Mrp Antiporters Have Important Roles in Diverse Bacteria and Archaea

Masahiro Ito1,2, Masato Morino3,2, Terry A. Krulwich3
1Bio-Nano Electronics Research Center, Toyo University, Japan
2Graduate School of Life Sciences, Toyo University, Japan
3Department of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, United States

Tóm tắt

Từ khóa


Tài liệu tham khảo

Aagesen, 2016, Effects of chromosomal deletion of the operon encoding the multiple resistance and pH-related antiporter in Vibrio cholerae., Microbiology, 162, 2147, 10.1099/mic.0.000384

Baranova, 2007, Single particle analysis confirms distal location of subunits NuoL and NuoM in Escherichia coli complex I., J. Struct. Biol., 159, 238, 10.1016/j.jsb.2007.01.009

Blanco-Rivero, 2009, mrpA (all1838), a gene involved in alkali and Na+ sensitivity, may also have a role in energy metabolism in the cyanobacterium Anabaena sp. strain PCC 7120., J. Plant Physiol., 166, 1488, 10.1016/j.jplph.2009.03.007

Boyd, 2014, Hydrogen metabolism and the evolution of biological respiration., Microbe, 9, 361, 10.1128/microbe.9.361.1

Cheng, 2016, Alkaline response of a halotolerant alkaliphilic halomonas strain and functional diversity of its Na+ (K+)/H+ antiporters., J. Biol. Chem., 291, 26056, 10.1074/jbc.M116.751016

Dibrov, 2005, The sodium cycle in Vibrio cholerae: riddles in the dark., Biochemistry, 70, 150, 10.1007/s10541-005-0094-3

Dzioba-Winogrodzki, 2009, The Vibrio cholerae Mrp system: cation/proton antiport properties and enhancement of bile salt resistance in a heterologous host., J. Mol. Microbiol. Biotechnol., 16, 176, 10.1159/000119547

Efremov, 2011, Structure of the membrane domain of respiratory complex I., Nature, 476, 414, 10.1038/nature10330

Fujinami, 2013, Draft genome sequence of sodium-independent alkaliphilic Microbacterium sp. strain TS-1., Genome Announc., 1, 10.1128/genomeA.01043-13

Fukaya, 2009, An Mrp-like cluster in the halotolerant cyanobacterium Aphanothece halophytica functions as a Na+/H+ antiporter., Appl. Environ. Microbiol., 75, 6626, 10.1128/AEM.01387-09

Fuster, 2014, Traditional and emerging roles for the SLC9 Na+/H+ exchangers., Pflugers Arch., 466, 61, 10.1007/s00424-013-1408-8

Gemperli, 2007, Transport of Na+ and K+ by an antiporter-related subunit from the Escherichia coli NADH dehydrogenase I produced in Saccharomyces cerevisiae., Arch. Microbiol., 188, 509, 10.1007/s00203-007-0272-3

Hamamoto, 1994, Characterization of a gene responsible for the Na+/H+ antiporter system of alkalophilic Bacillus species strain C-125., Mol. Microbiol., 14, 939, 10.1111/j.1365-2958.1994.tb01329.x

Hisamitsu, 2012, Na+/H+ exchanger 1 directly binds to calcineurin A and activates downstream NFAT signaling, leading to cardiomyocyte hypertrophy., Mol. Cell. Biol., 32, 3265, 10.1128/MCB.00145-12

Holt, 2003, The location of NuoL and NuoM subunits in the membrane domain of the Escherichia coli complex I: implications for the mechanism of proton pumping., J. Biol. Chem., 278, 43114, 10.1074/jbc.M308247200

Ito, 1999, mrp, a multigene, multifunctional locus in Bacillus subtilis with roles in resistance to cholate and to Na+ and in pH homeostasis., J. Bacteriol., 181, 2394, 10.1128/JB.181.8.2394-2402.1999

Ito, 2000, Effects of nonpolar mutations in each of the seven Bacillus subtilis mrp genes suggest complex interactions among the gene products in support of Na+ and alkali but not cholate resistance., J. Bacteriol., 182, 5663, 10.1128/JB.182.20.5663-5670.2000

Ivey, 1993, Cloning and characterization of a putative Ca2+/H+ antiporter gene from Escherichia coli upon functional complementation of Na+/H+ antiporter-deficient strains by the overexpressed gene., J. Biol. Chem., 268, 11296, 10.1016/S0021-9258(18)82124-X

Jackson, 1973, Thermomicrobium, a new genus of extremely thermophilic bacteria., Int. J. Syst. Bacteriol., 23, 28, 10.1099/00207713-23-1-28

Jasso-Chavez, 2013, MrpA functions in energy conversion during acetate-dependent growth of Methanosarcina acetivorans., J. Bacteriol., 195, 3987, 10.1128/JB.00581-13

Jasso-Chavez, 2017, Functional role of MrpA in the MrpABCDEFG Na+/H+ antiporter complex from the Archaeon Methanosarcina acetivorans., J. Bacteriol., 199, 10.1128/JB.00662-16

Ji, 2001, Identification of critical staphylococcal genes using conditional phenotypes generated by antisense RNA., Science, 293, 2266, 10.1126/science.1063566

Kajiyama, 2007, Complex formation by the mrpABCDEFG gene products, which constitute a principal Na+/H+ antiporter in Bacillus subtilis., J. Bacteriol., 189, 7511, 10.1128/JB.00968-07

Kajiyama, 2009, The MrpA, MrpB and MrpD subunits of the Mrp antiporter complex in Bacillus subtilis contain membrane-embedded and essential acidic residues., Microbiology, 155, 2137, 10.1099/mic.0.025205-0

Kashyap, 2006, A Na+:H+ antiporter and a molybdate transporter are essential for arsenite oxidation in Agrobacterium tumefaciens., J. Bacteriol., 188, 1577, 10.1128/JB.188.4.1577-1584.2006

Kim, 2010, Formate-driven growth coupled with H2 production., Nature, 467, 352, 10.1038/nature09375

Kosono, 2005, Characterization of a multigene-encoded sodium/hydrogen antiporter (sha) from Pseudomonas aeruginosa: its involvement in pathogenesis., J. Bacteriol., 187, 5242, 10.1128/JB.187.15.5242-5248.2005

Kosono, 2006, Functional involvement of membrane-embedded and conserved acidic residues in the ShaA subunit of the multigene-encoded Na+/H+ antiporter in Bacillus subtilis., Biochim. Biophys. Acta, 1758, 627, 10.1016/j.bbamem.2006.04.012

Kosono, 1999, Analyses of a Bacillus subtilis homologue of the Na+/H+ antiporter gene which is important for pH homeostasis of alkaliphilic Bacillus sp. C-125., Biochim. Biophys. Acta, 1409, 171, 10.1016/S0005-2728(98)00157-1

Kosono, 2000, Function of a principal Na+/H+ antiporter, ShaA, is required for initiation of sporulation in Bacillus subtilis., J. Bacteriol., 182, 898, 10.1128/JB.182.4.898-904.2000

Krulwich, 2009, Cation/proton antiporter complements of bacteria: Why so large and diverse?, Mol. Microbiol., 74, k257, 10.1111/j.1365-2958.2009.06842.x

Krulwich, 2013, “Prokaryotic alkaliphiles,” in, The Prokaryotes, 10.1007/978-3-642-30123-0_58

Krulwich, 2011, Molecular aspects of bacterial pH sensing and homeostasis., Nat. Rev. Microbiol., 9, 330, 10.1038/nrmicro2549

Kudo, 1990, DNA sequences required for the alkalophily of Bacillus sp. strain C-125 are located close together on its chromosomal DNA., J. Bacteriol., 172, 7282, 10.1128/jb.172.12.7282-7283.1990

Lewinson, 2003, The Escherichia coli multidrug transporter MdfA catalyzes both electrogenic and electroneutral transport reactions., Proc. Natl. Acad. Sci. U.S.A., 100, 1667, 10.1073/pnas.0435544100

Lim, 2010, Identification of a novel class of membrane-bound [NiFe]-hydrogenases in Thermococcus onnurineus NA1 by in silico analysis., Appl. Environ. Microbiol., 76, 6286, 10.1128/AEM.00123-10

Lim, 2014, Energy conservation by oxidation of formate to carbon dioxide and hydrogen via a sodium ion current in a hyperthermophilic archaeon., Proc. Natl. Acad. Sci. U.S.A., 111, 11497, 10.1073/pnas.1407056111

Marreiros, 2014, Respiratory complex I from Escherichia coli does not transport Na+ in the absence of its NuoL subunit., FEBS Lett., 588, 4520, 10.1016/j.febslet.2014.10.030

Mathiesen, 2003, The ‘antiporter module’ of respiratory chain complex I includes the MrpC/NuoK subunit – a revision of the modular evolution scheme., FEBS Lett., 549, 7, 10.1016/S0014-5793(03)00767-1

Meng, 2014, Cloning and identification of Group 1 mrp operon encoding a novel monovalent cation/proton antiporter system from the moderate halophile Halomonas zhaodongensis., Extremophiles, 18, 963, 10.1007/s00792-014-0666-5

Mesbah, 2009, The halophilic alkalithermophile Natranaerobius thermophilus adapts to multiple environmental extremes using a large repertoire of Na+ (K+)/H+ antiporters., Mol. Microbiol., 74, 270, 10.1111/j.1365-2958.2009.06845.x

Moparthi, 2011, “Recruitment of the antiporter module — a key event in complex I evolution,” in, A Structural Perspective on Complex I, 123

Moparthi, 2014, Functional role of the MrpA- and MrpD-homologous protein subunits in enzyme complexes evolutionary related to respiratory chain complex I., Biochim. Biophys. Acta, 1837, 178, 10.1016/j.bbabio.2013.09.012

Moparthi, 2011, Homologous protein subunits from Escherichia coli NADH:quinone oxidoreductase can functionally replace MrpA and MrpD in Bacillus subtilis., Biochim. Biophys. Acta, 1807, 427, 10.1016/j.bbabio.2011.01.005

Morino, 2012, Functional expression of the multi-subunit type calcium/proton antiporter from Thermomicrobium roseum., FEMS Microbiol. Lett., 335, 26, 10.1111/j.1574-6968.2012.02634.x

Morino, 2010, Single site mutations in the hetero-oligomeric Mrp antiporter from alkaliphilic Bacillus pseudofirmus OF4 that affect Na+/H+ antiport activity, sodium exclusion, individual Mrp protein levels, or Mrp complex formation., J. Biol. Chem., 285, 30942, 10.1074/jbc.M110.118661

Morino, 2008, Single gene deletions of mrpA to mrpG and mrpE point mutations affect activity of the Mrp Na+/H+ antiporter of alkaliphilic Bacillus and formation of hetero-oligomeric Mrp complexes., J. Bacteriol., 190, 4162, 10.1128/JB.00294-08

Morino, 2017, Differences in the phenotypic effects of mutations in homologous MrpA and MrpD subunits of the multi-subunit Mrp-type Na+/H+ antiporter., Extremophiles, 21, 51, 10.1007/s00792-016-0877-z

Morino, 2014, Purification and functional reconstitution of a seven-subunit mrp-type Na+/H+ antiporter., J. Bacteriol., 196, 28, 10.1128/JB.01029-13

Mourin, 2017, Physiology of the Vc-NhaP paralogous group of cation-proton antiporters in Vibrio cholerae., Mol. Cell. Biochem., 428, 87, 10.1007/s11010-016-2919-3

Nakamaru-Ogiso, 2010, The membrane subunit NuoL(ND5) is involved in the indirect proton pumping mechanism of Escherichia coli complex I., J. Biol. Chem., 285, k39070, 10.1074/jbc.M110.157826

Nakamaru-Ogiso, , The ND5 subunit was labeled by a photoaffinity analogue of fenpyroximate in bovine mitochondrial complex I., Biochemistry, 42, 746, 10.1021/bi0269660

Nakamaru-Ogiso, , Amiloride inhibition of the proton-translocating NADH-quinone oxidoreductase of mammals and bacteria., FEBS Lett., 549, 43, 10.1016/S0014-5793(03)00766-X

Ohgaki, 2011, Organellar Na+/H+ exchangers: novel players in organelle pH regulation and their emerging functions., Biochemistry, 50, 443, 10.1021/bi101082e

Ohnishi, 2010, A new hypothesis on the simultaneous direct and indirect proton pump mechanisms in NADH-quinone oxidoreductase (complex I)., FEBS Lett., 584, 4131, 10.1016/j.febslet.2010.08.039

Orlowski, 2004, Diversity of the mammalian sodium/proton exchanger SLC9 gene family., Pflugers Arch., 447, 549, 10.1007/s00424-003-1110-3

Orlowski, 2011, Na+/H+ exchangers., Compr. Physiol., 1, 2083, 10.1002/cphy.c110020

Padan, 2014, Functional and structural dynamics of NhaA, a prototype for Na+ and H+ antiporters, which are responsible for Na+ and H+ homeostasis in cells., Biochim. Biophys. Acta, 1837, 1047, 10.1016/j.bbabio.2013.12.007

Padan, 2005, Alkaline pH homeostasis in bacteria: new insights., Biochim. Biophys. Acta, 1717, 67, 10.1016/j.bbamem.2005.09.010

Padan, 2016, Sodium-proton (Na+/H+) antiporters: properties and roles in health and disease., Met. Ions Life Sci., 16, 391, 10.1007/978-3-319-21756-7_12

Padan, 1994, Molecular physiology of the Na+/H+ antiporter in Escherichia coli., J. Exp. Biol., 196, 443, 10.1242/jeb.196.1.443

Padan, 2001, Na+/H+ antiporters., Biochim. Biophys. Acta, 1505, 144, 10.1016/S0005-2728(00)00284-X

Pang, 2001, Calcineurin homologous protein as an essential cofactor for Na+/H+ exchangers., J. Biol. Chem., 276, 17367, 10.1074/jbc.M100296200

Preiss, 2015, Alkaliphilic bacteria with impact on industrial applications, concepts of early life forms, and bioenergetics of ATP synthesis., Front. Bioeng. Biotechnol., 3, 10.3389/fbioe.2015.00075

Putnoky, 1998, The pha gene cluster of Rhizobium meliloti involved in pH adaptation and symbiosis encodes a novel type of K+ efflux system., Mol. Microbiol., 28, 1091, 10.1046/j.1365-2958.1998.00868.x

Resch, 2011, Insights into the biochemistry of the ubiquitous NhaP family of cation/H+ antiporters., Biochem. Cell Biol., 89, 130, 10.1139/o10-149

Saier, 2016, The transporter classification database (TCDB): recent advances., Nucleic Acids Res., 44, D372, 10.1093/nar/gkv1103

Saier, 2009, The transporter classification database: recent advances., Nucleic Acids Res., 37, D274, 10.1093/nar/gkn862

Sazanov, 2014, The mechanism of coupling between electron transfer and proton translocation in respiratory complex I., J. Bioenerg. Biomembr., 46, 247, 10.1007/s10863-014-9554-z

Sazanov, 2015, A giant molecular proton pump: structure and mechanism of respiratory complex I., Nat. Rev. Mol. Cell Biol., 16, 375, 10.1038/nrm3997

Schut, 2013, The modular respiratory complexes involved in hydrogen and sulfur metabolism by heterotrophic hyperthermophilic archaea and their evolutionary implications., FEMS Microbiol. Rev., 37, 182, 10.1111/j.1574-6976.2012.00346.x

Shijuku, 2002, Expression of chaA, a sodium ion extrusion system of Escherichia coli, is regulated by osmolarity and pH., Biochim. Biophys. Acta, 1556, 142, 10.1016/S0005-2728(02)00345-6

Sperling, 2016, Functional differentiation of antiporter-like polypeptides in complex I; a site-directed mutagenesis study of residues conserved in MrpA and NuoL but not in MrpD, NuoM, and NuoN., PLOS ONE, 11, 10.1371/journal.pone.0158972

Steuber, 2003, The C-terminally truncated NuoL subunit (ND5 homologue) of the Na+-dependent complex I from Escherichia coli transports Na+., J. Biol. Chem., 278, 26817, 10.1074/jbc.M301682200

Swartz, 2005, The Mrp system: a giant among monovalent cation/proton antiporters?, Extremophiles, 9, 345, 10.1007/s00792-005-0451-6

Swartz, 2007, Catalytic properties of Staphylococcus aureus and Bacillus members of the secondary cation/proton antiporter-3 (Mrp) family are revealed by an optimized assay in an Escherichia coli host., J. Bacteriol., 189, 3081, 10.1128/JB.00021-07

Terashima, 2010, The flagellar basal body-associated protein FlgT is essential for a novel ring structure in the sodium-driven Vibrio motor., J. Bacteriol., 192, 5609, 10.1128/JB.00720-10

Torres-Bacete, 2007, Characterization of the NuoM (ND4) subunit in Escherichia coli NDH-1: conserved charged residues essential for energy-coupled activities., J. Biol. Chem., 282, 36914, 10.1074/jbc.M707855200

Torres-Bacete, 2011, Structural contribution of C-terminal segments of NuoL (ND5) and NuoM (ND4) subunits of complex I from Escherichia coli., J. Biol. Chem., 286, 34007, 10.1074/jbc.M111.260968

Vimont, 2000, NhaA, an Na+/H+ antiporter involved in environmental survival of Vibrio cholerae., J. Bacteriol., 182, 2937, 10.1128/JB.182.10.2937-2944.2000

Waditee, 2001, Halotolerant cyanobacterium Aphanothece halophytica contains an Na+/H+ antiporter, homologous to eukaryotic ones, with novel ion specificity affected by C-terminal tail., J. Biol. Chem., 276, 36931, 10.1074/jbc.M103650200

Wakabayashi, 1997, Molecular physiology of vertebrate Na+/H+ exchangers., Physiol. Rev., 77, 51, 10.1152/physrev.1997.77.1.51

Yamaguchi, 2009, pH-dependent regulation of the multi-subunit cation/proton antiporter Pha1 system from Sinorhizobium meliloti., Microbiology, 155, 2750, 10.1099/mic.0.028563-0

Yoshinaka, 2003, A shaE deletion mutant showed lower Na+ sensitivity compound to other deletion mutants in the Bacillus subtilis sodium/hydrogen antiporter (Sha) system., J. Biosci. Bioeng., 95, 306, 10.1016/S1389-1723(03)80035-X

Zilberstein, 1982, The sodium/proton antiporter is part of the pH homeostasis mechanism in Escherichia coli., J. Biol. Chem., 257, 3687, 10.1016/S0021-9258(18)34835-X