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FOF1-ATPase mediates regulation of fermentation and energy metabolism at pH 5.5.

Λεπτομέρειες βιβλιογραφικής εγγραφής
Τίτλος: FOF1-ATPase mediates regulation of fermentation and energy metabolism at pH 5.5.
Συγγραφείς: Gevorgyan H; Department of Biochemistry, Microbiology and Biotechnology, Faculty of Biology, Yerevan State University, 0025, Yerevan, Armenia.; Scientific-Research Institute of Biology, Faculty of Biology, Yerevan State University, 1 A. Manoogian Str., 0025, Yerevan, Armenia.; Microbial Biotechnologies and Biofuel Innovation Center, Yerevan State University, 0025, Yerevan, Armenia., Trchounian K; Department of Biochemistry, Microbiology and Biotechnology, Faculty of Biology, Yerevan State University, 0025, Yerevan, Armenia. k.trchounian@ysu.am.; Scientific-Research Institute of Biology, Faculty of Biology, Yerevan State University, 1 A. Manoogian Str., 0025, Yerevan, Armenia. k.trchounian@ysu.am.; Microbial Biotechnologies and Biofuel Innovation Center, Yerevan State University, 0025, Yerevan, Armenia. k.trchounian@ysu.am.
Πηγή: Scientific reports [Sci Rep] 2025 Oct 14; Vol. 15 (1), pp. 35873. Date of Electronic Publication: 2025 Oct 14.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101563288 Publication Model: Electronic Cited Medium: Internet ISSN: 2045-2322 (Electronic) Linking ISSN: 20452322 NLM ISO Abbreviation: Sci Rep Subsets: MEDLINE
Imprint Name(s): Original Publication: London : Nature Publishing Group, copyright 2011-
Ιατρικοί όροι (MeSH): Escherichia coli*/metabolism , Escherichia coli*/enzymology , Escherichia coli*/genetics , Proton-Translocating ATPases*/metabolism , Proton-Translocating ATPases*/genetics , Escherichia coli Proteins*/metabolism , Escherichia coli Proteins*/genetics , Fermentation* , Energy Metabolism*, Glucose/metabolism ; Formates/metabolism ; Glycerol/metabolism ; Hydrogen/metabolism ; Hydrogen-Ion Concentration ; Proton-Motive Force
Περίληψη: The activity of FOF1-ATP synthase (FOF1) is vital for the survival and anaerobic growth under acidic conditions providing efficient metabolism and energy for cellular function. This study demonstrated the role of FOF1-ATPase in the metabolic pathways and regulation of proton motive force in Escherichia coli at pH 5.5 during the fermentation of glucose, glycerol and formate. Alteration of the ratio of fermentation end-products was shown. The possible mechanisms for efficient energy utilization in cells lacking FOF1 were shown. It is suggested that Fdh-H transfers H+ from formate to Hyd, which serves not only for H₂ generation but also for H+ cycling to FOF1 or directly to FOF1 in cells grown for 20 h. The interaction between H2 and H+ cycling was proposed as an essential mechanism for balancing ΔpH at acidic conditions. FOF1-ATPase was identified to play a pivotal role in forming both components of Δp at 20 h and 72 h.
(© 2025. The Author(s).)
Competing Interests: Declarations. Competing interests: The authors declare no competing interests.
References: J Bacteriol. 2000 Feb;182(3):620-6. (PMID: 10633094)
Biotechnol Bioeng. 2006 Aug 5;94(5):821-9. (PMID: 16715533)
Biol Pharm Bull. 2022;45(10):1404-1411. (PMID: 36184496)
Biochim Biophys Acta Bioenerg. 2023 Jan 1;1864(1):148919. (PMID: 36152681)
Microb Biotechnol. 2021 May;14(3):829-858. (PMID: 33438829)
Biosci Rep. 2000 Aug;20(4):277-88. (PMID: 11092250)
J Bacteriol. 1970 Mar;101(3):885-91. (PMID: 4908786)
Curr Microbiol. 2013 Jan;66(1):49-55. (PMID: 23053487)
Acta Physiol Scand. 1978 May;103(1):40-6. (PMID: 665258)
FEMS Microbiol Lett. 2022 Nov 25;369(1):. (PMID: 36370455)
J Bioenerg Biomembr. 2011 Dec;43(6):645-50. (PMID: 22081210)
FEBS Lett. 1999 Mar 26;447(2-3):144-8. (PMID: 10214935)
Microbiology (Reading). 2016 Sep;162(9):1672-1679. (PMID: 27488847)
Genes (Basel). 2020 Aug 25;11(9):. (PMID: 32854287)
Trends Biochem Sci. 2019 May;44(5):391-400. (PMID: 30655166)
Annu Rev Microbiol. 2013;67:65-81. (PMID: 23701194)
Nat Commun. 2020 Mar 20;11(1):1496. (PMID: 32198415)
PLoS One. 2010 Apr 12;5(4):e10132. (PMID: 20405029)
Cell Biochem Biophys. 2006;46(3):201-8. (PMID: 17272848)
Eur J Biochem. 1999 Jun;262(2):595-9. (PMID: 10336647)
FEMS Microbiol Rev. 2022 Nov 2;46(6):. (PMID: 35906711)
FEBS Lett. 2002 Apr 10;516(1-3):172-8. (PMID: 11959127)
Proc Natl Acad Sci U S A. 1974 Oct;71(10):3896-900. (PMID: 4279406)
Arch Biochem Biophys. 2024 May;755:109999. (PMID: 38621444)
Biophys Chem. 2005 May 1;115(1):55-61. (PMID: 15848284)
PLoS One. 2012;7(12):e52577. (PMID: 23300708)
J Bacteriol. 1974 Mar;117(3):1141-8. (PMID: 4205190)
IUBMB Life. 2020 May;72(5):915-921. (PMID: 31856407)
Anal Biochem. 1983 Apr 1;130(1):54-9. (PMID: 6346946)
IUBMB Life. 2021 Jun;73(6):883-892. (PMID: 33773019)
Biochim Biophys Acta Bioenerg. 2024 Apr 1;1865(2):149034. (PMID: 38354879)
Biochim Biophys Acta. 2012 Oct;1817(10):1711-21. (PMID: 22459334)
Biochimie. 2025 Sep;236:1-9. (PMID: 40516687)
IUBMB Life. 2018 Oct;70(10):1040-1047. (PMID: 30161297)
FEMS Microbiol Rev. 2014 Nov;38(6):1091-125. (PMID: 24898062)
Pharmacol Rev. 1972 Mar;24(1):67-157. (PMID: 4402043)
Microorganisms. 2024 Feb 01;12(2):. (PMID: 38399713)
Mol Microbiol. 1991 Nov;5(11):2807-14. (PMID: 1779767)
Adv Microb Physiol. 2009;55:1-79, 317. (PMID: 19573695)
J Exp Biol. 2000 Jan;203(Pt 1):89-95. (PMID: 10600677)
J Bacteriol. 2011 Jun;193(12):3072-7. (PMID: 21478347)
FEMS Microbiol Lett. 2001 Oct 16;204(1):61-4. (PMID: 11682179)
FEBS Lett. 1974 Jul 15;43(2):189-94. (PMID: 4277328)
J Biol Chem. 2010 Jun 4;285(23):17498-506. (PMID: 20299454)
Bacteriol Rev. 1977 Mar;41(1):100-80. (PMID: 860983)
J Bacteriol. 1991 Jan;173(2):687-96. (PMID: 1987159)
J Biol Chem. 1951 Nov;193(1):265-75. (PMID: 14907713)
Proc Natl Acad Sci U S A. 1979 Sep;76(9):4530-3. (PMID: 159458)
World J Microbiol Biotechnol. 2010 Jul;26(7):1181-6. (PMID: 24026921)
J Bacteriol. 1984 Dec;160(3):1055-60. (PMID: 6238948)
Grant Information: 23LCG-1F003 State Committee of Science
Contributed Indexing: Keywords: Acidic pH; FOF1-ATPase; Proton and hydrogen cycling; Proton conductance; Proton motive force; Proton permeability
Substance Nomenclature: EC 3.6.3.14 (Proton-Translocating ATPases)
IY9XDZ35W2 (Glucose)
0 (Formates)
PDC6A3C0OX (Glycerol)
0YIW783RG1 (formic acid)
7YNJ3PO35Z (Hydrogen)
0 (Escherichia coli Proteins)
Entry Date(s): Date Created: 20251014 Date Completed: 20251014 Latest Revision: 20251017
Update Code: 20260130
PubMed Central ID: PMC12521522
DOI: 10.1038/s41598-025-21047-w
PMID: 41087635
Βάση Δεδομένων: MEDLINE
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  – Url: https://dx.doi.org/doi:10.1038/s41598-025-21047-w
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PubType: Academic Journal
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  Label: Title
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  Data: F<subscript>O</subscript>F<subscript>1</subscript>-ATPase mediates regulation of fermentation and energy metabolism at pH 5.5.
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  Data: <searchLink fieldCode="AU" term="%22Gevorgyan+H%22">Gevorgyan H</searchLink>; Department of Biochemistry, Microbiology and Biotechnology, Faculty of Biology, Yerevan State University, 0025, Yerevan, Armenia.; Scientific-Research Institute of Biology, Faculty of Biology, Yerevan State University, 1 A. Manoogian Str., 0025, Yerevan, Armenia.; Microbial Biotechnologies and Biofuel Innovation Center, Yerevan State University, 0025, Yerevan, Armenia.<br /><searchLink fieldCode="AU" term="%22Trchounian+K%22">Trchounian K</searchLink>; Department of Biochemistry, Microbiology and Biotechnology, Faculty of Biology, Yerevan State University, 0025, Yerevan, Armenia. k.trchounian@ysu.am.; Scientific-Research Institute of Biology, Faculty of Biology, Yerevan State University, 1 A. Manoogian Str., 0025, Yerevan, Armenia. k.trchounian@ysu.am.; Microbial Biotechnologies and Biofuel Innovation Center, Yerevan State University, 0025, Yerevan, Armenia. k.trchounian@ysu.am.
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  Data: <searchLink fieldCode="JN" term="%22101563288%22">Scientific reports</searchLink> [Sci Rep] 2025 Oct 14; Vol. 15 (1), pp. 35873. <i>Date of Electronic Publication: </i>2025 Oct 14.
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  Data: <i>Publisher: </i><searchLink fieldCode="PB" term="%22Nature+Publishing+Group%22">Nature Publishing Group </searchLink><i>Country of Publication: </i>England <i>NLM ID: </i>101563288 <i>Publication Model: </i>Electronic <i>Cited Medium: </i>Internet <i>ISSN: </i>2045-2322 (Electronic) <i>Linking ISSN: </i><searchLink fieldCode="IS" term="%2220452322%22">20452322 </searchLink><i>NLM ISO Abbreviation: </i>Sci Rep <i>Subsets: </i>MEDLINE
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  Data: <i>Original Publication</i>: London : Nature Publishing Group, copyright 2011-
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  Data: <searchLink fieldCode="MM" term="%22Escherichia+coli%22">Escherichia coli*</searchLink>/<searchLink fieldCode="MM" term="%22Escherichia+coli+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Escherichia+coli%22">Escherichia coli*</searchLink>/<searchLink fieldCode="MM" term="%22Escherichia+coli+enzymology%22">enzymology</searchLink> <br /><searchLink fieldCode="MM" term="%22Escherichia+coli%22">Escherichia coli*</searchLink>/<searchLink fieldCode="MM" term="%22Escherichia+coli+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Proton-Translocating+ATPases%22">Proton-Translocating ATPases*</searchLink>/<searchLink fieldCode="MM" term="%22Proton-Translocating+ATPases+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Proton-Translocating+ATPases%22">Proton-Translocating ATPases*</searchLink>/<searchLink fieldCode="MM" term="%22Proton-Translocating+ATPases+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Escherichia+coli+Proteins%22">Escherichia coli Proteins*</searchLink>/<searchLink fieldCode="MM" term="%22Escherichia+coli+Proteins+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Escherichia+coli+Proteins%22">Escherichia coli Proteins*</searchLink>/<searchLink fieldCode="MM" term="%22Escherichia+coli+Proteins+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Fermentation%22">Fermentation*</searchLink> <br /><searchLink fieldCode="MM" term="%22Energy+Metabolism%22">Energy Metabolism*</searchLink><br /><searchLink fieldCode="MH" term="%22Glucose%22">Glucose</searchLink>/<searchLink fieldCode="MH" term="%22Glucose+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Formates%22">Formates</searchLink>/<searchLink fieldCode="MH" term="%22Formates+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Glycerol%22">Glycerol</searchLink>/<searchLink fieldCode="MH" term="%22Glycerol+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Hydrogen%22">Hydrogen</searchLink>/<searchLink fieldCode="MH" term="%22Hydrogen+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Hydrogen-Ion+Concentration%22">Hydrogen-Ion Concentration</searchLink> ; <searchLink fieldCode="MH" term="%22Proton-Motive+Force%22">Proton-Motive Force</searchLink>
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: The activity of F<subscript>O</subscript>F<subscript>1</subscript>-ATP synthase (F<subscript>O</subscript>F<subscript>1</subscript>) is vital for the survival and anaerobic growth under acidic conditions providing efficient metabolism and energy for cellular function. This study demonstrated the role of F<subscript>O</subscript>F<subscript>1</subscript>-ATPase in the metabolic pathways and regulation of proton motive force in Escherichia coli at pH 5.5 during the fermentation of glucose, glycerol and formate. Alteration of the ratio of fermentation end-products was shown. The possible mechanisms for efficient energy utilization in cells lacking F<subscript>O</subscript>F<subscript>1</subscript> were shown. It is suggested that Fdh-H transfers H<superscript>+</superscript> from formate to Hyd, which serves not only for H₂ generation but also for H<superscript>+</superscript> cycling to F<subscript>O</subscript>F<subscript>1</subscript> or directly to F<subscript>O</subscript>F<subscript>1</subscript> in cells grown for 20 h. The interaction between H<subscript>2</subscript> and H<superscript>+</superscript> cycling was proposed as an essential mechanism for balancing ΔpH at acidic conditions. F<subscript>O</subscript>F<subscript>1</subscript>-ATPase was identified to play a pivotal role in forming both components of Δp at 20 h and 72 h.<br /> (© 2025. The Author(s).)
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: Declarations. Competing interests: The authors declare no competing interests.
– Name: Ref
  Label: References
  Group: RefInfo
  Data: J Bacteriol. 2000 Feb;182(3):620-6. (PMID: <searchLink fieldCode="PM" term="%2210633094%22">10633094)</searchLink><br />Biotechnol Bioeng. 2006 Aug 5;94(5):821-9. (PMID: <searchLink fieldCode="PM" term="%2216715533%22">16715533)</searchLink><br />Biol Pharm Bull. 2022;45(10):1404-1411. (PMID: <searchLink fieldCode="PM" term="%2236184496%22">36184496)</searchLink><br />Biochim Biophys Acta Bioenerg. 2023 Jan 1;1864(1):148919. (PMID: <searchLink fieldCode="PM" term="%2236152681%22">36152681)</searchLink><br />Microb Biotechnol. 2021 May;14(3):829-858. (PMID: <searchLink fieldCode="PM" term="%2233438829%22">33438829)</searchLink><br />Biosci Rep. 2000 Aug;20(4):277-88. (PMID: <searchLink fieldCode="PM" term="%2211092250%22">11092250)</searchLink><br />J Bacteriol. 1970 Mar;101(3):885-91. (PMID: <searchLink fieldCode="PM" term="%224908786%22">4908786)</searchLink><br />Curr Microbiol. 2013 Jan;66(1):49-55. (PMID: <searchLink fieldCode="PM" term="%2223053487%22">23053487)</searchLink><br />Acta Physiol Scand. 1978 May;103(1):40-6. (PMID: <searchLink fieldCode="PM" term="%22665258%22">665258)</searchLink><br />FEMS Microbiol Lett. 2022 Nov 25;369(1):. (PMID: <searchLink fieldCode="PM" term="%2236370455%22">36370455)</searchLink><br />J Bioenerg Biomembr. 2011 Dec;43(6):645-50. (PMID: <searchLink fieldCode="PM" term="%2222081210%22">22081210)</searchLink><br />FEBS Lett. 1999 Mar 26;447(2-3):144-8. (PMID: <searchLink fieldCode="PM" term="%2210214935%22">10214935)</searchLink><br />Microbiology (Reading). 2016 Sep;162(9):1672-1679. (PMID: <searchLink fieldCode="PM" term="%2227488847%22">27488847)</searchLink><br />Genes (Basel). 2020 Aug 25;11(9):. (PMID: <searchLink fieldCode="PM" term="%2232854287%22">32854287)</searchLink><br />Trends Biochem Sci. 2019 May;44(5):391-400. (PMID: <searchLink fieldCode="PM" term="%2230655166%22">30655166)</searchLink><br />Annu Rev Microbiol. 2013;67:65-81. (PMID: <searchLink fieldCode="PM" term="%2223701194%22">23701194)</searchLink><br />Nat Commun. 2020 Mar 20;11(1):1496. (PMID: <searchLink fieldCode="PM" term="%2232198415%22">32198415)</searchLink><br />PLoS One. 2010 Apr 12;5(4):e10132. (PMID: <searchLink fieldCode="PM" term="%2220405029%22">20405029)</searchLink><br />Cell Biochem Biophys. 2006;46(3):201-8. (PMID: <searchLink fieldCode="PM" term="%2217272848%22">17272848)</searchLink><br />Eur J Biochem. 1999 Jun;262(2):595-9. (PMID: <searchLink fieldCode="PM" term="%2210336647%22">10336647)</searchLink><br />FEMS Microbiol Rev. 2022 Nov 2;46(6):. (PMID: <searchLink fieldCode="PM" term="%2235906711%22">35906711)</searchLink><br />FEBS Lett. 2002 Apr 10;516(1-3):172-8. (PMID: <searchLink fieldCode="PM" term="%2211959127%22">11959127)</searchLink><br />Proc Natl Acad Sci U S A. 1974 Oct;71(10):3896-900. (PMID: <searchLink fieldCode="PM" term="%224279406%22">4279406)</searchLink><br />Arch Biochem Biophys. 2024 May;755:109999. 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(PMID: <searchLink fieldCode="PM" term="%2222459334%22">22459334)</searchLink><br />Biochimie. 2025 Sep;236:1-9. (PMID: <searchLink fieldCode="PM" term="%2240516687%22">40516687)</searchLink><br />IUBMB Life. 2018 Oct;70(10):1040-1047. (PMID: <searchLink fieldCode="PM" term="%2230161297%22">30161297)</searchLink><br />FEMS Microbiol Rev. 2014 Nov;38(6):1091-125. (PMID: <searchLink fieldCode="PM" term="%2224898062%22">24898062)</searchLink><br />Pharmacol Rev. 1972 Mar;24(1):67-157. (PMID: <searchLink fieldCode="PM" term="%224402043%22">4402043)</searchLink><br />Microorganisms. 2024 Feb 01;12(2):. (PMID: <searchLink fieldCode="PM" term="%2238399713%22">38399713)</searchLink><br />Mol Microbiol. 1991 Nov;5(11):2807-14. (PMID: <searchLink fieldCode="PM" term="%221779767%22">1779767)</searchLink><br />Adv Microb Physiol. 2009;55:1-79, 317. (PMID: <searchLink fieldCode="PM" term="%2219573695%22">19573695)</searchLink><br />J Exp Biol. 2000 Jan;203(Pt 1):89-95. (PMID: <searchLink fieldCode="PM" term="%2210600677%22">10600677)</searchLink><br />J Bacteriol. 2011 Jun;193(12):3072-7. (PMID: <searchLink fieldCode="PM" term="%2221478347%22">21478347)</searchLink><br />FEMS Microbiol Lett. 2001 Oct 16;204(1):61-4. (PMID: <searchLink fieldCode="PM" term="%2211682179%22">11682179)</searchLink><br />FEBS Lett. 1974 Jul 15;43(2):189-94. (PMID: <searchLink fieldCode="PM" term="%224277328%22">4277328)</searchLink><br />J Biol Chem. 2010 Jun 4;285(23):17498-506. (PMID: <searchLink fieldCode="PM" term="%2220299454%22">20299454)</searchLink><br />Bacteriol Rev. 1977 Mar;41(1):100-80. (PMID: <searchLink fieldCode="PM" term="%22860983%22">860983)</searchLink><br />J Bacteriol. 1991 Jan;173(2):687-96. (PMID: <searchLink fieldCode="PM" term="%221987159%22">1987159)</searchLink><br />J Biol Chem. 1951 Nov;193(1):265-75. (PMID: <searchLink fieldCode="PM" term="%2214907713%22">14907713)</searchLink><br />Proc Natl Acad Sci U S A. 1979 Sep;76(9):4530-3. (PMID: <searchLink fieldCode="PM" term="%22159458%22">159458)</searchLink><br />World J Microbiol Biotechnol. 2010 Jul;26(7):1181-6. (PMID: <searchLink fieldCode="PM" term="%2224026921%22">24026921)</searchLink><br />J Bacteriol. 1984 Dec;160(3):1055-60. (PMID: <searchLink fieldCode="PM" term="%226238948%22">6238948)</searchLink>
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  Data: <i>Keywords: </i>Acidic pH; FOF1-ATPase; Proton and hydrogen cycling; Proton conductance; Proton motive force; Proton permeability
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        Value: 10.1038/s41598-025-21047-w
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      – Code: eng
        Text: English
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      Pagination:
        StartPage: 35873
    Subjects:
      – SubjectFull: Glucose metabolism
        Type: general
      – SubjectFull: Formates metabolism
        Type: general
      – SubjectFull: Glycerol metabolism
        Type: general
      – SubjectFull: Hydrogen metabolism
        Type: general
      – SubjectFull: Hydrogen-Ion Concentration
        Type: general
      – SubjectFull: Proton-Motive Force
        Type: general
      – SubjectFull: Escherichia coli metabolism
        Type: general
      – SubjectFull: Escherichia coli enzymology
        Type: general
      – SubjectFull: Escherichia coli genetics
        Type: general
      – SubjectFull: Proton-Translocating ATPases metabolism
        Type: general
      – SubjectFull: Proton-Translocating ATPases genetics
        Type: general
      – SubjectFull: Escherichia coli Proteins metabolism
        Type: general
      – SubjectFull: Escherichia coli Proteins genetics
        Type: general
      – SubjectFull: Fermentation
        Type: general
      – SubjectFull: Energy Metabolism
        Type: general
    Titles:
      – TitleFull: FOF1-ATPase mediates regulation of fermentation and energy metabolism at pH 5.5.
        Type: main
  BibRelationships:
    HasContributorRelationships:
      – PersonEntity:
          Name:
            NameFull: Gevorgyan H
      – PersonEntity:
          Name:
            NameFull: Trchounian K
    IsPartOfRelationships:
      – BibEntity:
          Dates:
            – D: 14
              M: 10
              Text: 2025 Oct 14
              Type: published
              Y: 2025
          Identifiers:
            – Type: issn-electronic
              Value: 2045-2322
          Numbering:
            – Type: volume
              Value: 15
            – Type: issue
              Value: 1
          Titles:
            – TitleFull: Scientific reports
              Type: main
ResultId 1