Home LiteratureArticle Details
PMID: 7832586 Published · ppublish English Journal Article Review

Bioenergetics: the evolution of molecular mechanisms and the development of bioenergetic concepts.

Antonie van Leeuwenhoek ·Vol. 65 ·No. 4 ·1994-00-00 ·Pages 271-84

Skulachev VP

Abstract

Possible routes for the evolution of cell energetics are considered. It is assumed that u.v. light was the primary energy source for the precursors of the primordial living cell and that primitive energetics might have been based on the use of the adenine moiety of ADP as the u.v. chromophore. It is proposed that the excitation of the adenine residue facilitated phosphorylation of its amino group with subsequent transfer of a phosphoryl group to the terminal phosphate of ADP to form ATP. ATP-driven carbohydrate synthesis is considered as a mechanism for storing u.v.-derived energy, which was then used in the dark. Glycolysis presumably produced compounds like ethanol and CO2, which easily penetrate the membrane and therefore were lost by the cell. Later lactate-producing glycolysis appeared, the end product being non-penetrant and, hence, retained inside the cell to be utilized to regenerate carbohydrates when light energy became available. Production of lactate was accompanied by accumulation of equimolar H+. To avoid acidification of the cell interior, an F0-type H+ channel was employed. Later it was supplemented with F1. This allowed the ATP energy to be used for 'uphill' H+ pumping to the medium, which was acidified due to glycolytic activity of the cells. In the subsequent course of evolution, u.v. light was replaced by visible light, which has lower energy but is less dangerous for the cell. It is assumed that bacteriorhodopsin, a simple and very stable light-driven H+ pump which still exists in halophilic and thermophilic Archaea, was the primary system utilizing visible light. The delta mu-H+ formed was used to reverse the H(+)-ATPase, which began to function as H(+)-ATP-synthase. Later, bacteriorhodopsin photosynthesis was substituted by a more efficient chlorophyll photosynthesis, producing not only ATP, but also carbohydrates. O2, a side product of this process, was consumed by the H(+)-motive respiratory chain to form delta mu-H+ in the dark. At the next stage of evolution, a parallel energy-transducing mechanism appeared which employed Na+ instead of H+ as the coupling ion (the Na+ cycle).(ABSTRACT TRUNCATED AT 400 WORDS)

MeSH Terms
Adenine/metabolism,radiation effects Bacteria/metabolism Biological Evolution Energy Metabolism Flagella/metabolism Glycolysis Models, Biological Molecular Biology Photosynthesis Proton-Translocating ATPases/metabolism Protons Sodium/metabolism Ultraviolet Rays
Chemicals
Protons Sodium Proton-Translocating ATPases Adenine
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Skulachev V P
Department of Bioenergetics, A.N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Russia.
References (57)
57 references, click to expand
  1. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy.
    J Mol Biol. 1990 Jun 20;213(4):899-929 PMID: 2359127
  2. A protonmotive force drives bacterial flagella.
    Proc Natl Acad Sci U S A. 1977 Jul;74(7):3060-4 PMID: 19741
  3. Bacterial motility and signal transduction.
    Cell. 1993 Apr 9;73(1):15-22 PMID: 8096433
  4. Motility in Bacillus subtilis driven by an artificial protonmotive force.
    FEBS Lett. 1977 Oct 15;82(2):187-90 PMID: 410660
  5. Structural determination of a cyclic metabolite of NAD+ with intracellular Ca2+-mobilizing activity.
    J Biol Chem. 1989 Jan 25;264(3):1608-15 PMID: 2912976
  6. Photosynthetic reaction centres: variations on a common structural theme?
    Trends Biochem Sci. 1991 Jul;16(7):241-5 PMID: 1926331
  7. Mutants of Streptococcus faecalis sensitive to alkaline pH lack Na(+)-ATPase.
    J Bacteriol. 1990 Apr;172(4):1732-5 PMID: 2138604
  8. Utilization of energy stored in the form of Na+ and K+ ion gradients by bacterial cells.
    Eur J Biochem. 1983 Aug 1;134(2):345-9 PMID: 6307692
  9. SYNTHESIS OF ADENOSINE TRIPHOSPHATE UNDER POSSIBLE PRIMITIVE EARTH CONDITIONS.
    Nature. 1963 Jul 20;199:222-6 PMID: 14076678
  10. Bioenergetic aspects of the translocation of macromolecules across bacterial membranes.
    Biochim Biophys Acta. 1994 Jan 4;1183(3):417-51 PMID: 8286395
  11. Chemomechanical coupling without ATP: the source of energy for motility and chemotaxis in bacteria.
    Proc Natl Acad Sci U S A. 1974 Apr;71(4):1239-43 PMID: 4598295
  12. Evolution of an ion-translocating ATPase.
    Ann N Y Acad Sci. 1992 Nov 30;671:257-72 PMID: 1337674
  13. Na+-driven flagellar motors of an alkalophilic Bacillus strain YN-1.
    J Biol Chem. 1983 Sep 10;258(17):10577-81 PMID: 6885795
  14. MECHANISMS FOR OXIDATIVE PHOSPHORYLATION AT THE PYRIDINE NUCLEOTIDE/FLAVOPROTEIN LEVEL.
    Nature. 1963 Aug 24;199:759-61 PMID: 14071183
  15. Adaptation of Bacillus FTU and Escherichia coli to alkaline conditions: the Na(+)-motive respiration.
    Biochim Biophys Acta. 1991 Dec 3;1098(1):95-104 PMID: 1751551
  16. Structure and cell envelope associations of flagellar basal complexes of Vibrio cholerae and Campylobacter fetus.
    Can J Microbiol. 1984 Mar;30(3):322-33 PMID: 6426766
  17. Transmembrane electrochemical H+-potential as a convertible energy source for the living cell.
    FEBS Lett. 1977 Feb 15;74(1):1-9 PMID: 14031
  18. Membrane ultrastructure of alkaliphilic Bacillus species studied by rapid-freeze electron microscopy.
    J Bacteriol. 1992 Aug;174(15):5123-6 PMID: 1629169
  19. Basal-body-associated disks are additional structural elements of the flagellar apparatus isolated from Wolinella succinogenes.
    J Bacteriol. 1989 May;171(5):2803-10 PMID: 2708319
  20. Potassium uniport and ATP synthesis in Halobacterium halobium.
    Eur J Biochem. 1978 Aug 15;89(1):169-79 PMID: 29755
  21. Evidence for a common structure for a class of membrane channels.
    Eur J Biochem. 1993 Apr 1;213(1):21-30 PMID: 7682941
  22. The sodium ion translocating adenosinetriphosphatase of Propionigenium modestum pumps protons at low sodium ion concentrations.
    Biochemistry. 1989 Sep 5;28(18):7194-8 PMID: 2554965
  23. The proton pump is a molecular engine of motile bacteria.
    Nature. 1978 Mar 16;272(5650):280-2 PMID: 24186
  24. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation.
    Biol Rev Camb Philos Soc. 1966 Aug;41(3):445-502 PMID: 5329743
  25. Gene to ultrastructure: the case of the flagellar basal body.
    J Bacteriol. 1993 Apr;175(8):2169-74 PMID: 8468277
  26. The happy family of cytochrome oxidases.
    Biochem Soc Trans. 1991 Aug;19(3):608-12 PMID: 1664390
  27. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism.
    Nature. 1961 Jul 8;191:144-8 PMID: 13771349
  28. Membrane-linked energy buffering as the biological function of Na+/K+ gradient.
    FEBS Lett. 1978 Mar 15;87(2):171-9 PMID: 344066
  29. The influence of some cations on an adenosine triphosphatase from peripheral nerves.
    Biochim Biophys Acta. 1957 Feb;23(2):394-401 PMID: 13412736
  30. Fine structure of Ectothiorhodospira mobilis Pelsh.
    J Bacteriol. 1968 Jun;95(6):2374-92 PMID: 5669908
  31. Na(+)-translocating NADH-quinone reductase of marine and halophilic bacteria.
    J Bioenerg Biomembr. 1993 Aug;25(4):385-91 PMID: 8226720
  32. TonB protein and energy transduction between membranes.
    J Bioenerg Biomembr. 1993 Dec;25(6):591-601 PMID: 8144488
  33. The bacterial energy-transducing NADH-quinone oxidoreductases.
    Biochim Biophys Acta. 1993 Feb 8;1141(1):1-17 PMID: 8435434
  34. Orphan enzyme or patriarch of a new tribe: the arsenic resistance ATPase of bacterial plasmids.
    Mol Microbiol. 1993 May;8(4):637-42 PMID: 8332056
  35. Studies of factors involved in oxidative phosphorylation.
    Proc Natl Acad Sci U S A. 1962 Sep 15;48:1659-63 PMID: 14489690
  36. Mechanisms of TonB-catalyzed iron transport through the enteric bacterial cell envelope.
    J Bioenerg Biomembr. 1993 Dec;25(6):603-11 PMID: 8144489
  37. Interrelations of bioenergetic and sensory functions of the retinal proteins.
    Q Rev Biophys. 1993 May;26(2):177-99 PMID: 8284350
  38. ATP-driven Na+ transport and Na(+)-dependent ATP synthesis in Escherichia coli grown at low delta mu H+.
    FEBS Lett. 1993 Feb 15;317(3):267-70 PMID: 8425616
  39. Involvement of a d-type oxidase in the Na(+)-motive respiratory chain of Escherichia coli growing under low delta mu H+ conditions.
    FEBS Lett. 1992 Jul 20;306(2-3):199-202 PMID: 1321735
  40. Study of the torque of the bacterial flagellar motor using a rotating electric field.
    Biophys J. 1993 Mar;64(3):925-33 PMID: 8471735
  41. Energy transduction in the thermophilic anaerobic bacterium Clostridium fervidus is exclusively coupled to sodium ions.
    Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):7975-9 PMID: 8367451
  42. Nobel lecture. The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis.
    EMBO J. 1989 Aug;8(8):2149-70 PMID: 2676514
  43. A soluble protein fraction required for coupling phosphorylation to oxidation in submitochondrial fragments of beef heart mitochondria.
    Arch Biochem Biophys. 1958 Jul;76(1):227-30 PMID: 13560032
  44. The sodium cycle. III. Vibrio alginolyticus resembles Vibrio cholerae and some other vibriones by flagellar motor and ribosomal 5S-RNA structures.
    Biochim Biophys Acta. 1986 Jul 23;850(3):466-72 PMID: 3730372
  45. Molecular mechanics of protonmotive F0F1 ATPases. Rolling well and turnstile hypothesis.
    FEBS Lett. 1985 Mar 11;182(1):1-7 PMID: 2857661
  46. Shared thematic elements in photochemical reaction centers.
    Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):1642-6 PMID: 8446577
  47. Recent advances in bacterial ion transport.
    Annu Rev Microbiol. 1986;40:263-86 PMID: 2430517
  48. Bacterial NADH-quinone oxidoreductases: iron-sulfur clusters and related problems.
    J Bioenerg Biomembr. 1993 Aug;25(4):347-56 PMID: 8226716
  49. The bacterial flagellum and flagellar motor: structure, assembly and function.
    Adv Microb Physiol. 1991;32:109-72 PMID: 1882727
  50. Effects of mot gene expression on the structure of the flagellar motor.
    J Mol Biol. 1988 Aug 5;202(3):575-84 PMID: 3050128
  51. Chemiosmotic systems in bioenergetics: H(+)-cycles and Na(+)-cycles.
    Biosci Rep. 1991 Dec;11(6):387-441; discussion 441-4 PMID: 1668527
  52. Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin.
    EMBO J. 1993 Jan;12(1):1-8 PMID: 8428572
  53. Release of flagellar filament-hook-rod complex by a Salmonella typhimurium mutant defective in the M ring of the basal body.
    J Bacteriol. 1989 Apr;171(4):2075-82 PMID: 2649485
  54. Sodium ion transport decarboxylases and other aspects of sodium ion cycling in bacteria.
    Microbiol Rev. 1987 Sep;51(3):320-40 PMID: 2444866
  55. Isotope and thermal effects in chemiosmotic coupling to the flagellar motor of Streptococcus.
    Cell. 1983 Mar;32(3):913-9 PMID: 6831561
  56. Location of the basal disk and a ringlike cytoplasmic structure, two additional structures of the flagellar apparatus of Wolinella succinogenes.
    J Bacteriol. 1992 Jan;174(1):263-8 PMID: 1370283
  57. Amplification of the Na+-ATPase of Streptococcus faecalis at alkaline pH.
    FEBS Lett. 1990 Feb 12;261(1):135-8 PMID: 2137787
Article Info
Journal
Antonie van Leeuwenhoek
Abbr.
Antonie Van Leeuwenhoek
ISSN
0003-6072
Published
1994-00-00
Pages
271-84
Language
English
Region
Netherlands
NLM ID
0372625
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com