Characterization of the N-ATPase, a distinct, laterally transferred Na+-translocating form of the bacterial F-type membrane ATPase
Open accessAbstract
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. Contact: galperin@ncbi.nlm.nih.gov; amulkid@uos.de Supplementary information: Supplementary data are available at Bioinformatics online.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Only three members of a single archaeal lineage, Methanosarcinales, contain F-type ATP synthases in addition to their A/V-type complex.
“Conversely, only three members of a single archaeal lineage, Methanosarcinales, contain F-type ATP synthases in addition to their A/V-type complex”
From ATP synthase evolution on a cross-braced dated tree of life (2023) · cites this paper as [56]
Results §3.1 identifies F-type N-ATPase operons alongside A-type ATPases in two archaea, Methanosarcina barkeri and M. acetivorans. Results §3.2 says the operon was not found in the sequenced genome of the third, M. mazei, although it discusses earlier functional evidence for a second ATPase there. The Discussion also predicts that N-ATPases do not synthesize ATP, so the claim overstates both the count and their designation as ATP synthases. (LLM, conf=0.90)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Pfam protein families database
Finn, R. D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J. E., Gavin, O. L., Gunasekaran, P., Ceric, G., Forslund, K., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkp985 · Cited by 2,694 · see citing works
NCBI Reference Sequences: current status, policy and new initiatives
Pruitt, K. D., Tatusova, T., Klimke, W., & Maglott, D. R. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkn721 · Cited by 736 · cited 5× · see citing works
“1475 [16:25 12/5/2010 Bioinformatics-btq234.tex] Page: 1476 1473–1476 This separate branching suggests a possible early divergence of the N-ATPases, which is compatible with the following, supposedly ancestral traits of these enzymes: (i) Both AtpFN subunit of the N-ATPase and the E subunit of the peripheral stalk of…”
BackgroundInfluentialInventing the dynamo machine: the evolution of the F-type and V-type ATPases
Mulkidjanian, A. Y., Makarova, K. S., Galperin, M. Y., & Koonin, E. V. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1767 · Cited by 210 · see citing works
Self-citationCo-evolution of primordial membranes and membrane proteins
Mulkidjanian, A. Y., Galperin, M. Y., & Koonin, E. V. (2009) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2009.01.005 · Cited by 169 · see citing works
Self-citationEvolutionary primacy of sodium bioenergetics
Mulkidjanian, A. Y., Galperin, M. Y., Makarova, K. S., Wolf, Y. I., & Koonin, E. V. (2008) · Biology Direct · doi:10.1186/1745-6150-3-13 · Cited by 163 · see citing works
Self-citationF0F1-ATPase Genes from an Archaebacterium,Methanosarcina barkeri
Sumi, M., Yohda, M., Koga, Y., & Yoshida, M. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.7809 · Cited by 21 · see citing works
Saum, R., Schlegel, K., Meyer, B., & Müller, V. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01785.x · Cited by 15 · see citing works
Flagged first, then by citations
Research works printed but not linked: 27
- Altschul SF Gapped BLAST and PSI-BLAST—a new generation of protein database search programs Nucleic Acids Res. 1997 25 3389 3402 9254694 PMC146917
- Becher B Müller V ΔμNa+drives the synthesis of ATP via an ΔμNa+-translocating F1Fo-ATP synthase in membrane vesicles of the archaeon Methanosarcina mazei Gö1 J. Bacteriol. 1994 176 2543 2550 8169202 PMC205391
- Crooks GE WebLogo: a sequence logo generator Genome Res. 2004 14 1188 1190 15173120 PMC419797
- Davidsen T The comprehensive microbial resource Nucleic Acids Res. 2010 38 D340 D345 19892825 PMC2808947
- Davis BK Molecular evolution before the origin of species Prog. Biophys. Mol. Biol. 2002 79 77 133 12225777
- Forgac M Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology Nat. Rev. Mol. Cell Biol. 2007 8 917 929 17912264
- Glöckner FO Complete genome sequence of the marine planctomycete Pirellulasp. strain 1 Proc. Natl Acad. Sci. USA 2003 100 8298 8303 12835416 PMC166223
- Hilario E Gogarten JP The prokaryote-to-eukaryote transition reflected in the evolution of the V/F/A-ATPase catalytic and proteolipid subunits J. Mol. Evol. 1998 46 703 715 9608053
- Hunter S InterPro: the integrative protein signature database Nucleic Acids Res. 2009 37 D211 D215 18940856 PMC2686546
- Krogh A Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes J. Mol. Biol. 2001 305 567 580 11152613
- Kumar S MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences Brief. Bioinform. 2008 9 299 306 18417537 PMC2562624
- Marchler-Bauer A CDD: specific functional annotation with the Conserved Domain Database Nucleic Acids Res. 2009 37 D205 D210 18984618 PMC2686570
- McInerney MJ The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth Proc. Natl Acad. Sci. USA 2007 104 7600 7605 17442750 PMC1863511
- Meier T Structure of the rotor ring of F-type Na+-ATPase from Ilyobacter tartaricus Science 2005 308 659 662 15860619
- Meier T Complete ion-coordination structure in the rotor ring of Na+-dependent F-ATP synthases J. Mol. Biol. 2009 391 498 507 19500592
- Mulkidjanian AY The past and present of the sodium energetics: may the sodium-motive force be with you Biochim. Biophys. Acta 2008b 1777 985 992 18485887 PMC2695506
- Murata T Structure of the rotor of the V-type Na+-ATPase from Enterococcus hirae Science 2005 308 654 659 15802565
- Onaca C Degradation of alkyl methyl ketones by Pseudomonas veroniiMEK700 J. Bacteriol. 2007 189 3759 3767 17351032 PMC1913341
- Pallen MJ Evolutionary links between FliH/YscL-like proteins from bacterial type III secretion systems and second-stalk components of the FoF1 and vacuolar ATPases Protein Sci. 2006 15 935 941 16522800 PMC2242474
- Pisa KY The coupling ion in the methanoarchaeal ATP synthases: H+vs. Na+in the A1AoATP synthase from the archaeon Methanosarcina mazeiGö1 FEMS Microbiol. Lett. 2007 277 56 63 17986085
- Pogoryelov D Sodium dependency of the photosynthetic electron transport in the alkaliphilic cyanobacterium Arthrospira platensis J. Bioenerg. Biomembr. 2003 35 427 437 14740891
- Saum R The F1FoATP synthase genes in Methanosarcina acetivoransare dispensable for growth and ATP synthesis FEMS Microbiol. Lett. 2009 300 230 236 19796137
- Skulachev VP Membrane Bioenergetics. 1988 Berlin Springer
- Suzuki T The product of uncIgene in F1Fo-ATP synthase operon plays a chaperone-like role to assist c-ring assembly Proc. Natl Acad. Sci. USA 2007 104 20776 20781 18083842 PMC2410078
- Swingley WD Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina Proc. Natl Acad. Sci. USA 2008 105 2005 2010 18252824 PMC2538872
- von Ballmoos C Unique rotary ATP synthase and its biological diversity Annu. Rev. Biophys. 2008 37 43 64 18573072
- Willey JM Sodium-coupled motility in a swimming cyanobacterium J. Bacteriol. 1987 169 3429 3434 3112121 PMC212413
Cited by
Sorted by citations
ATP synthase evolution on a cross-braced dated tree of life
Mahendrarajah, T. A., Moody, E. R. R., Schrempf, D., Szánthó, L. L., Dombrowski, N., Davín, A. A., Pisani, D., Donoghue, P. C. J., Szöllősi, G. J., Williams, T. A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42924-w · Cited by 86 · see citing works
“In this scenario, the evolution of the membrane components could have occurred later, potentially in conjunction with the speciation of Bacteria and Archaea and the ‘ lipid divide ’ 36,79 .”
BackgroundLipid Droplets Mediate Salt Stress Tolerance in <i>Parachlorella kessleri</i> 1
You, Z., Zhang, Q., Peng, Z., & Miao, X. (2019) · Plant Physiology · doi:10.1104/pp.19.00666 · Cited by 87 · see citing works
- Authors
- Dibrova, D. V., Galperin, M. Y., & Mulkidjanian, A. Y.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Galperin, Michael Y.
- Mulkidjanian, Armen Y.
- Venue
- Bioinformatics
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-05-13
- Volume
- 26
- Issue
- 12
- Pages
- 1473-1476
- ISSN
- 1367-4803 (ISSN-L)
- 1367-4811
- PMC
- PMC2881411
- OpenAlex
- W2148380033
- Cited by
- 70
- References
- 7
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 6 · 2022: 6 · 2021: 3 · 2020: 8 · 2019: 5 · 2018: 3 · 2017: 4 · 2016: 6 · 2015: 4 · 2014: 1 · 2013: 7 · 2012: 9
- FWCI
- 2.48
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Bioinformatics (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- Deutscher Akademischer Austauschdienst
- Deutsche Forschungsgemeinschaft
- National Institutes of Health (Z99 LM999999)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
- Keywords
- horizontal gene transfer, archaea, Methanosarcina, halotolerant bacteria, Burkholderia, atp operon, delta subunit, V-type ATPase
- MeSH terms
- Adenosine Triphosphatases, Bacterial Proteins, Genome, Bacterial, Cation Transport Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
