1887

Abstract

Polyamines constitute a group of organic polycations positively charged at physiological pH. They are involved in a large variety of biological processes, including the protection against physiological stress. In this study, we show that the genome of , a commensal bacterium of the intestine and the vagina and one of the most common agents responsible of neonate infections, does not encode proteins homologous to the specific enzymes involved in the known polyamine synthetic pathways. This lack of biosynthetic capability was verified experimentally by TLC analysis of the intracellular content of grown in the absence of polyamines. However, similar analyses showed that the polyamines spermidine, spermine and putrescine can be imported from the growth media into the bacteria. We found that all strains of possess the genes encoding the polyamine ABC transporter PotABCD. We demonstrated that these genes form an operon with , a gene involved in folate biosynthesis, , a gene involved in peptidoglycan biosynthesis, and with , a gene encoding a Cl/H antiporter involved in resistance to acid stress in . Transcription of the operon is induced by peroxide-induced oxidative stress but not by acidic stress. Spermidine and spermine were found to be inducers of transcription at pH 7.4 whereas putrescine induces this expression only during peroxide-induced oxidative stress. Using a deletion mutant of , we were nevertheless unable to associate phenotypic traits to the PotABCD transporter, probably due to the existence of one or more as yet identified transporters with a redundant action.

Funding
This study was supported by the:
  • INRAE- International Mobility Service
    • Principle Award Recipient: SarahKhazaal
  • Fondation Universitaire Rabelais (Tours, France)
    • Principle Award Recipient: SarahKhazaal
  • Lebanese Association for Scientific Research
    • Principle Award Recipient: SarahKhazaal
  • Azm and Saade Association
    • Principle Award Recipient: SarahKhazaal
  • 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.
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2021-12-15
2022-01-28
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References

  1. 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]
  2. Shah P, Swiatlo E. A multifaceted role for polyamines in bacterial pathogens. Mol Microbiol 2008; 68:4–16 [View Article] [PubMed]
    [Google Scholar]
  3. Chattopadhyay MK, Tabor CW, Tabor H. Polyamines protect Escherichia coli cells from the toxic effect of oxygen. Proc Natl Acad Sci USA 2003; 100:2261–2265 [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. 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]
  6. 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]
  7. Tabor CW, Tabor H. Polyamines in microorganisms. Microbiol Rev 1985; 49:81–99 [View Article] [PubMed]
    [Google Scholar]
  8. Igarashi K, Kashiwagi K. Polyamine transport in bacteria and yeast. Biochem J 1999; 344 Pt 3:633–642 [PubMed]
    [Google Scholar]
  9. Nakada Y, Itoh Y. Identification of the putrescine biosynthetic genes in Pseudomonas aeruginosa and characterization of agmatine deiminase and N-carbamoylputrescine amidohydrolase of the arginine decarboxylase pathway. Microbiology (Reading) 2003; 149:707–714 [View Article] [PubMed]
    [Google Scholar]
  10. Hanfrey CC, Pearson BM, Hazeldine S, Lee J, Gaskin DJ et al. Alternative spermidine biosynthetic route is critical for growth of Campylobacter jejuni and is the dominant polyamine pathway in human gut microbiota. J Biol Chem 2011; 286:43301–43312 [View Article] [PubMed]
    [Google Scholar]
  11. Potter AJ, Paton JC. Spermidine biosynthesis and transport modulate pneumococcal autolysis. J Bacteriol 2014; 196:3556–3561 [View Article] [PubMed]
    [Google Scholar]
  12. Applebaum DM, Dunlap JC, Morris DR. Comparison of the biosynthetic and biodegradative ornithine decarboxylases of Escherichia coli. Biochemistry 1977; 16:1580–1584 [View Article] [PubMed]
    [Google Scholar]
  13. Kallio A, McCann PP. Difluoromethylornithine irreversibly inactivates ornithine decarboxylase of Pseudomonas aeruginosa, but does not inhibit the enzymes of Escherichia coli. Biochem J 1981; 200:69–75 [View Article] [PubMed]
    [Google Scholar]
  14. Ohnuma M, Terui Y, Tamakoshi M, Mitome H, Niitsu M et al. N1-aminopropylagmatine, a new polyamine produced as a key intermediate in polyamine biosynthesis of an extreme thermophile, Thermus thermophilus. J Biol Chem 2005; 280:30073–30082 [View Article] [PubMed]
    [Google Scholar]
  15. Morimoto N, Fukuda W, Nakajima N, Masuda T, Terui Y et al. Dual biosynthesis pathway for longer-chain polyamines in the hyperthermophilic archaeon Thermococcus kodakarensis. J Bacteriol 2010; 192:4991–5001 [View Article] [PubMed]
    [Google Scholar]
  16. Lee J, Sperandio V, Frantz DE, Longgood J, Camilli A et al. An alternative polyamine biosynthetic pathway is widespread in bacteria and essential for biofilm formation in Vibrio cholerae. J Biol Chem 2009; 284:9899–9907 [View Article] [PubMed]
    [Google Scholar]
  17. Hamasaki-Katagiri N, Katagiri Y, Tabor CW, Tabor H. Spermine is not essential for growth of Saccharomyces cerevisiae: identification of the SPE4 gene (spermine synthase) and characterization of a spe4 deletion mutant. Gene 1998; 210:195–201 [View Article] [PubMed]
    [Google Scholar]
  18. Michael AJ. Polyamines in eukaryotes, bacteria, and archaea. J Biol Chem 2016; 291:14896–14903 [View Article] [PubMed]
    [Google Scholar]
  19. Liu W, Tan M, Zhang C, Xu Z, Li L et al. Functional characterization of murB-potABCD operon for polyamine uptake and peptidoglycan synthesis in Streptococcus suis. Microbiol Res 2018; 207:177–187 [View Article] [PubMed]
    [Google Scholar]
  20. Lombardo MJ, Miller CG, Rudd KE. Physical mapping of the Escherichia coli pepT and potABCD genes. J Bacteriol 1993; 175:7745–7746 [View Article] [PubMed]
    [Google Scholar]
  21. Kashiwagi K, Pistocchi R, Shibuya S, Sugiyama S, Morikawa K et al. Spermidine-preferential uptake system in Escherichia coli. Identification of amino acids involved in polyamine binding in PotD protein. J Biol Chem 1996; 271:12205–12208 [View Article] [PubMed]
    [Google Scholar]
  22. Kashiwagi K, Hosokawa N, Furuchi T, Kobayashi H, Sasakawa C et al. Isolation of polyamine transport-deficient mutants of Escherichia coli and cloning of the genes for polyamine transport proteins. J Biol Chem 1990; 265:20893–20897 [PubMed]
    [Google Scholar]
  23. Pistocchi R, Kashiwagi K, Miyamoto S, Nukui E, Sadakata Y et al. Characteristics of the operon for a putrescine transport system that maps at 19 minutes on the Escherichia coli chromosome. J Biol Chem 1993; 268:146–152 [View Article] [PubMed]
    [Google Scholar]
  24. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD et al. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 2001; 293:498–506 [View Article] [PubMed]
    [Google Scholar]
  25. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K et al. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 2002; 359:1819–1827 [View Article] [PubMed]
    [Google Scholar]
  26. Read TD, Peterson SN, Tourasse N, Baillie LW, Paulsen IT et al. The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 2003; 423:81–86 [View Article] [PubMed]
    [Google Scholar]
  27. Fléchard M, Gilot P, Héry-Arnaud G, Mereghetti L, Rosenau A. Analysis and identification of IS1548 insertion targets in Streptococcus agalactiae. FEMS Microbiol Lett 2013; 340:65–72 [View Article] [PubMed]
    [Google Scholar]
  28. Kashiwagi K, Innami A, Zenda R, Tomitori H, Igarashi K. The ATPase activity and the functional domain of PotA, a component of the sermidine-preferential uptake system in Escherichia coli. J Biol Chem 2002; 277:24212–24219 [View Article] [PubMed]
    [Google Scholar]
  29. 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]
  30. 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]
  31. Stoll BJ, Hansen NI, Sánchez PJ, Faix RG, Poindexter BB et al. Early onset neonatal sepsis: the burden of group B Streptococcal and E. coli disease continues. Pediatrics 2011; 127:817–826 [View Article] [PubMed]
    [Google Scholar]
  32. Phares CR, Lynfield R, Farley MM, Mohle-Boetani J, Harrison LH et al. Active bacterial core surveillance/emerging infections program network. Epidemiology of invasive group B streptococcal disease in the United States, 1999-2005. JAMA 2008; 299:2056–2065
    [Google Scholar]
  33. 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]
  34. Evans JJ, Bohnsack JF, Klesius PH, Whiting AA, Garcia JC et al. Phylogenetic relationships among Streptococcus agalactiae isolated from piscine, dolphin, bovine and human sources: a dolphin and piscine lineage associated with a fish epidemic in Kuwait is also associated with human neonatal infections in Japan. J Med Microbiol 2008; 57:1369–1376 [View Article] [PubMed]
    [Google Scholar]
  35. Sitkiewicz I, Green NM, Guo N, Bongiovanni AM, Witkin SS et al. Transcriptome adaptation of group B Streptococcus to growth in human amniotic fluid. PLoS One 2009; 4:e6114 [View Article] [PubMed]
    [Google Scholar]
  36. Gao X-Y, Zhi X-Y, Li H-W, Klenk H-P, Li W-J. Comparative genomics of the bacterial genus Streptococcus illuminates evolutionary implications of species groups. PLoS One 2014; 9:e101229 [View Article] [PubMed]
    [Google Scholar]
  37. Batista RP, Ferreira CR. Streptococcus agalactiae septicemia in a patient with diabetes and hepatic cirrhosis. Autops Case Rep 2015; 5:35–43 [View Article] [PubMed]
    [Google Scholar]
  38. 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 [View Article] [PubMed]
    [Google Scholar]
  39. Dulaney EL, Marx LM. A folig acid linked system in bacterial cell wall synthesis?. J Antibiot 1971; 24:713–714 [View Article]
    [Google Scholar]
  40. 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: [View Article] [PubMed]
    [Google Scholar]
  41. Ware D, Watt J, Swiatlo E. Utilization of putrescine by Streptococcus pneumoniae during growth in choline-limited medium. J Microbiol 2005; 43:398–405 [PubMed]
    [Google Scholar]
  42. Kamio Y, Nakamura K. Putrescine and cadaverine are constituents of peptidoglycan in Veillonella alcalescens and Veillonella parvula. J Bacteriol 1987; 169:2881–2884 [View Article] [PubMed]
    [Google Scholar]
  43. Hirao T, Sato M, Shirahata A, Kamio Y. Covalent linkage of polyamines to peptidoglycan in Anaerovibrio lipolytica. J Bacteriol 2000; 182:1154–1157 [View Article] [PubMed]
    [Google Scholar]
  44. Abeyrathne PD, Chami M, Stahlberg H. Biochemical and biophysical approaches to study the structure and function of the chloride channel (ClC) family of proteins. Biochimie 2016; 128–129:154–162 [View Article]
    [Google Scholar]
  45. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual CSHL Press; 2001
    [Google Scholar]
  46. 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]
  47. 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]
  48. 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]
  49. Pedrol N, Tiburcio FA. Polyamines determination by TLC and HPLC. Handbook of Plant Ecophysiology Techniques 2001; chapter 21:335–363
    [Google Scholar]
  50. Sekowska A, Coppée JY, Le Caer JP, Martin-Verstraete I, Danchin A. S-adenosylmethionine decarboxylase of Bacillus subtilis is closely related to archaebacterial counterparts. Mol Microbiol 2000; 36:1135–1147 [View Article] [PubMed]
    [Google Scholar]
  51. Swinscow TDV. Statistics at Square One, 4th edn. London: BMA; 1978
    [Google Scholar]
  52. Braibant M, Gilot P, Content J. The ATP binding cassette (ABC) transport systems of Mycobacterium tuberculosis. FEMS Microbiol Rev 2000; 24:449–467 [View Article] [PubMed]
    [Google Scholar]
  53. Shah P, Marquart M, Quin LR, Swiatlo E. Cellular location of polyamine transport protein PotD in Streptococcus pneumoniae. FEMS Microbiol Lett 2006; 261:235–237 [View Article] [PubMed]
    [Google Scholar]
  54. Shah P, Nanduri B, Swiatlo E, Ma Y, Pendarvis K. Polyamine biosynthesis and transport mechanisms are crucial for fitness and pathogenesis of Streptococcus pneumoniae. Microbiology (Reading) 2011; 157:504–515 [View Article] [PubMed]
    [Google Scholar]
  55. Vassylyev DG, Tomitori H, Kashiwagi K, Morikawa K, Igarashi K. Crystal structure and mutational analysis of the Escherichia coli putrescine receptor. J Biol Chem 1998; 273:17604–17609 [View Article]
    [Google Scholar]
  56. Naville M, Gautheret D. Transcription attenuation in bacteria: theme and variations. Brief Funct Genomics 2010; 9:178–189 [View Article] [PubMed]
    [Google Scholar]
  57. Rosinski-Chupin I, Sauvage E, Sismeiro O, Villain A, Da Cunha V et al. Single nucleotide resolution RNA-seq uncovers new regulatory mechanisms in the opportunistic pathogen Streptococcus agalactiae. BMC Genomics 2015; 16:419 [View Article] [PubMed]
    [Google Scholar]
  58. Ware D, Jiang Y, Lin W, Swiatlo E. Involvement of PotD in Streptococcus pneumoniae polyamine transport and pathogenesis. Infect Immun 2006; 74:352–361 [View Article] [PubMed]
    [Google Scholar]
  59. Nasrallah GK, Riveroll AL, Chong A, Murray LE, Lewis PJ et al. Legionella pneumophila requires polyamines for optimal intracellular growth. J Bacteriol 2011; 193:4346–4360 [View Article] [PubMed]
    [Google Scholar]
  60. Yoshida T, Sakamoto A, Terui Y, Takao K, Sugita Y et al. Effect of spermidine analogues on cell growth of Escherichia coli polyamine requiring mutant MA261. PLoS ONE 2016; 11:e0159494 [View Article]
    [Google Scholar]
  61. Joshi GS, Spontak JS, Klapper DG, Richardson AR. Arginine catabolic mobile element encoded speG abrogates the unique hypersensitivity of Staphylococcus aureus to exogenous polyamines. Mol Microbiol 2011; 82:9–20 [View Article] [PubMed]
    [Google Scholar]
  62. Rozansky R, Bachrach U, Grossowicz N. Studies on the antibacterial action of spermine. J Gen Microbiol 1954; 10:11–16 [View Article]
    [Google Scholar]
  63. Antognoni F, Del Duca S, Kuraishi A, Kawabe E, Fukuchi-Shimogori T et al. Transcriptional inhibition of the operon for the spermidine uptake system by the substrate-binding protein PotD. J Biol Chem 1999; 274:1942–1948 [View Article] [PubMed]
    [Google Scholar]
  64. Santi I, Grifantini R, Jiang S-M, Brettoni C, Grandi G et al. CsrRS regulates group B Streptococcus virulence gene expression in response to environmental pH: a new perspective on vaccine development. J Bacteriol 2009; 191:5387–5397 [View Article] [PubMed]
    [Google Scholar]
  65. Lamy M-C, Zouine M, Fert J, Vergassola M, Couve E et al. CovS/CovR of group B streptococcus: a two-component global regulatory system involved in virulence. Mol Microbiol 2004; 54:1250–1268 [View Article] [PubMed]
    [Google Scholar]
  66. Khan AU, Di Mascio P, Medeiros MH, Wilson T. Spermine and spermidine protection of plasmid DNA against single-strand breaks induced by singlet oxygen. Proc Natl Acad Sci USA 1992; 89:11428–11430 [View Article] [PubMed]
    [Google Scholar]
  67. Ha HC, Sirisoma NS, Kuppusamy P, Zweier JL, Woster PM et al. The natural polyamine spermine functions directly as a free radical scavenger. Proc Natl Acad Sci USA 1998; 95:11140–11145 [View Article] [PubMed]
    [Google Scholar]
  68. Kashiwagi K, Kobayashi H, Igarashi K. Apparently unidirectional polyamine transport by proton motive force in polyamine-deficient Escherichia coli. J Bacteriol 1986; 165:972–977 [View Article] [PubMed]
    [Google Scholar]
  69. Yao X, Lu C-D. Functional characterization of the potRABCD operon for spermine and spermidine uptake and regulation in Staphylococcus aureus. Curr Microbiol 2014; 69:75–81 [View Article] [PubMed]
    [Google Scholar]
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