Features of Betaine Reduction by Haloalkaliphilic Bacteria Alkaliphilus peptidifermentans during Growth on Amino Acids and Ethanolamine

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Resumo

The ability of the haloalkaliphilic anaerobic bacterium Alkaliphilus peptidifermentans Z-7036T to utilize betaine in oxidation-reduction reactions as an electron acceptor was studied. During growth on serine/threonine, a previously unknown molar stoichiometric ratio with betaine of 1 : 2 was revealed. To explain this phenomenon, a pathway for the degradation of these amino acids was proposed and the sites of conjugation with the betaine reductase complex were determined. The activities of key enzymes of threonine and serine metabolism were measured. The Stickland reaction with betaine for proline and ornithine was demonstrated for the first time and a rationale for its implementation was proposed. Biochemical mechanisms were revealed that make it possible to reduce betaine during growth on ethanolamine. Based on the genome annotation, schemes of metabolic pathways for the degradation of threonine, serine, proline, glutamate, arginine, ornithine and ethanolamine were constructed. For all used substrates, the exchange products were determined and stoichiometric ratios with betaine and products were obtained.

Sobre autores

Yu. Boltyanskaya

S. N. Winogradsky Institute of Microbiology, FRC “Fundamentals of Biotechnology” of the RAS

Moscow, Russia

E. Detkova

S. N. Winogradsky Institute of Microbiology, FRC “Fundamentals of Biotechnology” of the RAS

Moscow, Russia

I. Oshkin

S. N. Winogradsky Institute of Microbiology, FRC “Fundamentals of Biotechnology” of the RAS

Moscow, Russia

S. Parshina

S. N. Winogradsky Institute of Microbiology, FRC “Fundamentals of Biotechnology” of the RAS

Moscow, Russia

N. Pimenov

S. N. Winogradsky Institute of Microbiology, FRC “Fundamentals of Biotechnology” of the RAS

Moscow, Russia

V. Kevbrin

S. N. Winogradsky Institute of Microbiology, FRC “Fundamentals of Biotechnology” of the RAS

Email: kevbrin@inmi.ru
Moscow, Russia

Bibliografia

  1. Болтянская Ю.В., Деткова Е.Н., Шумский А.Н., Дулов Л.Е., Пушева М.А. Осмоадаптация у представителей галоалкалофильных бактерий из содовых озер // Микробиология. 2005. Т. 74. С. 738–744.
  2. Boltyanskaya Yu.V., Detkova E.N., Shumskii A.N., Dulov L.E., Pusheva M.A. Osmoadaptation in representatives of haloalkaliphilic bacteria from soda lakes // Microbiology (Moscow). 2005. V. 75. P. 640–645.
  3. Деткова Е.Н., Болтянская Ю.В., Кевбрин В.В. Деградация глицинбетаина в реакции Стикленда галоалкалофильной бактерией Halonatronomonas betaini, выделенной из содового озера Танатар III // Микробиология. 2022. Т. 91. С. 720–725.
  4. Detkova E.N., Boltyanskaya Y.V., Kevbrin V.V. Glycine betaine degradation via the Stickland reaction by a haloalkaliphilic bacterium Halonatronomonas betaini isolated from the Tanatar III soda lake // Microbiology (Moscow). 2022. V. 91. P. 721–726.
  5. Деткова Е.Н., Болтянская Ю.В., Пименов Н.В., Марданов А.В., Кевбрин В.В. Анализ генома и реконструкция метаболических путей деградации аминокислот и бетаина у галоалкалофильной бактерии Anoxynatronum sibiricum // Микробиология. 2024. Т. 93. С. 702–714.
  6. Detkova E.N., Boltyanskaya Yu.V., Pimenov N.V., Mardanov A.V., Kevbrin V.V. Genome analysis and reconstruction of metabolic pathways of amino acid and betaine degradation in the haloalkaliphilic bacterium Anoxynatronum sibiricum // Microbiology (Moscow). 2024. V. 93. P. 748–760.
  7. Жилина Т.Н., Заварзина Д.Г., Колганова Т.В., Лысенко А.М., Турова Т.П. Alkaliphilus peptidofermentans sp. nov., новая алкалофильная бактерия из содового озера, сбраживающая пептиды и восстанавливающая Fe (III) // Микробиология. 2009. Т. 78. С. 496–505.
  8. Zhilina T.N., Zavarzina D.G., Kolganova T.V., Lysenko A.M., Tourova T.P. Alkaliphilus peptidofermentans sp. nov., a new alkaliphilic bacterial soda lake isolate capable of peptide fermentation and Fe(III) reduction // Microbiology (Moscow). 2009. V. 78. P. 445–454.
  9. Ahn A.-C., Jongepier E., Schuurmans J.M., Rijpstra W.I.C., Damsté J.S.S., Galinski E.A., Roman P., Sorokin D., Muyzer G. Molecular and physiological adaptations to low temperature in Thioalkalivibrio strains isolated from soda lakes with different temperature regimes // mSystems. 2021. V. 6. Art. e01202-20.
  10. Alain K., Pignet P., Zbinden M., Quillevere M., Duchiron F., Donval J.P., Lesongeur F., Raguenes G., Crassous P., Querellou J., Cambon-Bonavita M.A. Caminicella sporogenes gen. nov., sp. nov., a novel thermophilic spore-forming bacterium isolated from an East-Pacific Rise hydrothermal vent // Int. J. Syst. Evol. Microbiol. 2002. V. 52. P. 1621–1628.
  11. Alvarez-Coque M.C., Hernandez M.J., Camanas R.M., Fernandez C. Studies on the formation and stability of isoindoles derived from amino acids, o-phthalaldehyde and N-acetyl-L-cysteine // Anal. Biochem. 1989. V. 180. P. 172–176.
  12. Andreesen J.R. Glycine reductase mechanism // Curr. Opin. Chem. Biol. 2004. V. 8. P. 454–461.
  13. Blackwell C.M., Scarlett F.A., Turner J.M. Ethanolamine catabolism by bacteria, including Escherichia coli // Biochem. Soc. Trans. 1976. V. 4. P. 495–497.
  14. Bes M., Merrouch M., Joseph M., Quéméneur M., Payri C., Pelletier B., Ollivier B., Fardeau M.-L., Erauso G., Postec A. Acetoanaerobium pronyense sp. nov., an anaerobic alkaliphilic bacterium isolated from a carbonate chimney of the Prony Hydrothermal Field (New Caledonia) // Int. J. Syst. Evol. Microbiol. 2015. V. 65. P. 2574–2580.
  15. Boltyanskaya Y., Zhilina T., Grouzdev D., Detkova E., Pimenov N., Kevbrin V. Halanaerobium polyolivorans sp. nov. – a novel halophilic alkalitolerant bacterium capable of polyol degradation: physiological properties and genomic insights // Microorganisms. 2023. V. 11. Art. 2325.
  16. Buckel W. Unusual enzymes involved in five pathways of glutamate fermentation // Appl. Microbiol. Biotechnol. 2001. V. 57. P. 263–273.
  17. Chang A., Jeske L., Ulbrich S., Hofmann J., Koblitz J., Schomburg I., Neumann-Schaal M., Jahn D., Schomburg D. BRENDA, the ELIXIR core data resource in 2021: new developments and updates // Nucl. Acids Res. 2021. V. 49. P. D498–D508.
  18. Fan C., Bobik T.A. The PduX enzyme of Salmonella enterica is an L-threonine kinase used for coenzyme B12 synthesis // J. Biol. Chem. 2008. V. 283. P. 11322–11329.
  19. Feijó Delgado F., Cermak N., Hecht V.C., Son S., Li Y., Knudsen S.M., Olcum S., Higgins J.M., Chen J., Grover W.H., Manalis S.R. Intracellular water exchange for measuring the dry mass, water mass and changes in chemical composition of living cells // PLoS One. 2013. V. 8. Art. e67590.
  20. Fernandez M., Zúñiga M. Amino acid catabolic pathways of lactic acid bacteria // Crit. Rev. Microbiol. 2006. V. 32. P. 155–183.
  21. Fonknechten N., Perret A., Perchat N., Tricot S., Lechaplais C., Vallenet D., Vergne C., Zaparucha A., Le Paslier D., Weissenbach J., Salanoubat M. A conserved gene cluster rules anaerobic oxidative degradation of L-ornithine // J. Bacteriol. 2009. V. 191. P. 3162–3167.
  22. Galinski E.A. Osmoadaptation in bacteria // Adv. Microb. Physiol. 1995. V. 37. P. 273–328.
  23. Gunde-Cimerman N., Plemenitaš A., Oren A. Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations // FEMS Microbiol. Rev. 2018. V. 42. P. 353–373.
  24. Halsey C.R., Lei Sh., Wax J.K., Lehman M.K., Nuxoll A.S., Steinke L., Sadykov M., Powers R., Fey P.D. Amino acid catabolism in Staphylococcus aureus and the function of carbon catabolite repression // mBio. 2017. V. 8. Art. e01434-16. https://doi.org/10.1128/mBio.01434-16
  25. Imhoff J.F., Rodriguez-Valera F. Betaine is the main compatible solute of halophilic eubacteria // J Bacteriol. 1984. V. 160. P. 478–479.
  26. Kanehisa M., Sato Y., Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences // J. Mol. Biol. 2016. V. 428. P. 726–731.
  27. Kerfeld C., Aussignargues C., Zarzycki J., Cai F., Sutter M. Bacterial microcompartments // Nat. Rev. Microbiol. 2018. V. 16. P. 277–290.
  28. Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms // Mol. Biol. Evol. 2018. V. 35. P. 1547–1549.
  29. Larson T.J., Ehrmann M., Boos W. Periplasmic glycerophosphodiester phosphodiesterase of Escherichia coli, a new enzyme of the glp regulon // J. Biol. Chem. 1983. V. 258. P. 5428–5432.
  30. Mouné S., Manac’h N., Hirschler A., Caumette P., Willison J.C., Matheron R. Haloanaerobacter salinarius sp. nov., a novel halophilic fermentative bacterium that reduces glycine-betaine to trimethylamine with hydrogen or serine as electron donors; emendation of the genus Haloanaerobacter // Int. J. Syst. Bacteriol. 1999. V. 1. P. 103–112.
  31. Naumann E., Hippe H., Gottschalk G. Betaine: new oxidant in the Stickland reaction and methanogenesis from betaine and L-alanine by a Clostridium sporogenes – Methanosarcina barkeri coculture // Appl. Environ. Microbiol. 1983. V. 45. P. 474–483.
  32. Olson R.D., Assaf R., Brettin T., Conrad N., Cucinell C., Davis J.J., Dempsey D.M., Dickerman A., Dietrich E.M., Kenyon R.W., Kuscuoglu M., Lefkowitz E.J., Lu J., Machi D., Macken C., Mao C., Niewiadomska A., Nguyen M., Olsen G.J., Overbeek J.C., Parrello B., Parrello V., Porter J.S., Pusch G.D., Shukla M., Singh I., Stewart L., Tan G., Thomas C., Van Oeffelen M., Vonstein V., Wallace Z.S., Warren A.S., Wattam A.R., Xia F., Yoo H., Zhang Y., Zmasek C.M., Scheuermann R.H., Stevens R.L. Introducing the bacterial and viral bioinformatics resource center (BV-BRC): a resource combining PATRIC, IRD and ViPR // Nucl. Acids Res. 2023. V. 51. P. D678–D689.
  33. Parshina S.N., Kleerebezem R., Sanz J.L., Lettinga G., Nozhevnikova A.N., Kostrikina N.A., Lysenko A.M., Stams A.J.M. Soehngenia saccharolytica gen. nov., sp. nov. and Clostridium amygdalinum sp. nov., two novel anaerobic, benzaldehyde-converting bacteria // Int. J. Syst. Evol. Microbiol. 2003. V. 53 P. 1791–1799.
  34. Pavao A., Graham M., Arrieta-Ortiz M.L., Immanuel S.R.C., Baliga N.S., Bry L. Reconsidering the in vivo functions of clostridial Stickland amino acid fermentations // Anaerobe. 2022. V. 76. Art. 102600.
  35. Pols T., Singh S., Deelman-Driessen C., Gaastra B.F., Poolman B. Enzymology of the pathway for ATP production by arginine breakdown // FEBS J. 2021. V. 288. P. 293–309.
  36. Roeßler M., Müller V. Osmoadaptation in bacteria and archaea: common principles and differences // Environ. Microbiol. 2001. V. 3. P. 743–754.
  37. Sangavai C, Chellapandi P. Amino acid catabolism-directed biofuel production in Clostridium sticklandii: an insight into model-driven systems engineering // Biotechnol. Rep. 2017. V. 16. P. 32–43.
  38. Sangavai C, Chellapandi P. Growth‐associated catabolic potential of Acetoanaerobium sticklandii DSM 519 on gelatin and amino acids // J. Basic Microbiol. 2020. V. 60. P. 817‒915.
  39. Sawers G. The anaerobic degradation of L-serine and L-threonine in enterobacteria: networks of pathways and regulatory signals // Arch. Microbiol. 1998. V. 171. P. 1–5.
  40. Smiddy M., Sleator R.D., Patterson M.F., Hill C., Kelly A.L. Role for compatible solutes glycine betaine and L-carnitine in listerial barotolerance // Appl. Environ. Microbiol. 2004. V. 70. P. 7555–7557.

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