Abstract
In Bacteria, the pathways of polyamine biosynthesis start with the amino acids l-lysine, l-ornithine, l-arginine, or l-aspartic acid. Some of these polyamines are of special interest due to their use in the production of engineering plastics (e.g., polyamides) or as curing agents in polymer applications. At present, the polyamines for industrial use are mainly synthesized on chemical routes. However, since a commercial market for polyamines as well as an industry for the fermentative production of amino acid exist, and since bacterial strains overproducing the polyamine precursors l-lysine, l-ornithine, and l-arginine are known, it was envisioned to engineer these amino acid-producing strains for polyamine production. Only recently, researchers have investigated the potential of amino acid-producing strains of Corynebacterium glutamicum and Escherichia coli for polyamine production. This mini-review illustrates the current knowledge of polyamine metabolism in Bacteria, including anabolism, catabolism, uptake, and excretion. The recent advances in engineering the industrial model bacteria C. glutamicum and E. coli for efficient production of the most promising polyamines, putrescine (1,4-diaminobutane), and cadaverine (1,5-diaminopentane), are discussed in more detail.
References
Applebaum DM, Dunlap JC, Morris DR (1977) Comparison of the biosynthetic and biodegradative ornithine decarboxylases of Escherichia coli. Biochemistry 16:1580–1584
Applebaum D, Sabo DL, Fischer EH, Morris DR (1975) Biodegradative ornithine decarboxylase of Escherichia coli. Purification, properties, and pyridoxal 5′-phosphate binding site. Biochemistry 14:3675–3681
Bachrach U (1962a) Formation of pyrroline and propane diamine from spermidine by extracts of Serratia marcescens. Nature 194:377–378
Bachrach U (1962b) Spermidine oxidase from Serratia marcescens. J Biol Chem 237:3443–3448
Bellmann A, Vrljic M, Patek M, Sahm H, Krämer R, Eggeling L (2001) Expression control and specificity of the basic amino acid exporter LysE of Corynebacterium glutamicum. Microbiology 147:1765–1774
Blethen SL, Boeker EA, Snell EE (1968) Arginine decarboxylase from Escherichia coli I. Purification and specificity for substrates and coenzyme. J Biol Chem 243:1671–1677
Bowman WH, Tabor CW, Tabor H (1973) Spermidine biosynthesis. Purification and properties of propylamine transferase from Escherichia coli. J Biol Chem 248:2480–2486
Brickman TJ, Armstrong SK (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
Buschke N, Schröder H, Wittmann C (2011) Metabolic engineering of Corynebacterium glutamicum for production of 1,5-diaminopentane from hemicellulose. Biotechnol J 6:306–317
Cacciapuoti G, Porcelli M, Moretti MA, Sorrentino F, Concilio L, Zappia V, Liu Z, Tempel W, Schubot F, Rose JP, Wang B, Brereton PS, Jenney FE, Adams MWW (2007) The first agmatine/cadaverine aminopropyl transferase: biochemical and structural characterization of an enzyme involved in polyamine biosynthesis in the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 189:6057–6067
Chattopadhyay MK, Tabor CW, Tabor H (2009) Polyamines are not required for aerobic growth of Escherichia coli: preparation of a strain with deletions in all of the genes for polyamine biosynthesis. J Bacteriol 191:5549–5552
Driessen AJ, Smid EJ, Konings WN (1988) Transport of diamines by Enterococcus faecalis is mediated by an agmatine–putrescine antiporter. J Bacteriol 170:4522–4527
Eppelmann K, Nossin PMM, Kremer SM, Wubbolts MG (2006) Biochemical synthesis of 1,4-butanediamine. WO 2006005604
Filippou P, Lioliou E, Panagiotidis C, Athanassopoulos C, Garnelis T, Papaioannou D, Kyriakidis D (2007) Effect of polyamines and synthetic polyamine-analogues on the expression of antizyme (AtoC) and its regulatory genes. BMC Biochem 8:1
Foster JW (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Micro 2:898–907
Fothergill JC, Guest JR (1977) Catabolism of l-lysine by Pseudomonas aeruginosa. J Gen Microbiol 99:139–155
Furuchi T, Kashiwagi K, Kobayashi H, Igarashi K (1991) Characteristics of the gene for a spermidine and putrescine transport system that maps at 15 min on the Escherichia coli chromosome. J Biol Chem 266:20928–20933
Gong S, Richard H, Foster JW (2003) YjdE (AdiC) is the arginine:agmatine antiporter essential for arginine-dependent acid resistance in Escherichia coli. J Bacteriol 185:4402–4409
Glansdorff N, Xu Y (2007) Microbial arginine biosynthesis: pathway, regulation and industrial production. In: Wendisch VF (ed) Amino acid biosynthesis—pathways, regulation and metabolic engineering. Springer, Berlin
Gunji Y, Yasueda H (2006) Enhancement of l-lysine production in methylotroph Methylophilus methylotrophus by introducing a mutant LysE exporter. J Biotechnol 127:1–13
Hamana K, Matsuzaki S (1992) Polyamines as a chemotaxonomic marker in bacterial systematics. Crit Rev Microbiol 18:261–283
Higashi K, Ishigure H, Demizu R, Uemura T, Nishino K, Yamaguchi A, Kashiwagi K, Igarashi K (2008) Identification of a spermidine excretion protein complex (MdtJI) in Escherichia coli. J Bacteriol 190:872–878
Hisano T, Abe S, Wakashiro M, Kimura A, Murata K (1990) Microbial spermidine dehydrogenase: purification and properties of the enzyme in Pseudomonas aeruginosa and Citrobacter freundii. J Ferment Bioeng 69:335–340
Hofle MG (1984) Degradation of putrescine and cadaverine in seawater cultures by marine bacteria. Appl Environ Microbiol 47:843–849
Igarashi K, Kashiwagi K (2010) Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol Biochem 48:506–512
Jung IL, Oh TJ, Kim G (2003) Abnormal growth of polyamine-deficient Escherichia coli mutant is partially caused by oxidative stress-induced damage. Arch Biochem Biophys 418:125–132
Kashiwagi K, Miyamoto S, Suzuki F, Kobayashi H, Igarashi K (1992) Excretion of putrescine by the putrescine–ornithine antiporter encoded by the potE gene of Escherichia coli. Proc Natl Acad Sci USA 89:4529–4533
Kashiwagi K, Shibuya S, Tomitori H, Kuraishi A, Igarashi K (1997) Excretion and uptake of putrescine by the PotE protein in Escherichia coli. J Biol Chem 272:6318–6323
Kikuchi Y, Kojima H, Tanaka T, Takatsuka Y, Kamio Y (1997) Characterization of a second lysine decarboxylase isolated from Escherichia coli. J Bacteriol 179:4486–4492
Kind S, Jeong WK, Schröder H, Zelder O, Wittmann C (2010a) Identification and elimination of the competing N-acetyldiaminopentane pathway for improved production of diaminopentane by Corynebacterium glutamicum. Appl Environ Microbiol 76:5175–5180
Kind S, Jeong WK, Schröder H, Wittmann C (2010b) Systems-wide metabolic pathway engineering in Corynebacterium glutamicum for bio-based production of diaminopentane. Metab Eng 12:341–351
Knott JM (2009) Biosynthesis of long-chain polyamines by crenarchaeal polyamine synthases from Hyperthermus butylicus and Pyrobaculum aerophilum. FEBS Lett 583:3519–3524
Kroschwitz JI, Seidel A (2004) Kirk–Othmer encyclopedia of chemical technology, 5th edn. Wiley-Interscience, Hoboken
Kurihara S, Suzuki H, Oshida M, Benno Y (2011) A novel putrescine importer required for type 1 pili-driven surface motility induced by extracellular putrescine in Escherichia coli K-12. J Biol Chem. doi:https://doi.org/10.1074/jbc.M110.176032
Kurihara S, Oda S, Tsuboi Y, Kim HG, Oshida M, Kumagai H, Suzuki H (2008) Gamma-glutamylputrescine synthetase in the putrescine utilization pathway of Escherichia coli K-12. J Biol Chem 283:19981–19990
Kurihara S, Kato K, Asada K, Kumagai H, Suzuki H (2010) A putrescine-inducible pathway comprising PuuE-YneI in which gamma-aminobutyrate is degraded into succinate in Escherichia coli K-12. J Bacteriol 192:4582–4591
Kurihara S, Tsuboi Y, Oda S, Kim HG, Kumagai H, Suzuki H (2009) Putrescine importer PuuP of Escherichia coli K-12. J Bacteriol 191:2776–2782
Kurihara S, Oda S, Kato K, Kim HG, Koyanagi T, Kumagai H, Suzuki H (2005) A novel putrescine utilization pathway involves gamma-glutamylated intermediates of Escherichia coli K-12. J Biol Chem 280:4602–4608
Lee J, Sperandio V, Frantz DE, Longgood J, Camilli A, Phillips MA, Michael AJ (2009) An alternative polyamine biosynthetic pathway is widespread in bacteria and essential for biofilm formation in Vibrio cholerae. J Biol Chem 284:9899–9907
Lee KH, Park JH, Kim TY, Kim HU, Lee SY (2007) Systems metabolic engineering of Escherichia coli for l-threonine production. Mol Syst Biol 3:149
Legrain C, Halleux P, Stalon V, Glansdorff N (1972) The dual genetic control of ornithine carbamoyltransferase in Escherichia coli: a case of bacterial hybrid enzymes. Eur J Biochem 27:93–102
Limsuwun K, Jones PG (2000) Spermidine acetyltransferase is required to prevent spermidine toxicity at low temperatures in Escherichia coli. J Bacteriol 182:5373–5380
Madduri K, Stuttard C, Vining LC (1989) Lysine catabolism in Streptomyces spp. is primarily through cadaverine: beta-lactam producers also make alpha-aminoadipate. J Bacteriol 171:299–302
Matsui I, Kamei M, Otani S, Morisawa S, Pegg AE (1982) Occurrence and induction of spermidine-N1-acetyltransferase in Escherichia coli. Biochem Biophys Res Commun 106:1155–1160
Mimitsuka T, Sawai H, Hatsu M, Yamada K (2007) Metabolic engineering of Corynebacterium glutamicum for cadaverine fermentation. Biosci Biotechnol Biochem 71:2130–2135
Miyamoto S, Kashiwagi K, Ito K, Watanabe S, Igarashi K (1993) Estimation of polyamine distribution and polyamine stimulation of protein synthesis in Escherichia coli. Arch Biochem Biophys 300:63–68
Morimoto N, Fukuda W, Nakajima N, Msuda T, Terui Y, Kanai T, Oshima T, Imanaka T, Fujiwara S (2010) Dual biosynthesis pathway for longer-chain polyamines in the hyperthermophilic archaeon Thermococcus kodakarensis. J Bacteriol 192:4991–5001
Nakada Y, Itoh Y (2003) Identification of the putrescine biosynthetic genes in Pseudomonas aeruginosa and characterization of agmatine deiminase and N-carbamoylputrescine amidohydrolase of the arginine decarboxylase pathway. Microbiology 149:707–714
Nakao H, Shinoda S, Yamamoto S (1991) Purification and some properties of carboxynorspermidine synthase participating in a novel biosynthetic pathway for norspermidine in Vibrio alginolyticus. Microbiology 137:1737–1742
Nakao H, Shinoda S, Yamamoto S (1990) Purification and properties of carboxynorspermidine decarboxylase, a novel enzyme involved in norspermidine biosynthesis, from Vibrio alginolyticus. Microbiology 136:1699–1704
Nandineni MR, Gowrishankar J (2004) Evidence for an arginine exporter encoded by yggA (argO) that is regulated by the LysR-Type transcriptional regulator ArgP in Escherichia coli. J Bacteriol 186:3539–3546
Nishi K, Endo S, Mori Y, Totsuka K, Hirao Y (2007) Method for producing cadaverine dicarboxylate. US 7189543 B2
Ohnuma M, Terui Y, Tamakoshi M, Mitome H, Niitsu M, Samejima K, Kawashima E, Oshima T (2005) N1-aminopropylagmatine, a new polyamine produced as a key intermediate in polyamine biosynthesis of an extreme thermophile, Thermus thermophilus. J Biol Chem 280:30073–30082
Oshima T (2007) Unique polyamines produced by an extreme thermophile, Thermus thermophilus. Amino Acids 33:367–372
Oshima T (2010) Enigmas of biosyntheses of unusual polyamines in an extreme thermophile, Thermus thermophilus. Plant Physiol Biochem 48:521–526
Park JH, Lee SY (2010) Metabolic pathways and fermentative production of l-aspartate family amino acids. Biotechnol J 5:560–577
Patel CN, Wortham BW, Lines JL, Fetherston JD, Perry RD, Oliveira MA (2006) Polyamines are essential for the formation of plague biofilm. J Bacteriol 188:2355–2363
Paulin L, Ruohola H, Nykänen I, Pösö H (1983) The incorporation of 1,3-diaminopropane into thermine by an extreme thermophile: a novel route for the biosynthesis of polyamines. FEMS Microbiol Lett 19:299–302
Peters-Wendisch PG, Schiel B, Wendisch VF, Katsoulidis E, Möckel B, Sahm H, Eikmanns BJ (2001) Pyruvate carboxylase is a major bottleneck for glutamate and lysine production by Corynebacterium glutamicum. J Mol Microbiol Biotechnol 3:295–300
Peters-Wendisch PG, Kreutzer C, Kalinowski J, Pátek M, Sahm H, Eikmanns BJ (1998) Pyruvate carboxylase from Corynebacterium glutamicum: characterization, expression and inactivation of the pyc gene. Microbiology 144:915–927
Pistocchi R, Kashiwagi K, Miyamoto S, Nukui E, Sadakata Y, Kobayashi H, Igarashi K (1993) Characteristics of the operon for a putrescine transport system that maps at 19 minutes on the Escherichia coli chromosome. J Biol Chem 268:146–152
Platt DK (2003) Engineering and high performance plastics market report. A Rapra market report. Rapra Technology Ltd., Shawbury
Qian Z, Xia X, Lee SY (2009) Metabolic engineering of Escherichia coli for the production of putrescine: a four carbon diamine. Biotechnol Bioeng 104:651–662
Qian Z, Xia X, Lee SY (2011) Metabolic engineering of Escherichia coli for the production of cadaverine: a five carbon diamine. Biotechnol Bioeng 108:93–103
Ren Q, Paulsen IT (2005) Comparative analyses of fundamental differences in membrane transport capabilities in prokaryotes and eukaryotes. PLoS Comp Biol 1:e27
Revelles O, Espinosa-Urgel M, Fuhrer T, Sauer U, Ramos JL (2005) Multiple and interconnected pathways for l-lysine catabolism in Pseudomonas putida KT2440. J Bacteriol 187:7500–7510
Riedel C, Rittmann D, Dangel P, Möckel B, Petersen S, Sahm H, Eikmanns BJ (2001) Characterization of the phosphoenolpyruvate carboxykinase gene from Corynebacterium glutamicum and significance of the enzyme for growth and amino acid production. J Mol Microbiol Biotechnol 3:573–583
Rosen BP (1971) Basic amino acid transport in Escherichia coli. J Biol Chem 246:3653–3662
Sabo DL, Boeker EA, Byers B, Waron H, Fischer EH (1974) Purification and physical properties of inducible Escherichia coli lysine decarboxylase. Biochemistry 13:662–670
Satishchandran C, Boyle SM (1986) Purification and properties of agmatine ureohydrolyase, a putrescine biosynthetic enzyme in Escherichia coli. J Bacteriol 165:843–848
Schneider J, Wendisch VF (2010) Putrescine production by engineered Corynebacterium glutamicum. Appl Microbiol Biotechnol 88:859–868
Seep-Feldhaus AH, Kalinowski J, Pühler A (1991) Molecular analysis of the Corynebacterium glutamicum lysl gene involved in lysine uptake. Mol Microbiol 5:2995–3005
Seiler N (2004) Catabolism of polyamines. Amino Acids 26:217–233
Seiler N (1990) Polyamine metabolism. Digestion 46:319–330
Sekowska A, Danchin A (2002) The methionine salvage pathway in Bacillus subtilis. BMC Microbiol 2:8
Shaibe E, Metzer E, Halpern YS (1985) Metabolic pathway for the utilization of l-arginine, l-ornithine, agmatine, and putrescine as nitrogen sources in Escherichia coli K-12. J Bacteriol 163:933–937
Shimizu H, Hirasawa T (2007) Production of glutamate and glutamate-related amino acids: molecular mechanism analysis and metabolic engineering. In: Wendisch VF (ed) Amino acid biosynthesis—pathways, regulation and metabolic engineering. Springer, Berlin
Soksawatmaekhin W, Kuraishi A, Sakata K, Kashiwagi K, Igarashi K (2004) Excretion and uptake of cadaverine by CadB and its physiological functions in Escherichia coli. Mol Microbiol 51:1401–1412
Steffes C, Ellis J, Wu J, Rosen BP (1992) The lysP gene encodes the lysine-specific permease. J Bacteriol 174:3242–3249
Stäbler N, Oikawa T, Bott M, Eggeling L (2011) Corynebacterium glutamicum as a host for synthesis and export of d-amino acids. J Bacteriol 193:1702–1709
Sturgill G, Rather PN (2004) Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis. Mol Microbiol 51:437–446
Suzuki O, Ishikawa Y, Miyazaki K, Izu K, Matsumoto T (1986) Acetylputrescine deacetylase from Micrococcus luteus K-11. Biochim Biophys Acta Gen Subj 882:140–142
Tabor CW, Tabor H (1985) Polyamines in microorganisms. Microbiol Rev 49:81–99
Tait GH (1976) A new pathway for the biosynthesis of spermidine. Biochem Soc Trans 4:610–612
Tait GH (1979) The formation of homospermidine by an enzyme from Rhodopseudomonas viridis. Biochem Soc Trans 7:199–201
Takatsuka Y, 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
Tateno T, Okada Y, Tsuchidate T, Tanaka T, Fukuda H, Kondo A (2008) Direct production of cadaverine from soluble starch using Corynebacterium glutamicum coexpressing alpha-amylase and lysine decarboxylase. Appl Microbiol Biotechnol 82:115–121
van Hellemond EW, van Dijk M, Heuts DPHM, Janssen DB, Fraaije MW (2008) Discovery and characterization of a putrescine oxidase from Rhodococcus erythropolis NCIMB 11540. Appl Microbiol Biotechnol 78:455–463
Verseck S, Häger H, Karau A, Eggeling L, Sahm H (2008) Verfahren zur fermentativen Herstellung von Cadaverin. DE 102007005072 A1
Völkert M, Zelder O, Ernst B, Jeong WK (2010) Method for fermentatively producing 1,5-diaminopentane. US 20100292429 A1
Vrljic M, Sahm H, Eggeling L (1996) A new type of transporter with a new type of cellular function: l-lysine export from Corynebacterium glutamicum. Mol Microbiol 22:815–826
Vrljic M, Garg J, Bellmann A, Wachi S, Freudl R, Malecki MJ, Sahm H, Kozina VJ, Eggeling L, Saier MH (1999) The LysE superfamily: topology of the lysine exporter LysE of Corynebacterium glutamicum, a paradyme for a novel superfamily of transmembrane solute translocators. J Mol Microbiol Biotechnol 1:327–336
Wallace HM, Fraser AV, Hughes A (2003) A perspective of polyamine metabolism. Biochem J 376:1–14
Wargnies B, Lauwers N, Stalon V (1979) Structure and properties of the putrescine carbamoyltransferase of Streptococcus faecalis. Eur J Biochem 101:143–152
Wittmann C, Becker J (2007) The l-lysine story: from metabolic pathways to industrial production. In: Wendisch VF (ed) Amino acid biosynthesis—pathways, regulation and metabolic engineering. Springer, Berlin
Wissenbach U, Six S, Bongaerts J, Ternes D, Steinwachs S, Unden G (1995) A third periplasmic transport system for l-arginine in Escherichia coli: molecular characterization of the artPIQMJ genes, arginine binding and transport. Mol Microbiol 17:675–686
Wu WH, Morris DR (1973) Biosynthetic arginine decarboxylase from Escherichia coli: subunit interactions and the role of magnesium ion. J Biol Chem 248:1696–1699
Yamamoto S, Hamanaka K, Suemoto Y, Ono B, Shinoda S (1986) Evidence for the presence of a novel biosynthetic pathway for norspermidine in Vibrio. Can J Microbiol 32:99–103
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Schneider, J., Wendisch, V.F. Biotechnological production of polyamines by Bacteria: recent achievements and future perspectives. Appl Microbiol Biotechnol 91, 17–30 (2011). https://doi.org/10.1007/s00253-011-3252-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-011-3252-0