unable to efficiently transport riboflavin, but they import copper like CcoA. Nevertheless, even though expressed and membrane-localized in a R. capsulatus mutant lacking CcoA, these transporters were unable to accumulate Cu or complement for cbb3-Cox defect. This lack of functional exchangeability between the different subfamilies of CalT homologs suggests that MFS-type bacterial copper importers might be species-specific.

Authors:
 [1];  [2];  [3];  [4];  [5]; ORCiD logo [6];  [3];  [7]
  1. Univ. of Pennsylvania, Philadelphia, PA (United States); Xiamen Univ., Xiamen (China)
  2. Brookhaven National Lab. (BNL), Upton, NY (United States)
  3. Univ. of Pennsylvania, Philadelphia, PA (United States)
  4. Univ. of Pennsylvania, Philadelphia, PA (United States); Geisel School of Medicine at Dartmouth, Hanover, NH (United States)
  5. Univ. of Chile, Santiago (Chile)
  6. Albert-Ludwigs-Univ.Freiburg, Freiburg (Germany)
  7. Univ. of Pennsylvania, Philadelphia, PA (United States); UMR CNRS 5254 and Univ. de Pau et des Pays de l'Adour, Pau (France)
Publication Date:
Research Org.:
Brookhaven National Lab. (BNL), Upton, NY (United States); Univ. of Pennsylvania, Philadelphia, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division
OSTI Identifier:
1497377
Alternate Identifier(s):
OSTI ID: 1597464
Report Number(s):
BNL-211298-2019-JAAM
Journal ID: ISSN 2045-2322
Grant/Contract Number:  
SC0012704; FG02-91ER20052
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; MFS-type transporter; Riboflavin transport; Copper transport; cbb3; cytochrome coxidase; CcoA and RfnT

Citation Formats

Zhang, Yang, Blaby-Haas, Crysten E., Steimle, Stefan, Verissimo, Andreia F., Garcia-Angulo, Victor A., Koch, Hans -Georg, Daldal, Fevzi, and Khalfaoui-Hassani, Bahia. Cu Transport by the Extended Family of CcoA-like Transporters (CalT) in Proteobacteria. United States: N. p., 2019. Web. https://doi.org/10.1038/s41598-018-37988-4.
Zhang, Yang, Blaby-Haas, Crysten E., Steimle, Stefan, Verissimo, Andreia F., Garcia-Angulo, Victor A., Koch, Hans -Georg, Daldal, Fevzi, & Khalfaoui-Hassani, Bahia. Cu Transport by the Extended Family of CcoA-like Transporters (CalT) in Proteobacteria. United States. https://doi.org/10.1038/s41598-018-37988-4
Zhang, Yang, Blaby-Haas, Crysten E., Steimle, Stefan, Verissimo, Andreia F., Garcia-Angulo, Victor A., Koch, Hans -Georg, Daldal, Fevzi, and Khalfaoui-Hassani, Bahia. Mon . "Cu Transport by the Extended Family of CcoA-like Transporters (CalT) in Proteobacteria". United States. https://doi.org/10.1038/s41598-018-37988-4. https://www.osti.gov/servlets/purl/1497377.
@article{osti_1497377,
title = {Cu Transport by the Extended Family of CcoA-like Transporters (CalT) in Proteobacteria},
author = {Zhang, Yang and Blaby-Haas, Crysten E. and Steimle, Stefan and Verissimo, Andreia F. and Garcia-Angulo, Victor A. and Koch, Hans -Georg and Daldal, Fevzi and Khalfaoui-Hassani, Bahia},
abstractNote = {Comparative genomic studies of the bacterial MFS-type copper importer CcoA, required for cbb3-type cytochrome c oxidase (cbb3-Cox) biogenesis, revealed a widespread CcoA-like transporters (CalT) family, containing the conserved CcoA Cu-binding MxxxM and HxxxM motifs. Surprisingly, this family also included the RfnT-like proteins, earlier suggested to transport riboflavin. However, presence of the Cu-binding motifs in these proteins raised the possibility that they might be Cu transporters. To test this hypothesis, the genomic context of the corresponding genes was examined, and three of such genes from Ochrobactrum anthropi, Rhodopseudomonas palustris and Agrobacterium tumefaciens were expressed in Escherichia coli (ΔribB) and Rhodobacter capsulatus (ΔccoA) mutants. Copper and riboflavin uptake abilities of these strains were compared with those expressing R. capsulatus CcoA and Rhizobium leguminosarum RibN as bona fide copper and riboflavin importers, respectively. Altogether data demonstrated that the “RfnT-like” CalT proteins are unable to efficiently transport riboflavin, but they import copper like CcoA. Nevertheless, even though expressed and membrane-localized in a R. capsulatus mutant lacking CcoA, these transporters were unable to accumulate Cu or complement for cbb3-Cox defect. This lack of functional exchangeability between the different subfamilies of CalT homologs suggests that MFS-type bacterial copper importers might be species-specific.},
doi = {10.1038/s41598-018-37988-4},
journal = {Scientific Reports},
number = 1,
volume = 9,
place = {United States},
year = {2019},
month = {2}
}

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    Works referencing / citing this record:

    The cbb 3 -type cytochrome oxidase assembly factor CcoG is a widely distributed cupric reductase
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