{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,26]],"date-time":"2026-01-26T00:18:37Z","timestamp":1769386717891,"version":"3.49.0"},"reference-count":33,"publisher":"Oxford University Press (OUP)","issue":"12","license":[{"start":{"date-parts":[[2016,10,2]],"date-time":"2016-10-02T00:00:00Z","timestamp":1475366400000},"content-version":"vor","delay-in-days":2334,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc\/2.0\/uk\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2010,6,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>An analysis of the distribution of the Na+-translocating ATPases\/ATP synthases among microbial genomes identified an atypical form of the F1Fo-type ATPase that is present in the archaea Methanosarcina barkeri and M.acetivorans, in a number of phylogenetically diverse marine and halotolerant bacteria and in pathogens Burkholderia spp. In complete genomes, representatives of this form (referred to here as N-ATPase) are always present as second copies, in addition to the typical proton-translocating ATP synthases. The N-ATPase is encoded by a highly conserved atpDCQRBEFAG operon and its subunits cluster separately from the equivalent subunits of the typical F-type ATPases. N-ATPase c subunits carry a full set of sodium-binding residues, indicating that most of these enzymes are Na+-translocating ATPases that likely confer on their hosts the ability to extrude Na+ ions. Other distinctive properties of the N-ATPase operons include the absence of the delta subunit from its cytoplasmic sector and the presence of two additional membrane subunits, AtpQ (formerly gene 1) and AtpR (formerly gene X). We argue that N-ATPases are an early-diverging branch of membrane ATPases that, similarly to the eukaryotic V-type ATPases, do not synthesize ATP.<\/jats:p>\n               <jats:p>Contact: \u00a0galperin@ncbi.nlm.nih.gov; amulkid@uos.de<\/jats:p>\n               <jats:p>Supplementary information: \u00a0Supplementary data are available at Bioinformatics online.<\/jats:p>","DOI":"10.1093\/bioinformatics\/btq234","type":"journal-article","created":{"date-parts":[[2010,5,15]],"date-time":"2010-05-15T00:17:52Z","timestamp":1273882672000},"page":"1473-1476","source":"Crossref","is-referenced-by-count":65,"title":["Characterization of the N-ATPase, a distinct, laterally transferred Na+-translocating form of the bacterial F-type membrane ATPase"],"prefix":"10.1093","volume":"26","author":[{"given":"Daria V.","family":"Dibrova","sequence":"first","affiliation":[{"name":"1 School of Physics, University of Osnabr\u00fcck, D-49069 Osnabr\u00fcck, Germany, 2 School of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992, Russia, 3 NCBI, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA and 4 A.N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow 119992, Russia"},{"name":"1 School of Physics, University of Osnabr\u00fcck, D-49069 Osnabr\u00fcck, Germany, 2 School of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992, Russia, 3 NCBI, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA and 4 A.N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow 119992, Russia"}]},{"given":"Michael Y.","family":"Galperin","sequence":"additional","affiliation":[{"name":"1 School of Physics, University of Osnabr\u00fcck, D-49069 Osnabr\u00fcck, Germany, 2 School of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992, Russia, 3 NCBI, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA and 4 A.N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow 119992, Russia"}]},{"given":"Armen Y.","family":"Mulkidjanian","sequence":"additional","affiliation":[{"name":"1 School of Physics, University of Osnabr\u00fcck, D-49069 Osnabr\u00fcck, Germany, 2 School of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992, Russia, 3 NCBI, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA and 4 A.N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow 119992, Russia"},{"name":"1 School of Physics, University of Osnabr\u00fcck, D-49069 Osnabr\u00fcck, Germany, 2 School of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992, Russia, 3 NCBI, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA and 4 A.N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow 119992, Russia"}]}],"member":"286","published-online":{"date-parts":[[2010,5,13]]},"reference":[{"key":"2023012508034148300_B1","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1093\/nar\/25.17.3389","article-title":"Gapped BLAST and PSI-BLAST\u2014a new generation of protein database search programs","volume":"25","author":"Altschul","year":"1997","journal-title":"Nucleic Acids Res."},{"key":"2023012508034148300_B2","doi-asserted-by":"crossref","first-page":"2543","DOI":"10.1128\/jb.176.9.2543-2550.1994","article-title":"\u0394\u03bcNa+drives the synthesis of ATP via an \u0394\u03bcNa+-translocating F1Fo-ATP synthase in membrane vesicles of the archaeon Methanosarcina mazei G\u00f61","volume":"176","author":"Becher","year":"1994","journal-title":"J. Bacteriol."},{"key":"2023012508034148300_B3","doi-asserted-by":"crossref","first-page":"1188","DOI":"10.1101\/gr.849004","article-title":"WebLogo: a sequence logo generator","volume":"14","author":"Crooks","year":"2004","journal-title":"Genome Res."},{"key":"2023012508034148300_B4","doi-asserted-by":"crossref","first-page":"D340","DOI":"10.1093\/nar\/gkp912","article-title":"The comprehensive microbial resource","volume":"38","author":"Davidsen","year":"2010","journal-title":"Nucleic Acids Res."},{"key":"2023012508034148300_B5","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/S0079-6107(02)00012-3","article-title":"Molecular evolution before the origin of species","volume":"79","author":"Davis","year":"2002","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"2023012508034148300_B6","doi-asserted-by":"crossref","first-page":"D211","DOI":"10.1093\/nar\/gkp985","article-title":"The Pfam protein families database","volume":"38","author":"Finn","year":"2010","journal-title":"Nucleic Acids Res."},{"key":"2023012508034148300_B7","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1038\/nrm2272","article-title":"Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology","volume":"8","author":"Forgac","year":"2007","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023012508034148300_B8","doi-asserted-by":"crossref","first-page":"8298","DOI":"10.1073\/pnas.1431443100","article-title":"Complete genome sequence of the marine planctomycete Pirellulasp. strain 1","volume":"100","author":"Gl\u00f6ckner","year":"2003","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023012508034148300_B9","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1007\/PL00006351","article-title":"The prokaryote-to-eukaryote transition reflected in the evolution of the V\/F\/A-ATPase catalytic and proteolipid subunits","volume":"46","author":"Hilario","year":"1998","journal-title":"J. Mol. Evol."},{"key":"2023012508034148300_B10","doi-asserted-by":"crossref","first-page":"D211","DOI":"10.1093\/nar\/gkn785","article-title":"InterPro: the integrative protein signature database","volume":"37","author":"Hunter","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"2023012508034148300_B11","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1006\/jmbi.2000.4315","article-title":"Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes","volume":"305","author":"Krogh","year":"2001","journal-title":"J. Mol. Biol."},{"key":"2023012508034148300_B12","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1093\/bib\/bbn017","article-title":"MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences","volume":"9","author":"Kumar","year":"2008","journal-title":"Brief. Bioinform."},{"key":"2023012508034148300_B13","doi-asserted-by":"crossref","first-page":"D205","DOI":"10.1093\/nar\/gkn845","article-title":"CDD: specific functional annotation with the Conserved Domain Database","volume":"37","author":"Marchler-Bauer","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"2023012508034148300_B14","doi-asserted-by":"crossref","first-page":"7600","DOI":"10.1073\/pnas.0610456104","article-title":"The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth","volume":"104","author":"McInerney","year":"2007","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023012508034148300_B15","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1126\/science.1111199","article-title":"Structure of the rotor ring of F-type Na+-ATPase from Ilyobacter tartaricus","volume":"308","author":"Meier","year":"2005","journal-title":"Science"},{"key":"2023012508034148300_B16","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1016\/j.jmb.2009.05.082","article-title":"Complete ion-coordination structure in the rotor ring of Na+-dependent F-ATP synthases","volume":"391","author":"Meier","year":"2009","journal-title":"J. Mol. Biol."},{"key":"2023012508034148300_B17","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1038\/nrmicro1767","article-title":"Inventing the dynamo machine: the evolution of the F-type and V-type ATPases","volume":"5","author":"Mulkidjanian","year":"2007","journal-title":"Nat. Rev. Microbiol."},{"key":"2023012508034148300_B18","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/1745-6150-3-13","article-title":"Evolutionary primacy of sodium bioenergetics","volume":"3","author":"Mulkidjanian","year":"2008","journal-title":"Biol. Direct"},{"key":"2023012508034148300_B19","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1016\/j.bbabio.2008.04.028","article-title":"The past and present of the sodium energetics: may the sodium-motive force be with you","volume":"1777","author":"Mulkidjanian","year":"2008","journal-title":"Biochim. Biophys. Acta"},{"key":"2023012508034148300_B20","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1016\/j.tibs.2009.01.005","article-title":"Co-evolution of primordial membranes and membrane proteins","volume":"34","author":"Mulkidjanian","year":"2009","journal-title":"Trends Biochem. Sci."},{"key":"2023012508034148300_B21","doi-asserted-by":"crossref","first-page":"654","DOI":"10.1126\/science.1110064","article-title":"Structure of the rotor of the V-type Na+-ATPase from Enterococcus hirae","volume":"308","author":"Murata","year":"2005","journal-title":"Science"},{"key":"2023012508034148300_B22","doi-asserted-by":"crossref","first-page":"3759","DOI":"10.1128\/JB.01279-06","article-title":"Degradation of alkyl methyl ketones by Pseudomonas veroniiMEK700","volume":"189","author":"Onaca","year":"2007","journal-title":"J. Bacteriol."},{"key":"2023012508034148300_B23","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1110\/ps.051958806","article-title":"Evolutionary links between FliH\/YscL-like proteins from bacterial type III secretion systems and second-stalk components of the FoF1 and vacuolar ATPases","volume":"15","author":"Pallen","year":"2006","journal-title":"Protein Sci."},{"key":"2023012508034148300_B24","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1111\/j.1574-6968.2007.00939.x","article-title":"The coupling ion in the methanoarchaeal ATP synthases: H+vs. Na+in the A1AoATP synthase from the archaeon Methanosarcina mazeiG\u00f61","volume":"277","author":"Pisa","year":"2007","journal-title":"FEMS Microbiol. Lett."},{"key":"2023012508034148300_B25","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1023\/A:1027339814544","article-title":"Sodium dependency of the photosynthetic electron transport in the alkaliphilic cyanobacterium Arthrospira platensis","volume":"35","author":"Pogoryelov","year":"2003","journal-title":"J. Bioenerg. Biomembr."},{"key":"2023012508034148300_B26","doi-asserted-by":"crossref","first-page":"D32","DOI":"10.1093\/nar\/gkn721","article-title":"NCBI reference sequences: current status, policy and new initiatives","volume":"37","author":"Pruitt","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"2023012508034148300_B27","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1111\/j.1574-6968.2009.01785.x","article-title":"The F1FoATP synthase genes in Methanosarcina acetivoransare dispensable for growth and ATP synthesis","volume":"300","author":"Saum","year":"2009","journal-title":"FEMS Microbiol. Lett."},{"key":"2023012508034148300_B28","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-642-72978-2","volume-title":"Membrane Bioenergetics.","author":"Skulachev","year":"1988"},{"key":"2023012508034148300_B29","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1006\/bbrc.1997.7809","article-title":"FoF1-ATPase genes from an archaebacterium Methanosarcina barkeri","volume":"241","author":"Sumi","year":"1997","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"2023012508034148300_B30","doi-asserted-by":"crossref","first-page":"20776","DOI":"10.1073\/pnas.0708075105","article-title":"The product of uncIgene in F1Fo-ATP synthase operon plays a chaperone-like role to assist c-ring assembly","volume":"104","author":"Suzuki","year":"2007","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023012508034148300_B31","doi-asserted-by":"crossref","first-page":"2005","DOI":"10.1073\/pnas.0709772105","article-title":"Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina","volume":"105","author":"Swingley","year":"2008","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023012508034148300_B32","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1146\/annurev.biophys.37.032807.130018","article-title":"Unique rotary ATP synthase and its biological diversity","volume":"37","author":"von Ballmoos","year":"2008","journal-title":"Annu. Rev. Biophys."},{"key":"2023012508034148300_B33","doi-asserted-by":"crossref","first-page":"3429","DOI":"10.1128\/jb.169.8.3429-3434.1987","article-title":"Sodium-coupled motility in a swimming cyanobacterium","volume":"169","author":"Willey","year":"1987","journal-title":"J. Bacteriol."}],"container-title":["Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/26\/12\/1473\/48855940\/bioinformatics_26_12_1473.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/26\/12\/1473\/48855940\/bioinformatics_26_12_1473.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,25]],"date-time":"2023-01-25T08:06:54Z","timestamp":1674634014000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article\/26\/12\/1473\/287511"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2010,5,13]]},"references-count":33,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2010,6,15]]}},"URL":"https:\/\/doi.org\/10.1093\/bioinformatics\/btq234","relation":{},"ISSN":["1367-4811","1367-4803"],"issn-type":[{"value":"1367-4811","type":"electronic"},{"value":"1367-4803","type":"print"}],"subject":[],"published-other":{"date-parts":[[2010,6,15]]},"published":{"date-parts":[[2010,5,13]]}}}