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2.A.51 The Chromate Ion Transporter (CHR) Family

Homologues of the CHR family have been identified in bacteria, eukaryotes and archaea. Two Bacillus homologues are half length with six putative TMSs each (Nies et al., 1998). These two proteins together (2.A.51.1.5), but not singly, cause chromate resistance due to formation of a heterodimer and consequent chromate efflux (Díaz-Magaña et al., 2009). Half-sized homologues are found in several bacteria. The functionally characterized chromate efflux pumps of P. aeruginosa and A. eutrophus are plasmid-encoded. They are about 400 amino acyl residues long with 10 putative transmembrane α-helical spanners (TMSs). They arose by a tandem internal gene duplication event from a putative 6 TMS primordial precursor, but the first two TMSs in the A. entrophus ChrA protein have lost their hydrophobic character (Nies et al., 1998).

In a more recent study, (Diaz-Perez et al., 2007), 77 duplicated 'bidomains' (BDs) and 58 unduplicated 'monodomains' (MDs) were identified and analyzed. The MDs clustered separately from the N-terminal BDs, and both clustered separately from the C-terminal BDs. This suggests that the MDs, possibly present in inverted orientation in the membrane, may have a unique structure and mode of action (Diaz-Perez et al., 2007).

A more recent study of the membrane topology of the ChrA protein of P. aeruginosa was conducted using lacZ and phoA translational fusions (Jiminez-Mejia et al., 2006). A 13 TMS topology was predicted with the N-terminus in the cytoplasm and the C-terminus in the periplasm. Predicted TMSs 1-6 proved to be homologous to predicted TMSs 8-13, but with opposite orientation in the membrane.

Synechococcus sp. PCC7942 bears an endogenous 50 Kb plasmid-encoded, sulfur-regulated CHR homologue that apparently confers chromate sensitivity (rather than chromate resistance) when grown in media containing a low sulfate concentration. This protein, designated SrpC, may be a sulfate uptake permease that can also transport chromate, but this possibility has not been established. ChrA of P. aeruginosa is a secondary carrier which might function by chromate uniport, chromate:H+ antiport, or chromate:anion antiport. It catalyzes CrO4 efflux with a Km of 80 μM. SO4= and MoO4= inhibit efflux but arsenate and vanadate do not inhibit (Pimentel et al., 2002). A pmf dependency is likely since valinomycin, nigericin and protonophores such as CCCP inhibit. Ramírez-Díaz et al. (2008) have published a review concerning the mechanisms of bacterial resistance to chromium compounds.

The generalized transport reaction catalyzed by CHR may be:

CrO42- (in) [+ nH+ (out)] → CrO42- (out) [+ nH+ (in)]

The generalized transport reaction catalyzed by SrpC may be:

SO42- or CrO42- (out) + nH+ (out) → SO42- or CrO42- (in) + nH+ (in)

References associated with 2.A.51 family:

Aguilar-Barajas, E., E. Paluscio, C. Cervantes, and C. Rensing. (2008). Expression of chromate resistance genes from Shewanella sp. strain ANA-3 in Escherichia coli. FEMS Microbiol. Lett. 285: 97-100. 18537831
Alvarez, A.H., R. Moreno-Sánchez, and C. Cervantes. (1999). Chromate efflux by means of the ChrA chromate resistance protein from Pseudomonas aeruginosa. J. Bacteriol. 181: 7398-7400. 10572148
Cervantes, C., H. Ohtake, L. Chu, T.K. Misra, and S. Silver. (1990). Cloning, nucleotide sequence, and expression of the chromate resistance determinant of Pseudomonas aeruginosa plasmid pUM505. J. Bacteriol. 172: 287-291. 2152903
Diaz-Magana A., Aguilar-Barajas E., Moreno-Sanchez R., Ramirez-Diaz MI., Riveros-Rosas H., Vargas E. and Cervantes C. (2009). Short-chain chromate ion transporter proteins from Bacillus subtilis confer chromate resistance in Escherichia coli. J Bacteriol. 191(17):5441-5. 19581367
Diaz-Perez, C., C. Cervantes, J. Campos-García, A. Julián-Sánchez, and H. Riveros-Rosas. (2007). Phylogenetic analysis of the chromate ion transporter (CHR) superfamily. FEBS J. 274(23):6215-6227. 17986256
Jimenez-Mejia, R., J. Campos-Garcia, and C. Cervantes. (2006). Membrane topology of the chromate transporter ChrA of Pseudomonas aeruginosa. FEMS Microbiol. Lett. 262: 178-184. 16923073
Martínez-Valencia, R., G. Reyes-Cortés, M.I. Ramírez-Díaz, H. Riveros-Rosas, and C. Cervantes. (2012). Antiparallel membrane topology of paired short-chain chromate transport proteins in Bacillus subtilis. FEMS Microbiol. Lett. 336: 113-121. 22900751
Nicholson, M.L. and D.E. Laudenbach. (1995). Genes encoded on a cyanobacterial plasmid are transcriptionally regulated by sulfur availability and CysR. J. Bacteriol. 177: 2143-2150. 7536734
Nies, A., D.H. Nies, and S. Silver. (1990). Nucleotide sequence and expression of a plasmid-encoded chromate resistance determinant from Alcaligenes eutrophus. J. Biol. Chem. 265: 5648-5653. 2180932
Nies, D., S. Koch, S. Wachi, N. Peitzsch, and M.H. Saier, Jr. (1998). CHR, a novel family of prokaryotic proton motive force-driven transporters probably containing chromate/sulfate antiporters. J. Bacteriol. 180: 5799-5802. 9791139
Nies, D.H. and S. Silver. (1995). Ion efflux systems involved in bacterial metal resistances. J. Indus. Microbiol. 14: 186-199. 7766211
Pimentel, B.E., R. Moreno-Sanchez, and C. Cervantes. (2002). Efflux of chromate by Pseudomonas aeruginosa cells expressing the ChrA protein. FEMS Microbiol. Lett. 212: 249-254. 12113942
Ramírez-Díaz, M.I., C. Díaz-Pérez, E. Vargas, H. Riveros-Rosas, J. Campos-García, and C. Cervantes. (2008). Mechanisms of bacterial resistance to chromium compounds. Biometals 21: 321-332. 17934697