1887

Microbiology Society logo

Volume 168, Issue 8

imports spermidine by a member of the amino acid/polyamine antiporter family to endure citric acid stress at the vaginal pH Open Access

Abstract

Polyamines bind to various cellular components, such as nucleic acids, phospholipids, proteins and nucleotides. They are involved in the virulence and protection against physiological stresses of several bacterial species. is able to colonize the vaginal tract of asymptomatic pregnant women and to resist, by an as yet poorly characterized mechanism, pH 4.0, the low physiological pH of this environment. We identified a transporter of the amino acid/polyamine antiporter family (SAK_1604 in strain A909) that shares 39.8 % similar amino acids with CadB and 34.7 % with PotE, two transporters implicated in acid resistance in . We found that is overexpressed in the presence of spermidine and during citric acid stress at the vaginal pH, but not during lactic acid or HCl stresses at the same pH or during a sodium citrate stress at pH 7.4. Dihydrogen citrate is the predominant form of citric acid at pH 4.0. Using a deletion mutant, we proved that SAK_1604 is involved in the survival of during citric acid stress at pH 4.0 in the presence of spermidine, and we showed by TLC analysis that it is involved in spermidine transport in these conditions. Our data open new perspectives on the comprehension of the molecular mechanisms allowing to survive at the physiological pH of the vagina and on the unsuspected role of an ionic form of citric acid.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): AdiC , CadB , dihydrogen citrate , polyamine , PotE and vagina
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001219
2022-08-03
2024-12-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/168/8/mic001219.html?itemId=/content/journal/micro/10.1099/mic.0.001219&mimeType=html&fmt=ahah

References

  1. Cohen S. A Guide to the Polyamines New York: Oxford University Press; 1998
     [Google Scholar]
  2. Tabor CW, Tabor H. Polyamines. Annu Rev Biochem 1984; 53:749–790 [View Article] [PubMed]
     [Google Scholar]
  3. Miyamoto S, Kashiwagi K, Ito K, Watanabe S, Igarashi K. Estimation of polyamine distribution and polyamine stimulation of protein synthesis in Escherichia coli. Arch Biochem Biophys 1993; 300:63–68 [View Article] [PubMed]
     [Google Scholar]
  4. Shah P, Romero DG, Swiatlo E. Role of polyamine transport in Streptococcus pneumoniae response to physiological stress and murine septicemia. Microb Pathog 2008; 45:167–172 [View Article] [PubMed]
     [Google Scholar]
  5. Hou MH, Lin SB, Yuann JM, Lin WC, Wang AH et al. Effects of polyamines on the thermal stability and formation kinetics of DNA duplexes with abnormal structure. Nucleic Acids Res 2001; 29:5121–5128 [View Article] [PubMed]
     [Google Scholar]
  6. Lee YH, Kim BH, Kim JH, Yoon WS, Bang SH et al. CadC has a global translational effect during acid adaptation in Salmonella enterica serovar Typhimurium. J Bacteriol 2007; 189:2417–2425 [View Article] [PubMed]
     [Google Scholar]
  7. Moreau PL. The lysine decarboxylase CadA protects Escherichia coli starved of phosphate against fermentation acids. J Bacteriol 2007; 189:2249–2261 [View Article] [PubMed]
     [Google Scholar]
  8. Shah P, Swiatlo E. A multifaceted role for polyamines in bacterial pathogens. Mol Microbiol 2008; 68:4–16 [View Article] [PubMed]
     [Google Scholar]
  9. Lancefield RC. A serological differentiation of human and other groups of hemolytic streptococci. J Exp Med 1933; 57:571–595 [View Article] [PubMed]
     [Google Scholar]
  10. Schuchat A. Epidemiology of group B streptococcal disease in the United States: shifting paradigms. Clin Microbiol Rev 1998; 11:497–513 [View Article] [PubMed]
     [Google Scholar]
  11. Phares CR, Lynfield R, Farley MM, Mohle-Boetani J, Harrison LH et al. Epidemiology of invasive group B streptococcal disease in the United States 1999-2005. JAMA 2008; 299:2056–2065
     [Google Scholar]
  12. Verani JR, McGee L, Schrag SJ. Division of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention (CDC) Prevention of perinatal group B streptococcal disease – revised guidelines from CDC, 2010. MMWR Recomm Rep 2010; 59:1–36 [PubMed]
     [Google Scholar]
  13. van der Mee-Marquet N, Domelier A-S, Salloum M, Violette J, Arnault L et al. Molecular characterization of temporally and geographically matched Streptococcus agalactiae strains isolated from food products and bloodstream infections. Foodborne Pathog Dis 2009; 6:1177–1183
     [Google Scholar]
  14. Khazaal S, Al Safadi R, Osman D, Hiron A, Gilot P. Investigation of the polyamine biosynthetic and transport capability of Streptococcus agalactiae: the non-essential PotABCD transporter. Microbiology 2021; 167:001124 [View Article] [PubMed]
     [Google Scholar]
  15. Igarashi K, Kashiwagi K. Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol Biochem 2010; 48:506–512 [View Article] [PubMed]
     [Google Scholar]
  16. Igarashi K, Kashiwagi K. Polyamine transport in Escherichia coli. Amino Acids 1996; 10:83–97 [View Article] [PubMed]
     [Google Scholar]
  17. Soksawatmaekhin W, Kuraishi A, Sakata K, Kashiwagi K, Igarashi K. Excretion and uptake of cadaverine by CadB and its physiological functions in Escherichia coli. Mol Microbiol 2004; 51:1401–1412 [View Article] [PubMed]
     [Google Scholar]
  18. Gao X, Zhou L, Jiao X, Lu F, Yan C et al. Mechanism of substrate recognition and transport by an amino acid antiporter. Nature 2010; 463:828–832 [View Article] [PubMed]
     [Google Scholar]
  19. Krammer E-M, Ghaddar K, André B, Prévost M. Unveiling the mechanism of arginine transport through AdiC with molecular dynamics simulations: the guiding role of aromatic residues. PLoS One 2016; 11:e0160219 [View Article] [PubMed]
     [Google Scholar]
  20. Krammer E-M, Prévost M. Function and regulation of acid resistance antiporters. J Membr Biol 2019; 252:465–481 [View Article] [PubMed]
     [Google Scholar]
  21. Khazaal S, Al Safadi R, Osman D, Hiron A, Gilot P. Dual and divergent transcriptional impact of IS1548 insertion upstream of the peptidoglycan biosynthesis gene murB of Streptococcus agalactiae. Gene 2019; 720:144094 [View Article] [PubMed]
     [Google Scholar]
  22. Sambrook J, Russell DW. Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 2001
     [Google Scholar]
  23. Dower WJ, Miller JF, Ragsdale CW. High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res 1988; 16:6127–6145 [View Article] [PubMed]
     [Google Scholar]
  24. Ricci ML, Manganelli R, Berneri C, Orefici G, Pozzi G. Electrotransformation of Streptococcus agalactiae with plasmid DNA. FEMS Microbiol Lett 1994; 119:47–52 [View Article] [PubMed]
     [Google Scholar]
  25. Biswas I, Gruss A, Ehrlich SD, Maguin E. High-efficiency gene inactivation and replacement system for gram-positive bacteria. J Bacteriol 1993; 175:3628–3635 [View Article] [PubMed]
     [Google Scholar]
  26. Poyart C, Trieu-Cuot P. A broad-host-range mobilizable shuttle vector for the construction of transcriptional fusions to beta-galactosidase in gram-positive bacteria. FEMS Microbiol Lett 1997; 156:193–198 [View Article] [PubMed]
     [Google Scholar]
  27. Pedrol N, Tiburcio F. A. Polyamines determination by TLC and HPLC. In Handbook of Plant Ecophysiology Techniques Kluwer: Dordrecht; 2001 pp 335–363 [View Article]
     [Google Scholar]
  28. Swinscow TDV. Statistics at Square One, 4th edn. London: BMA; 1978
     [Google Scholar]
  29. Tomitori H, Kashiwagi K, Igarashi K. Structure and function of polyamine-amino acid antiporters CadB and PotE in Escherichia coli. Amino Acids 2012; 42:733–740 [View Article] [PubMed]
     [Google Scholar]
  30. Kitko RD, Wilks JC, Garduque GM, Slonczewski JL. Osmolytes contribute to pH homeostasis of Escherichia coli. PLoS One 2010; 5:e10078 [View Article] [PubMed]
     [Google Scholar]
  31. Elbagerma MA, Alajtal AI, Edwards HGM, Azimi GH, Verma KD et al. Raman spectroscopic and potentiometric studies of acidity level and dissociation of citric acid in aqueous solution. J Appl Chem Sci Int 2015; 2:1–11
     [Google Scholar]
  32. Gavella M. A simple automated method for determination of citric acid levels in semen. Int J Androl 1983; 6:585–591 [View Article] [PubMed]
     [Google Scholar]
  33. Martin PD, Cheshire SK. A comparative study of the citrate and lactate concentrations in stains from semen, vaginal secretion and mixtures of the two using isotachophoresis. In Brinkmann B, Henningsen K. eds 11th Congress of the Society for Forensic Haemogenetics (Gesellschaft Für Forensische Blutgruppenkunde e.V.), Advances in Forensic Haemogenetics Berlin, Heidelberg: Springer; 1986 pp 299–303
     [Google Scholar]
  34. Sinha DP, Drury AR, Conner GH. The in vitro effect of citric acid and sodium citrate on Streptococcus agalactiae in milk. Indian Vet J 1968; 45:805–810 [PubMed]
     [Google Scholar]
  35. Nagaoka S, Murata S, Kimura K, Mori T, Hojo K. Antimicrobial activity of sodium citrate against Streptococcus pneumoniae and several oral bacteria. Lett Appl Microbiol 2010; 51:546–551 [View Article] [PubMed]
     [Google Scholar]
  36. Zhao B, Houry WA. Acid stress response in enteropathogenic gammaproteobacteria: an aptitude for survival. Biochem Cell Biol 2010; 88:301–314 [View Article] [PubMed]
     [Google Scholar]
  37. Zabiszak M, Nowak M, Taras-Goslinska K, Kaczmarek MT, Hnatejko Z et al. Carboxyl groups of citric acid in the process of complex formation with bivalent and trivalent metal ions in biological systems. J Inorg Biochem 2018; 182:37–47 [View Article] [PubMed]
     [Google Scholar]
  38. Nelson TM, Borgogna J-L, Brotman RM, Ravel J, Walk ST et al. Vaginal biogenic amines: biomarkers of bacterial vaginosis or precursors to vaginal dysbiosis?. Front Physiol 2015; 6:253 [View Article] [PubMed]
     [Google Scholar]
  39. Scheu PD, Witan J, Rauschmeier M, Graf S, Liao Y-F et al. CitA/CitB two-component system regulating citrate fermentation in Escherichia coli and its relation to the DcuS/DcuR system in vivo. J Bacteriol 2012; 194:636–645 [View Article] [PubMed]
     [Google Scholar]
  40. Glaser P, Rusniok C, Buchrieser C, Chevalier F, Frangeul L et al. Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol Microbiol 2002; 45:1499–1513 [View Article] [PubMed]
     [Google Scholar]
  41. Igarashi K, Sugawara K, Izumi I, Nagayama C, Hirose S. Effect of polyamines of polyphenylalanine synthesis by Escherichia coli and rat-liver ribosomes. Eur J Biochem 1974; 48:495–502 [View Article] [PubMed]
     [Google Scholar]
  42. Ito K, Igarashi K. The increase by spermidine of fidelity of protamine synthesis in a wheat-germ cell-free system. Eur J Biochem 1986; 156:505–510 [View Article] [PubMed]
     [Google Scholar]
  43. Yoshida M, Meksuriyen D, Kashiwagi K, Kawai G, Igarashi K. Polyamine stimulation of the synthesis of oligopeptide-binding protein (OppA). Involvement of a structural change of the Shine-Dalgarno sequence and the initiation codon AUG in OppA mRNA. J Biol Chem 1999; 274:22723–22728 [View Article] [PubMed]
     [Google Scholar]
  44. Kabir A, Suresh Kumar G. Binding of the biogenic polyamines to deoxyribonucleic acids of varying base composition: base specificity and the associated energetics of the interaction. PLoS One 2013; 8:e70510 [View Article] [PubMed]
     [Google Scholar]
  45. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci USA 2005; 102:13950–13955 [View Article] [PubMed]
     [Google Scholar]
/content/journal/micro/10.1099/mic.0.001219
Loading
Streptococcus agalactiae imports spermidine by a member of the amino acid/polyamine antiporter family to endure citric acid stress at the vaginal pH
Microbiology 168, 001219 (2022); https://doi.org/10.1099/mic.0.001219
/content/journal/micro/10.1099/mic.0.001219
/content/journal/micro/10.1099/mic.0.001219
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error