Extensive data in a wide range of organisms point to the importance of polyamine homeostasis for growth. The two most common polyamines found in bacteria are putrescine and spermidine. The investigation of polyamine function in bacteria has revealed that they are involved in a number of functions other than growth, which include incorporation into the cell wall and biosynthesis of siderophores. They are also important in acid resistance and can act as a free radical ion scavenger. More recently it has been suggested that polyamines play a potential role in signaling cellular differentiation in Proteus mirabilis. Polyamines have also been shown to be essential in biofilm formation in Yersinia pestis. The pleiotropic nature of polyamines has made their investigation difficult, particularly in discerning any specific effect from more global growth effects. Here we describe key developments in the investigation of the function of polyamines in bacteria that have revealed new roles for polyamines distinct from growth. We describe the bacterial genes necessary for biosynthesis and transport, with a focus on Y. pestis. Finally we review a novel role for polyamines in the regulation of biofilm development in Y. pestis and provide evidence that the investigation of polyamines in Y. pestis may provide a model for understanding the mechanism through which polyamines regulate biofilm formation.
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References
Balasundaram, D. and Tyagi, A.K. (1991) Polyamine--DNA nexus: structural ramifications and biological implications. Mol. Cell Biochem. 100, 129-140.
Brickman, T.J. and Armstrong, S.K. (1996) The ornithine decarboxylase gene odc is required for alcaligin siderophore biosynthesis in Bordetella spp.: putrescine is a precursor of alcaligin. J. Bacteriol. 178, 54-60.
Chattopadhyay, M.K., Tabor, C.W. and Tabor, H. (2003) Polyamines protect Escherichia coli cells from the toxic effect of oxygen. PNAS USA 100, 2261-2265.
Field, A.M., Rowatt, E. and Williams, R.J. (1989) The interaction of cations with lipopolysaccharide from Escherichia coli C as shown by measurement of binding constants and aggregation reactions. Biochem. J. 263, 695-702.
Foster, J.W. (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat. Rev. Microbiol. 2, 898-907.
Griffiths, G.L., Sigel, S.P., Payne, S.M. and Neilands, J.B. (1984) Vibriobactin, a siderophore from Vibrio cholerae. J. Biol. Chem. 259, 383-385.
Ha, H.C., Sirisoma, N.S., Kuppusamy, P., Zweier, J.L., Woster, P.M. and Casero, R.A., (1998) The natural polyamine spermine functions directly as a free radical scavenger. PNAS USA 95, 11140-11145.
Hackert, M.L., Carroll, D.W., Davidson, L., Kim, S.O., Momany, C., Vaaler, G.L. and Zhang, L. (1994) Sequence of ornithine decarboxylase from Lactobacillus sp. strain 30a. J. Bacteriol. 176, 7391-7394.
Hamana, K., Saito, T., Okada, M., Sakamoto, A. and Hosoya, R. (2002) Covalently linked polyamines in the cell wall peptidoglycan of Selenomonas, Anaeromusa, Dendrosporobacter, Acidaminococcus and Anaerovibrio belonging to the Sporomusa subbranch. J. Gen. Appl. Microbiol. 48, 177-180.
Hirao, T., Sato, M., Shirahata, A. and Kamio, Y. (2000) Covalent linkage of polyamines to peptidoglycan in Anaerovibrio lipolytica. J. Bacteriol. 182, 1154-1157.
Igarashi, K., Ito, K. and Kashiwagi, K. (2001) Polyamine uptake systems in Escherichia coli. Res. Microbiol. 152, 271-278.
Igarashi, K. and Kashiwagi, K. (1999) Polyamine transport in bacteria and yeast. Biochem. J. 344, 633-642.
Iyer, R., Williams, C. and Miller, C. (2003) Arginine-agmatine antiporter in extreme acid resistance in Escherichia coli. J. Bacteriol. 185, 6556-6561.
Jung, I.L., Oh, T.J. and Kim, I.G. (2003) Abnormal growth of polyamine-deficient Escherichia coli mutant is partially caused by oxidative stress-induced damage. Arch. Biochem. Biophys. 418, 125-132.
Kamio, Y. (1987) Structural specificity of diamines covalently linked to peptidoglycan for cell growth of Veillonella alcalescens and Selenomonas ruminantium. J. Bacteriol. 169, 4837-4840.
Kamio, Y. and Nakamura, K. (1987) Putrescine and cadaverine are constituents of peptidoglycan in Veillonella alcalescens and Veillonella parvula. J. Bacteriol. 169, 2881-2884.
Kamio, Y., Pösö, H., Terawaki, Y. and Paulin, L. (1986) Cadaverine covalently linked to a peptidoglycan is an essential constituent of the peptidoglycan necessary for the normal growth in Selenomonas ruminantium. J. Biol. Chem. 261, 6585-6589.
Karatan, E., Duncan, T.R. and Watnick, P.I. (2005) NspS, a Predicted Polyamine Sensor, Mediates Activation of Vibrio cholerae Biofilm Formation by Norspermidine. J. Bacteriol. 187, 7434-7443.
Kashiwagi, K., Kobayashi, H. and Igarashi, K. (1986) Apparently unidirectional polyamine transport by proton motive force in polyamine-deficient Escherichia coli. J. Bacteriol. 165, 972-977.
Kashiwagi, K., Shibuya, S., Tomitori, H., Kuraishi, A. and Igarashi, K. (1997) Excretion and uptake of putrescine by the PotE protein in Escherichia coli. J. Biol. Chem. 272, 6318-6323.
Koski, P. and Vaara, M. (1991) Polyamines as constituents of the outer membranes of Escherichia coli and Salmonella typhimurium. J. Bacteriol. 173, 3695-3699.
Lin, J., Smith, M.P., Chapin, K.C., Baik, H.S., Bennett, G.N. and Foster, J.W. (1996) Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl. Environ. Microbiol. 62, 3094-3100.
Lindemose, S., Nielsen, P.E. and Mollegaard, N.E. (2005) Polyamines preferentially interact with bent adenine tracts in double-stranded DNA. Nucleic Acids Res. 33, 1790-1803.
Litwin, C.M. and Calderwood, S.B. (1993) Role of iron in regulation of virulence genes. Clin. Microbiol. Rev. 6, 137-149.
Merrell, D.S. and Camilli, A. (2000) Regulation of Vibrio cholerae genes required for acid tolerance by a member of the “ToxR-like” family of transcriptional regulators. J. Bacteriol. 182, 5342-5350.
Miyamoto, S., Kashiwagi, K., Ito, K., Watanabe, S. and Igarashi, K. (1993) Estimation of polyamine distribution and polyamine stimulation of protein synthesis in Escherichia coli. Arch. Biochem. Biophys. 300, 63-68.
Mushegian, A.R. and Koonin, E.V. (1996) A minimal gene set for cellular life derived by comparison of complete bacterial genomes. PNAS 93, 10268-10273.
Nikaido, H. and Vaara, M. (1985) Molecular basis of bacterial outer membrane permeability. Microbiol. Rev. 49, 1-32.
Pastre, D., Pietrement, O., Landousy, F., Hamon, L., Sorel, I., David, M.O., Delain, E., Zozime, A. and Le Cam, E. (2006) A new approach to DNA bending by polyamines and its implication in DNA condensation. Eur. Biophys. J. 35, 214-223.
Patel, C.N., Wortham, B.W., Lines, J.L., Fetherston, J.D., Perry, R.D. and Oliveira, M.A. (2006) Polyamines are essential for the formation of plague biofilm. J. Bacteriol. 188, 2355-2363.
Polissi, A., Pontiggia, A., Feger, G., Altieri, M., Mottl, H., Ferrari, L. and Simon, D. (1998) Large-scale identification of virulence genes from Streptococcus pneumoniae. Infect. Immun. 66, 5620-5629.
Richard, H. and Foster, J.W. (2004) Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential. J. Bacteriol. 186, 6032-6041.
Samartzidou, H., Mehrazin, M., Xu, Z., Benedik, M.J. and Delcour, A.H. (2003) Cadaverine inhibition of porin plays a role in cell survival at acidic pH. J. Bacteriol. 185, 13-19.
Sandmeier, E., Hale, T.I. and Christen, P. (1994) Multiple evolutionary origin of pyridoxal-5'-phosphate-dependent amino acid decarboxylases. Eur. J. Biochem. 221, 997-1002.
Souzu, H. (1986) Fluorescence polarization studies on Escherichia coli membrane stability and its relation to the resistance of the cell to freeze-thawing. II. Stabilization of the membranes by polyamines. Biochim. Biophys. Acta 861, 361-367.
Stevenson, L.G. and Rather, P.N. (2006) A novel gene involved in regulating the flagellar gene cascade in Proteus mirabilis. J. Bacteriol. 188, 7830-7839.
Sturgill, G. and Rather, P.N. (2004) Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis. Mol. Microbiol. 51, 437-446.
Tabor, C.W. and Tabor, H. (1985) Polyamines in microorganisms. Microbiol. Rev. 49, 81-99.
Takatsuka, Y. and Kamio, Y. (2004) Molecular dissection of the Selenomonas ruminantium cell envelope and lysine decarboxylase involved in the biosynthesis of a polyamine covalently linked to the cell wall peptidoglycan layer. Biosci. Biotechnol. Biochem. 68, 1-19.
Terui, Y., Ohnuma, M., Hiraga, K., Kawashima, E. and Oshima, T. (2005) Stabilization of nucleic acids by unusual polyamines produced by an extreme thermophile, Thermus thermophilus. Biochem. J. 388, 427-433.
Tkachenko, A., Nesterova, L. and Pshenichnov, M. (2001) The role of the natural polyamine putrescine in defense against oxidative stress in Escherichia coli. Arch. Microbiol. 176, 155-157.
Vassylyev, D.G., Tomitori, H., Kashiwagi, K., Morikawa, K. and Igarashi, K. (1998) Crystal structure and mutational analysis of the Escherichia coli putrescine receptor. Structural basis for substrate specificity. J. Biol. Chem. 273, 17604-17609.
Wallace, H.M., Fraser, A.V. and Hughes, A. (2003) A perspective of polyamine metabolism. Biochem. J. 376, 1-14.
Ware, D., Jiang, Y., Lin, W. and Swiatlo, E. (2006) Involvement of potD in Streptococcus pneumoniae polyamine transport and pathogenesis. Infect. Immun. 74, 352-361.
Yoshida, M., Kashiwagi, K., Shigemasa, A., Taniguchi, S., Yamamoto, K., Makinoshima, H., Ishihama, A. and Igarashi, K. (2004) A unifying model for the role of polyamines in bacterial cell growth, the polyamine modulon. J. Biol. Chem. 279, 46008-46013.
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Wortham, B.W., Oliveira, M.A., Patel, C.N. (2007). Polyamines in Bacteria: Pleiotropic Effects yet Specific Mechanisms. In: Perry, R.D., Fetherston, J.D. (eds) The Genus Yersinia. Advances In Experimental Medicine And Biology, vol 603. Springer, New York, NY. https://doi.org/10.1007/978-0-387-72124-8_9
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