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:
-
[6];
- Univ. of Pennsylvania, Philadelphia, PA (United States); Xiamen Univ., Xiamen (China)
- Brookhaven National Lab. (BNL), Upton, NY (United States)
- Univ. of Pennsylvania, Philadelphia, PA (United States)
- Univ. of Pennsylvania, Philadelphia, PA (United States); Geisel School of Medicine at Dartmouth, Hanover, NH (United States)
- Univ. of Chile, Santiago (Chile)
- Albert-Ludwigs-Univ.Freiburg, Freiburg (Germany)
- 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. doi: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}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 6 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Involvement of SenC in Assembly of Cytochrome c Oxidase in Rhodobacter capsulatus
journal, November 2005
- Swem, D. L.; Swem, L. R.; Setterdahl, A.
- Journal of Bacteriology, Vol. 187, Issue 23
Absence of Thiol-Disulfide Oxidoreductase DsbA Impairs cbb3-Type Cytochrome c Oxidase Biogenesis in Rhodobacter capsulatus
journal, December 2017
- Onder, Ozlem; Verissimo, Andreia F.; Khalfaoui-Hassani, Bahia
- Frontiers in Microbiology, Vol. 8
SoxAX Cytochromes, a New Type of Heme Copper Protein Involved in Bacterial Energy Generation from Sulfur Compounds
journal, June 2008
- Kappler, Ulrike; Bernhardt, Paul V.; Kilmartin, James
- Journal of Biological Chemistry, Vol. 283, Issue 32
Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): A web tool for generating protein sequence similarity networks
journal, August 2015
- Gerlt, John A.; Bouvier, Jason T.; Davidson, Daniel B.
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1854, Issue 8
UFBoot2: Improving the Ultrafast Bootstrap Approximation
journal, October 2017
- Hoang, Diep Thi; Chernomor, Olga; von Haeseler, Arndt
- Molecular Biology and Evolution, Vol. 35, Issue 2
UniProt: the universal protein knowledgebase
journal, November 2016
- :(unav),
- Nucleic Acids Research, Vol. 45, Issue D1, p. D158-D169
Ins and Outs of Major Facilitator Superfamily Antiporters
journal, October 2008
- Law, Christopher J.; Maloney, Peter C.; Wang, Da-Neng
- Annual Review of Microbiology, Vol. 62, Issue 1, p. 289-305
Crystal structure of a prokaryotic homologue of the mammalian oligopeptide-proton symporters, PepT1 and PepT2: Crystal structure of a POT family oligopeptide transporter
journal, December 2010
- Newstead, Simon; Drew, David; Cameron, Alexander D.
- The EMBO Journal, Vol. 30, Issue 2
Identification and Characterization of RibN, a Novel Family of Riboflavin Transporters from Rhizobium leguminosarum and Other Proteobacteria
journal, August 2013
- Garcia Angulo, V. A.; Bonomi, H. R.; Posadas, D. M.
- Journal of Bacteriology, Vol. 195, Issue 20
A Copper Relay System Involving Two Periplasmic Chaperones Drives cbb 3 -Type Cytochrome c Oxidase Biogenesis in Rhodobacter capsulatus
journal, April 2018
- Trasnea, Petru-Iulian; Andrei, Andreea; Marckmann, Dorian
- ACS Chemical Biology, Vol. 13, Issue 5
Understanding transport by the major facilitator superfamily (MFS): structures pave the way
journal, January 2016
- Quistgaard, Esben M.; Löw, Christian; Guettou, Fatma
- Nature Reviews Molecular Cell Biology, Vol. 17, Issue 2
Biogenesis of cbb3-type cytochrome c oxidase in Rhodobacter capsulatus
journal, June 2012
- Ekici, Seda; Pawlik, Grzegorz; Lohmeyer, Eva
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 6
Copper transport and regulation in Schizosaccharomyces pombe
journal, November 2013
- Beaudoin, Jude; Ekici, Seda; Daldal, Fevzi
- Biochemical Society Transactions, Vol. 41, Issue 6
Structural advances for the major facilitator superfamily (MFS) transporters
journal, March 2013
- Yan, Nieng
- Trends in Biochemical Sciences, Vol. 38, Issue 3
CtpA, a Copper-translocating P-type ATPase Involved in the Biogenesis of Multiple Copper-requiring Enzymes
journal, April 2010
- Hassani, Bahia Khalfaoui; Astier, Chantal; Nitschke, Wolfgang
- Journal of Biological Chemistry, Vol. 285, Issue 25
Intracytoplasmic Copper Homeostasis Controls Cytochrome c Oxidase Production
journal, January 2014
- Ekici, Seda; Turkarslan, Serdar; Pawlik, Grzegorz
- mBio, Vol. 5, Issue 1
Copper Metallochaperones
journal, June 2010
- Robinson, Nigel J.; Winge, Dennis R.
- Annual Review of Biochemistry, Vol. 79, Issue 1
Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome c Oxidases
journal, February 2018
- Khalfaoui-Hassani, Bahia; Wu, Hongjiang; Blaby-Haas, Crysten E.
- mBio, Vol. 9, Issue 1
Characterization of Riboflavin (Vitamin B2) Transport Proteins from Bacillus subtilis and Corynebacterium glutamicum
journal, August 2007
- Vogl, C.; Grill, S.; Schilling, O.
- Journal of Bacteriology, Vol. 189, Issue 20
Structure and mechanism of the S component of a bacterial ECF transporter
journal, October 2010
- Zhang, Peng; Wang, Jiawei; Shi, Yigong
- Nature, Vol. 468, Issue 7324
Novel Transporter Required for Biogenesis of cbb3-Type Cytochrome c Oxidase in Rhodobacter capsulatus
journal, January 2012
- Ekici, Seda; Yang, Honghui; Koch, Hans-Georg
- mBio, Vol. 3, Issue 1
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014
- Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
- Molecular Biology and Evolution, Vol. 32, Issue 1
InterPro in 2017—beyond protein family and domain annotations
journal, November 2016
- Finn, Robert D.; Attwood, Teresa K.; Babbitt, Patricia C.
- Nucleic Acids Research, Vol. 45, Issue D1
Mutagenesis of methionine-183 drastically affects the physicochemical properties of cytochrome c1 of the bc1 complex of Rhodobacter capsulatus
journal, December 1992
- Gray, Kevin A.; Davidson, Edgar; Daldal, Fevzi
- Biochemistry, Vol. 31, Issue 47
Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation
journal, July 2002
- Vitreschak, A. G.
- Nucleic Acids Research, Vol. 30, Issue 14
Crystal structure of the human glucose transporter GLUT1
journal, May 2014
- Deng, Dong; Xu, Chao; Sun, Pengcheng
- Nature, Vol. 510, Issue 7503
The Transporter Classification Database (TCDB): recent advances
journal, November 2015
- Saier, Milton H.; Reddy, Vamsee S.; Tsu, Brian V.
- Nucleic Acids Research, Vol. 44, Issue D1
Extensive Identification of Bacterial Riboflavin Transporters and Their Distribution across Bacterial Species
journal, May 2015
- Gutiérrez-Preciado, Ana; Torres, Alfredo Gabriel; Merino, Enrique
- PLOS ONE, Vol. 10, Issue 5
Structure and Mechanism of the Lactose Permease of Escherichia coli
journal, August 2003
- Abramson, J.
- Science, Vol. 301, Issue 5633
Identification and characterization of two Streptomyces davawensis riboflavin biosynthesis gene clusters
journal, June 2007
- Grill, Simon; Yamaguchi, Hiroyuki; Wagner, Helen
- Archives of Microbiology, Vol. 188, Issue 4
Distinct functional roles of homologous Cu+ efflux ATPases in Pseudomonas aeruginosa: Role of Cu+ transport ATPases in Pseudomonas aeruginosa
journal, October 2010
- González-Guerrero, Manuel; Raimunda, Daniel; Cheng, Xin
- Molecular Microbiology, Vol. 78, Issue 5
Biosynthesis of flavocoenzymes
journal, January 2005
- Fischer, Markus; Bacher, Adelbert
- Natural Product Reports, Vol. 22, Issue 3
COBALT: constraint-based alignment tool for multiple protein sequences
journal, March 2007
- Papadopoulos, J. S.; Agarwala, R.
- Bioinformatics, Vol. 23, Issue 9
Creating the CIPRES Science Gateway for inference of large phylogenetic trees
conference, November 2010
- Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri
- 2010 Gateway Computing Environments Workshop (GCE)
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003
- Shannon, P.
- Genome Research, Vol. 13, Issue 11
The use of gene clusters to infer functional coupling
journal, March 1999
- Overbeek, R.; Fonstein, M.; D'Souza, M.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 6
Structure and Mechanism of the Glycerol-3-Phosphate Transporter from Escherichia coli
journal, August 2003
- Huang, Y.
- Science, Vol. 301, Issue 5633
ATP binding drives substrate capture in an ECF transporter by a release-and-catch mechanism
journal, June 2015
- Karpowich, Nathan K.; Song, Jin Mei; Cocco, Nicolette
- Nature Structural & Molecular Biology, Vol. 22, Issue 7
Movement of the Iron-Sulfur Subunit beyond the ef Loop of Cytochrome b Is Required for Multiple Turnovers of the bc 1 Complex but Not for Single Turnover Q o Site Catalysis
journal, November 2001
- Darrouzet, Elisabeth; Daldal, Fevzi
- Journal of Biological Chemistry, Vol. 277, Issue 5
Transcriptomics reveals a cross-modulatory effect between riboflavin and iron and outlines responses to riboflavin biosynthesis and uptake in Vibrio cholerae
journal, February 2018
- Sepúlveda-Cisternas, Ignacio; Lozano Aguirre, Luis; Fuentes Flores, Andrés
- Scientific Reports, Vol. 8, Issue 1
Uncovering the Transmembrane Metal Binding Site of the Novel Bacterial Major Facilitator Superfamily-Type Copper Importer CcoA
journal, January 2016
- Khalfaoui-Hassani, Bahia; Verissimo, Andreia F.; Koch, Hans-Georg
- mBio, Vol. 7, Issue 1
Cooperation between two periplasmic copper chaperones is required for full activity of the cbb 3 -type cytochrome c oxidase and copper homeostasis in Rhodobacter capsulatus : PccA-SenC interactions determine
journal, February 2016
- Trasnea, Petru-Iulian; Utz, Marcel; Khalfaoui-Hassani, Bahia
- Molecular Microbiology, Vol. 100, Issue 2
Energy coupling mechanisms of MFS transporters: Energy Coupling Mechanisms of MFS Transporters
journal, September 2015
- Zhang, Xuejun C.; Zhao, Yan; Heng, Jie
- Protein Science, Vol. 24, Issue 10
RibM from Streptomyces davawensis is a riboflavin/roseoflavin transporter and may be useful for the optimization of riboflavin production strains
journal, January 2011
- Hemberger, Sabrina; Pedrolli, Danielle B.; Stolz, Jürgen
- BMC Biotechnology, Vol. 11, Issue 1
Jalview Version 2--a multiple sequence alignment editor and analysis workbench
journal, January 2009
- Waterhouse, A. M.; Procter, J. B.; Martin, D. M. A.
- Bioinformatics, Vol. 25, Issue 9
Overlapping riboflavin supply pathways in bacteria
journal, November 2016
- García-Angulo, Víctor Antonio
- Critical Reviews in Microbiology, Vol. 43, Issue 2
Skylign: a tool for creating informative, interactive logos representing sequence alignments and profile hidden Markov models
journal, January 2014
- Wheeler, Travis J.; Clements, Jody; Finn, Robert D.
- BMC Bioinformatics, Vol. 15, Issue 1
The roles of Rhodobacter sphaeroides copper chaperones PCuAC and Sco (PrrC) in the assembly of the copper centers of the aa3-type and the cbb3-type cytochrome c oxidases
journal, June 2012
- Thompson, Audie K.; Gray, Jimmy; Liu, Aimin
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 6
Roles of the ccoGHIS gene products in the biogenesis of the cbb3-type cytochrome c oxidase
journal, March 2000
- Koch, Hans-Georg; Winterstein, Christine; Saribas, A. Sami
- Journal of Molecular Biology, Vol. 297, Issue 1
Size of the amino acid side chain at position 158 of cytochrome b is critical for an active cytochrome bc1 complex and for photosynthetic growth of Rhodobacter capsulatus.
journal, January 1991
- Atta-Asafo-Adjei, E.; Daldal, F.
- Proceedings of the National Academy of Sciences, Vol. 88, Issue 2
A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport
journal, January 1993
- Marger, Michael D.; Saier, Milton H.
- Trends in Biochemical Sciences, Vol. 18, Issue 1
Major Facilitator Superfamily
journal, January 1998
- Pao, Stephanie S.; Paulsen, Ian T.; Saier, Milton H.
- Microbiology and Molecular Biology Reviews, Vol. 62, Issue 1
Isolation and Characterization of Rhodobacter capsulatus Mutants Affected in Cytochromecbb
3 Oxidase Activity
journal, January 1998
- Koch, Hans-Georg; Hwang, Olivia; Daldal, Fevzi
- Journal of Bacteriology, Vol. 180, Issue 4
Why does the Aβ peptide of Alzheimer share structural similarity with antimicrobial peptides?
journal, March 2020
- Pastore, Annalisa; Raimondi, Francesco; Rajendran, Lawrence
- Communications Biology, Vol. 3, Issue 1
A synthetic RNA editing factor edits its target site in chloroplasts and bacteria
journal, May 2021
- Royan, Santana; Gutmann, Bernard; Colas des Francs-Small, Catherine
- Communications Biology, Vol. 4, Issue 1
UniProt: the Universal Protein knowledgebase
journal, January 2004
- Apweiler, R.
- Nucleic Acids Research, Vol. 32, Issue 90001
Biosynthesis of Flavocoenzymes
journal, August 2005
- Fischer, Markus; Bacher, Adelbert
- ChemInform, Vol. 36, Issue 35
UniProt: the universal protein knowledgebase
journal, February 2018
- UniProt Consortium, The
- Nucleic Acids Research, Vol. 46, Issue 5
Works referencing / citing this record:
The cbb 3 -type cytochrome oxidase assembly factor CcoG is a widely distributed cupric reductase
journal, September 2019
- Marckmann, Dorian; Trasnea, Petru-Iulian; Schimpf, Johannes
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 42