Abstract
Although an excellent nitrogen source for most bacteria, ammonium was—in analogy to plant and animal systems—assumed be detrimental to bacteria when present in high concentrations. In this study, we examined the effect of molar ammonium concentrations on different model bacteria, namely, Corynebacterium glutamicum, Escherichia coli, and Bacillus subtilis. The studied bacteria are highly resistant to ammonium. When growth was impaired upon addition of molar (NH4)2SO4 concentrations, this was not caused by an ammonium-specific effect but was due to an enhanced osmolarity or increased ionic strength of the medium. Therefore, it was concluded that ammonium is not detrimental to C. glutamicum and other bacteria even when present in molar concentrations.
Similar content being viewed by others
Literature Cited
Abe S, Takayama K, Kinoshita S (1967) Taxonomical studies on glutamic acid producing bacteria. J Gen Microbiol 13:279–301
Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1987) Current protocols in molecular biology. New York: Greene Publishing Associates and Wiley Interscience, John Wiley and Sons
Beckers G, Nolden L, Burkovski A (2001) Glutamate synthase of Corynebacterium glutamicum is not essential for glutamate synthesis and is regulated by the nitrogen status. Microbiology 147:2961–2970
Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ (2001) Futile transmembrane NH +4 cycling: A cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 98:4255–4258
Britto DT, Konzucker HJ (2002) NH +4 toxicity in higher plants: a critical review. J Plant Physiol 159:567–584
Burkovski A (2003) I do it my way: Regulation of ammonium uptake and ammonium assimilation in Corynebacterium glutamicum. Arch Microbiol 179:83–88
Burkovski A (2003) Ammonium assimilation and nitrogen control in Corynebacterium glutamicum and its relatives: an example for new regulatory mechanisms in actinomycetes. FEMS Microbiol Rev 27:617–628
Burkovski A (2005) Nitrogen metabolism and its regulation. In: Bott M, Eggeling L (eds) Handbook of Corynebacterium glutamicum. Boca Raton, FL: CRC Press, p 99–118
Davis BD, Mingioli ES (1950) Mutants of Escherichia coli requiring methionine or vitamin B12. J Bacteriol 60:17–28
Detsch C, Stülke J (2003) Ammonium utilization in Bacillus subtilis: transport and regulatory functions of NrgA and NrgB. Microbiology 149:3289–3297
Hermann T (2003) Industrial production of amino acids by coryneform bacteria. J Biotechnol 104:155–172
Jakoby M, Tesch M, Sahm H, Krämer R, Burkovski A (1997) Isolation of the Corynebacterium glutamicum glnA gene encoding glutamine synthetase I. FEMS Microbiol Lett 154:81–88
Jakoby M, Nolden L, Meier-Wagner J, Krämer R, Burkovski A (2000) AmtR, a global repressor in the nitrogen regulation system of Corynebacterium glutamicum. Mol Microbiol 37:964–977
Javelle A, Thomas G, Marini A-M, Krämer R, Merrick M (2005) In vivo functional characterization of the Escherichia coli ammonium channel AmtB: evidence for metabolic coupling of AmtB to glutamine synthetase. Biochem J 390:215–222
Jensen KF (1993) The Escherichia coli K-12 “wild types” W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels. J Bacteriol 175:3401–3407
Keilhauer C, Eggeling L, Sahm H (1993) Isoleucine synthesis in Corynebacterium glutamicum: molecular analysis of the ilvB-ilvN-ilvC operon. J Bacteriol 175:5595–5603
Khademi S, O’Connell J III, Remis J, Robles-Colmenares Y, Miercke LJW, Stroud RM (2005) Mechanism of ammonia transport by Amt/MEP/Rh: Structure of AmtB at 1.35 A. Science 305:1587–1594
Kleiner D (1981) The transport of NH3 and NH +4 across biological membranes. Biochim Biophys Acta 639:41–52
Kleiner D (1985) Bacterial ammonium transport. FEMS Microbiol Rev 32:87–100
Kleiner D (1993) Ammonium transport systems—an overview. In: Bakker EP (ed) Alkali cation transport systems in prokaryotes. Boca Raton, FL: CRC Press
Lindroth P, Mopper K (1979) High performance liquid chromatography determination of subpicomole amounts of amino acids by precolumn fluorescence derivatization with o-phthaldialdehyde. Anal Chem 51:1667–1674
Martinelle K, Häggström L (1993) Mechanisms of ammonia and ammonium ion toxicity in animal cells: Transport across cell membranes. J Biotechnol 30:339–350
Meier-Wagner J, Nolden L, Jakoby M, Siewe R, Krämer R, Burkovski A (2001) Multiplicity of ammonium uptake systems in Corynebacterium glutamicum: Role of Amt and AmtB. Microbiology 147:135–143
Nolden L, Farwick M, Krämer R, Burkovski A (2001) Glutamine synthetases in Corynebacterium glutamicum: transcriptional control and regulation of activity. FEMS Microbiol Lett 201:91–98
Puech V, Chami M, Lemassu A, Laneelle MA, Schiffler B, Gounon P, Bayan N, Benz R, Daffe M (2001) Structure of the cell envelope of corynebacteria: importance of the non-covalently bound lipids in the formation of the cell wall permeability barrier and fracture plane. Microbiology 147:1365–1382
Ritchie RJ, Gibson J (1987) Permeability of ammonia, methylamine and ethylamine in the cyanobacterium Synechococcus R-2 (Anacystis nidulans) PCC7942. J Membr Biol 95:131–142
Ritchie RJ, Gibson J (1987) Permeability of ammonia and amines in Rhodobacter spheroides and Bacillus firmus. Arch Biochem Biophys 258:322–341
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
Schäfer A, Tauch A, Jäger W, Kalinowski J, Thierbach G, Pühler A (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: Selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69–73
Siewe RM, Weil B, Krämer R (1995) Glutamine uptake by a sodium-dependent secondary transport system in Corynebacterium glutamicum. Arch Microbiol 164:98–103
Siewe RM, Weil B, Burkovski A, Eikmanns BJ, Eikmanns M, Krämer R (1996) Functional and genetic characterization of the (methyl)ammonium uptake carrier of Corynebacterium glutamicum. J Biol Chem 271:5398–5403
Soupene E, He L, Yan D, Kustu S (1998) Ammonia acquisition in enteric bacteria: physiological role of the ammonium/methylammonium transport B (AmtB) protein. Proc Natl Acad Sci USA 95:7030–7034
Soupene E, Lee H, Kustu S (2002) Ammonium/methylammonium transport (Amt) proteins facilitate diffusion of NH3 bidirectionally. Proc Natl Acad Sci USA 99:3926–3931
van der Rest ME, Lange C, Molenaar D (1999) A heat shock following electroporation induces highly efficient transformation of Corynebacterium glutamicum with xenogeneic plasmid DNA. Appl Microbiol Biotechnol 52:541–545
von Wirén N, Gazzarrini S, Gojon A, Frommer WB (2000) The molecular physiology of ammonium uptake and retrieval. Curr Opin Plant Biol 3:254–261
von Wirén N, Merrick M (2004) Regulation and function of ammonium carriers in plants, yeast and bacteria. Trends Curr Genet 9:95–120
Acknowledgments
The authors wish to thank Stephanie Kadow and Christine Eilender for technical support and Reinhard Krämer for continuous interest and support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Müller, T., Walter, B., Wirtz, A. et al. Ammonium Toxicity in Bacteria. Curr Microbiol 52, 400–406 (2006). https://doi.org/10.1007/s00284-005-0370-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-005-0370-x