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Polyphosphate Plays a Significant Role in the Maturation of Spores in Myxococcus xanthus

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Abstract

Myxococcus xanthus synthesizes polyphosphates (polyPs) with polyphosphate kinase 1 (Ppk1) and degrades short- and long-chain polyPs with the exopolyphosphatases, Ppx1 and Ppx2, respectively. M. xanthus polyP:AMP phosphotransferase (Pap) generates ADP from AMP and polyPs. Pap expression is induced by an elevation in intracellular polyP concentration. M. xanthus synthesized polyPs during the stationary phase; the ppk1 mutant died earlier than the wild-type strain after the stationary phase. In addition, M. xanthus cells cultured in phosphate-starved medium, H2O2-supplemented medium, or amino acid-deficient medium increased the intracellular polyP levels by six- to ninefold after 6 h of incubation. However, the growth of ppk1 and ppx2 mutants in phosphate-starved medium and H2O2-supplemented medium was not significantly different from that of wild-type strain, nor was there a significant difference in fruiting body formation and sporulation in starvation condition. During development, no difference was observed in the adenylate energy charge (AEC) values in the wild-type, ppk1 mutant, and pap mutant strains until the second day of development. However, after day 3, the ppk1 and pap mutants had a lower ADP ratio and a higher AMP ratio compared to wild-type strain, and as a result, the AEC values of these mutants were lower than those of the wild-type strain. Spores of ppk1 and pap mutants in the nutrient medium germinated later than those of the wild-type strain. These results suggested that polyPs produced during development may play an important role in cellular energy homeostasis of the spores by being used to convert AMP to ADP via Pap.

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References

  1. Kornberg A (1995) Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J Bacteriol 177:491–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Zhang H, Ishige K, Kornberg A (2002) A polyphosphate kinase (PPK2) widely conserved in bacteria. Proc Natl Acad Sci USA 99:16678–16683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hildenbrand JC, Teleki A, Jendrossek D (2020) A universal polyphosphate kinase: PPK2c of Ralstonia eutropha accepts purine and pyrimidine nucleotides including uridine diphosphate. Appl Microbiol Biotechnol 104:6659–6667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Ishige K, Noguchi T (2001) Polyphosphate:AMP Phosphotransferase and polyphosphate:ADP phosphotransferase activities of Pseudomonas aeruginosa. Biochem Biophys Res Commun 281:821–826

    Article  CAS  PubMed  Google Scholar 

  5. Akiyama M, Crooke E, Kornberg A (1993) An exopolyphosphatase of Escherichia coli. J Biol Chem 268:633–639

    Article  CAS  PubMed  Google Scholar 

  6. Kornberg A (1999) Inorganic polyphosphate: a molecule of many functions. Prog Mol Subcell Biol 23:1–18

    Article  CAS  PubMed  Google Scholar 

  7. Rashid MH, Rumbaugh K, Passador L, Davies DG, Hamood AN, Iglewski BH, Kornberg A (2000) Polyphosphate kinase is essential for biofilm development, quorum sensing, and virulence of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 97:9636–9641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Chen W, Palmer RJ, Kuramitsu HK (2002) Role of polyphosphate kinase in biofilm formation by Porphyromonas gingivalis. Infect Immun 70:4708–4715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Reusch RN, Sadoff HL (1988) Putative structure and functions of a poly-β-hydroxybutyrate/calcium polyphosphate channel in bacterial plasma membranes. Proc Natl Acad Sci USA 85:4176–4180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Nomura K, Kato J, Takiguchi N, Ohtake H, Kuroda A (2004) Effects of inorganic polyphosphate on the proteolytic and DNA-binding activities of Lon in Escherichia coli. J Biol Chem 279:34406–34410

    Article  CAS  PubMed  Google Scholar 

  11. Gray MJ, Wholey W-Y, Wagner NO, Cremers CM, Mueller-Schickert A, Hock NT, Krieger AG, Smith EM, Bender RA, Bardwell JCM, Jakob U (2014) Polyphosphate is a primordial chaperone. Mol Cell 53:689–699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Watson B, Dworkin M (1968) Comparative intermediary metabolism of vegetative cells and microcysts of Myxococcus xanthus. J Bacteriol 96:1456–1473

    Article  Google Scholar 

  13. Bretscher AP, Kaiser D (1978) Nutrition of Myxococcus xanthus, a fruiting myxobacterium. J Bacteriol 133:763–768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Youderian P, Lawes MC, Creighton C, Cook JC, Saier MH (1999) Mutations that confer resistance to 2-deoxyglucose reduce the specific activity of hexokinase from Myxococcus xanthus. J Bacteriol 181:2225–2235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Zhang H, Rao NN, Shiba T, Kornberg A (2005) Inorganic polyphosphate in the social life of Myxococcus xanthus: motility, development, and predation. Proc Natl Acad Sci USA 102:13416–13420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kamatani S, Takegawa K, Kimura Y (2018) Catalytic activity profile of polyphosphate kinase 1 from Myxococcus xanthus. Curr Microbiol 75:379–385

    Article  CAS  PubMed  Google Scholar 

  17. Kimura Y, Kamatani S (2021) Catalytic activity profile of polyP:AMP phosphotransferase from Myxococcus xanthus. J Biosci Bioeng 131:147–152

    Article  CAS  PubMed  Google Scholar 

  18. Harita D, Kanie K, Kimura Y (2021) Enzymatic properties of Myxococcus xanthus exopolyphosphatases mxPpx1 and mxPpx2. Biochim Biophys Acta-Proteins Proteom 1869(8):140660

    Article  CAS  PubMed  Google Scholar 

  19. Kimura Y, Kamimoto T, Tanaka N (2020) Enzymatic characteristics of a polyphosphate/ATP-NAD kinase, PanK, from Myxococcus xanthus. Curr Microbiol 77:173–178

    Article  CAS  PubMed  Google Scholar 

  20. Harita D, Nishida K, Kimura Y (2023) Synthesis and degradation of polyphosphate in Myxococcus xanthus. FEMS Microbiol Lett 370 fnad007

  21. Livermorea TM, Chubba JR, Saiardia A (2016) Developmental accumulation of inorganic polyphosphate affects germination and energetic metabolism in Dictyostelium discoideum. Proc Natl Acad Sci USA 113:996–1001

    Article  Google Scholar 

  22. Hodgkin J, Kaiser D (1977) Cell-to-cell stimulation of movement in non-motile mutants of Myxococcus. Proc Natl Acad Sci USA 74:2938–2942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hagan DC, Bretscher AP, Kaiser D (1978) Synergism between morphogenetic mutants of Myxococcus xanthus. Dev Biol 64:284–296

    Article  Google Scholar 

  24. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  25. Kimura Y, Yamamoto H, Kamatani S (2019) Enzymatic characteristics of two adenylate kinases, AdkA and AdkB, from Myxococcus xanthus. J Biochem 165:379–385

    Article  CAS  PubMed  Google Scholar 

  26. Rao NN, Liu S, Kornberg A (1998) Inorganic polyphosphate in Escherichia coli: the phosphate regulon and the stringent response. J Bacteriol 180:2186–2193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Shi X, Rao NN, Kornberg A (2002) Inorganic polyphosphate in Bacillus cereus: motility, biofilm formation, and sporulation. Proc Natl Acad Sci USA 101:17061–17065

    Article  Google Scholar 

  28. Atkinson DE (1977) Adenylate control and the adenylate energy charge in cellular energy metabolism and its regulation. Academic Press, New York, pp 85–107

    Book  Google Scholar 

  29. Kameda A, Shiba T, Kawazoe Y, Satoh Y, Ihara Y, Munekata M, Ishige K, Noguchi T (2001) A novel ATP regeneration system using polyphosphate-AMP phosphotransferase and polyphosphate kinase. J Biosci Bioeng 91:557–563

    Article  CAS  PubMed  Google Scholar 

  30. Lv H, Zhou Y, Liu B, Guan J, Zhang P, Deng X, Li D, Wanget J (2022) Polyphosphate kinase is required for the processes of virulence and persistence in Acinetobacter baumannii. Microbiol Spectr 10:e01230-e1322

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kimura Y, Yoshioka Y, Toshikuni K (2022) Physiological roles of catalases Cat1 and Cat2 in Myxococcus xanthus. J Microbiol 60:1168–1177

    Article  Google Scholar 

  32. Knowles JR (1980) Enzyme-catalyzed phosphoryl transfer reactions. Annu Rev Biochem 49:877–919

    Article  CAS  PubMed  Google Scholar 

  33. Atkinson DE, Walton GM (1967) Adenosine triphosphate conservation in metabolic regulation. Rat liver citrate cleavage enzyme. J Biol Chem 242:3239–3241

    Article  CAS  PubMed  Google Scholar 

  34. De La Fuente IM, Cortés JM, Valero E, Desroches M, Rodrigues S, Malaina I, Martínez L (2014) On the dynamics of the adenylate energy system: Homeorhesis vs homeostasis. PLoS ONE 9(10):e108676

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was supported by JSPS KAKENHI (Grant No.: JP19K05770).

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Authors and Affiliations

  1. Department of Applied Biological Science, Faculty of Agriculture, Kagawa University, Miki-cho, Kagawa, Japan

    Daiki Harita, Hiroka Matsukawa & Yoshio Kimura

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  1. Daiki Harita
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  2. Hiroka Matsukawa
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Contributions

DH and YK contributed to the conception and design of the project. DH and HM contributed to the acquisition, analysis, and interpretation of the data. The first draft of the manuscript was written by YK, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Yoshio Kimura.

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Harita, D., Matsukawa, H. & Kimura, Y. Polyphosphate Plays a Significant Role in the Maturation of Spores in Myxococcus xanthus. Curr Microbiol 81, 248 (2024). https://doi.org/10.1007/s00284-024-03778-7

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