{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,6]],"date-time":"2026-02-06T21:18:24Z","timestamp":1770412704376,"version":"3.49.0"},"reference-count":42,"publisher":"American Society for Microbiology","issue":"4","license":[{"start":{"date-parts":[[2016,2,15]],"date-time":"2016-02-15T00:00:00Z","timestamp":1455494400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"crossref","award":["14-14-00128"],"award-info":[{"award-number":["14-14-00128"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["J Bacteriol"],"published-print":{"date-parts":[[2016,2,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n          <jats:p>\n            Na\n            <jats:sup>+<\/jats:sup>\n            -translocating NADH:quinone oxidoreductase (Na\n            <jats:sup>+<\/jats:sup>\n            -NQR) catalyzes electron transfer from NADH to ubiquinone in the bacterial respiratory chain, coupled with Na\n            <jats:sup>+<\/jats:sup>\n            translocation across the membrane. Na\n            <jats:sup>+<\/jats:sup>\n            -NQR maturation involves covalent attachment of flavin mononucleotide (FMN) residues, catalyzed by flavin transferase encoded by the\n            <jats:italic>nqr<\/jats:italic>\n            -associated\n            <jats:italic>apbE<\/jats:italic>\n            gene. Analysis of complete bacterial genomes has revealed another putative gene (\n            <jats:italic>duf539<\/jats:italic>\n            , here renamed\n            <jats:italic>nqrM<\/jats:italic>\n            ) that usually follows the\n            <jats:italic>apbE<\/jats:italic>\n            gene and is present only in Na\n            <jats:sup>+<\/jats:sup>\n            -NQR-containing bacteria. Expression of the\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Vibrio harveyi<\/jats:named-content>\n            <jats:italic>nqr<\/jats:italic>\n            operon alone or with the associated\n            <jats:italic>apbE<\/jats:italic>\n            gene in\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Escherichia coli<\/jats:named-content>\n            , which lacks its own Na\n            <jats:sup>+<\/jats:sup>\n            -NQR, resulted in an enzyme incapable of Na\n            <jats:sup>+<\/jats:sup>\n            -dependent NADH or reduced nicotinamide hypoxanthine dinucleotide (dNADH) oxidation. However, fully functional Na\n            <jats:sup>+<\/jats:sup>\n            -NQR was restored when these genes were coexpressed with the\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">V. harveyi<\/jats:named-content>\n            <jats:italic>nqrM<\/jats:italic>\n            gene. Furthermore,\n            <jats:italic>nqrM<\/jats:italic>\n            lesions in\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Klebsiella pneumoniae<\/jats:named-content>\n            and\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">V. harveyi<\/jats:named-content>\n            prevented production of functional Na\n            <jats:sup>+<\/jats:sup>\n            -NQR, which could be recovered by an\n            <jats:italic>nqrM<\/jats:italic>\n            -containing plasmid. The Na\n            <jats:sup>+<\/jats:sup>\n            -NQR complex isolated from the\n            <jats:italic>nqrM<\/jats:italic>\n            -deficient strain of\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">V. harveyi<\/jats:named-content>\n            lacks several subunits, indicating that\n            <jats:italic>nqrM<\/jats:italic>\n            is necessary for Na\n            <jats:sup>+<\/jats:sup>\n            -NQR assembly. The protein product of the\n            <jats:italic>nqrM<\/jats:italic>\n            gene, NqrM, contains a single putative transmembrane \u03b1-helix and four conserved Cys residues. Mutating one of these residues (Cys33 in\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">V. harveyi<\/jats:named-content>\n            NqrM) to Ser completely prevented Na\n            <jats:sup>+<\/jats:sup>\n            -NQR maturation, whereas mutating any other Cys residue only decreased the yield of the mature protein. These findings identify NqrM as the second specific maturation factor of Na\n            <jats:sup>+<\/jats:sup>\n            -NQR in proteobacteria, which is presumably involved in the delivery of Fe to form the (Cys)\n            <jats:sub>4<\/jats:sub>\n            [Fe] center between subunits NqrD and NqrE.\n          <\/jats:p>\n          <jats:p>\n            <jats:bold>IMPORTANCE<\/jats:bold>\n            Na\n            <jats:sup>+<\/jats:sup>\n            -translocating NADH:quinone oxidoreductase complex (Na\n            <jats:sup>+<\/jats:sup>\n            -NQR) is a unique primary Na\n            <jats:sup>+<\/jats:sup>\n            pump believed to enhance the vitality of many bacteria, including important pathogens such as\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Vibrio cholerae<\/jats:named-content>\n            ,\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Vibrio parahaemolyticus<\/jats:named-content>\n            ,\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Haemophilus influenzae<\/jats:named-content>\n            ,\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Neisseria gonorrhoeae<\/jats:named-content>\n            ,\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Pasteurella multocida<\/jats:named-content>\n            ,\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Porphyromonas gingivalis<\/jats:named-content>\n            ,\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Enterobacter aerogenes<\/jats:named-content>\n            , and\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Yersinia pestis<\/jats:named-content>\n            . Production of Na\n            <jats:sup>+<\/jats:sup>\n            -NQR in bacteria requires Na\n            <jats:sup>+<\/jats:sup>\n            -NQR-specific maturation factors. We earlier identified one such factor (ApbE) that covalently attaches flavin residues to Na\n            <jats:sup>+<\/jats:sup>\n            -NQR. Here we identify the other protein factor, designated NqrM, and show that NqrM and ApbE suffice to produce functional Na\n            <jats:sup>+<\/jats:sup>\n            -NQR from the\n            <jats:named-content xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" content-type=\"genus-species\" xlink:type=\"simple\">Vibrio harveyi<\/jats:named-content>\n            <jats:italic>nqr<\/jats:italic>\n            operon. NqrM may be involved in Fe delivery to a unique Cys\n            <jats:sub>4<\/jats:sub>\n            [Fe] center during Na\n            <jats:sup>+<\/jats:sup>\n            -NQR assembly. Besides highlighting Na\n            <jats:sup>+<\/jats:sup>\n            -NQR biogenesis, these findings suggest a novel drug target to combat Na\n            <jats:sup>+<\/jats:sup>\n            -NQR-containing bacteria.\n          <\/jats:p>","DOI":"10.1128\/jb.00757-15","type":"journal-article","created":{"date-parts":[[2015,12,8]],"date-time":"2015-12-08T15:05:40Z","timestamp":1449587140000},"page":"655-663","update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":10,"title":["NqrM (DUF539) Protein Is Required for Maturation of Bacterial Na\n            <sup>+<\/sup>\n            -Translocating NADH:Quinone Oxidoreductase"],"prefix":"10.1128","volume":"198","author":[{"given":"Vitaly A.","family":"Kostyrko","sequence":"first","affiliation":[{"name":"Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yulia V.","family":"Bertsova","sequence":"additional","affiliation":[{"name":"Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marina V.","family":"Serebryakova","sequence":"additional","affiliation":[{"name":"Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alexander A.","family":"Baykov","sequence":"additional","affiliation":[{"name":"Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alexander V.","family":"Bogachev","sequence":"additional","affiliation":[{"name":"Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"235","reference":[{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2009.12.020"},{"key":"e_1_3_3_3_2","doi-asserted-by":"publisher","DOI":"10.1007\/400_2007_028"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10541-005-0093-4"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M311692200"},{"key":"e_1_3_3_6_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0005-2728(00)00275-9"},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6968.2007.01015.x"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1042\/bst0200577"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0014-5793(98)00016-7"},{"key":"e_1_3_3_10_2","doi-asserted-by":"publisher","DOI":"10.1016\/0014-5793(95)01164-A"},{"key":"e_1_3_3_11_2","doi-asserted-by":"publisher","DOI":"10.1016\/0014-5793(95)00283-F"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1021\/bi048689y"},{"key":"e_1_3_3_13_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.162361299"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature14003"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.1021\/bi991664s"},{"key":"e_1_3_3_16_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0014-5793(00)01595-7"},{"key":"e_1_3_3_17_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M113.455402"},{"key":"e_1_3_3_18_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2013.12.006"},{"key":"e_1_3_3_19_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00203-007-0254-5"},{"key":"e_1_3_3_20_2","doi-asserted-by":"publisher","DOI":"10.1016\/0378-1119(89)90358-2"},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.2144\/000113418"},{"key":"e_1_3_3_22_2","doi-asserted-by":"publisher","DOI":"10.1134\/S0006297911020040"},{"key":"e_1_3_3_23_2","doi-asserted-by":"publisher","DOI":"10.1021\/bi900524m"},{"key":"e_1_3_3_24_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0959-437X(99)00025-8"},{"key":"e_1_3_3_25_2","doi-asserted-by":"publisher","DOI":"10.1006\/jmbi.2000.4315"},{"key":"e_1_3_3_26_2","first-page":"166","article-title":"TMbase\u2014a database of membrane spanning proteins segments","volume":"347","author":"Hofmann K","year":"1993","unstructured":"Hofmann K, Stoffel W. 1993. 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