Abstract
Nitrosomonas europaea has a single three-gene operon (nitABC) encoding an iron ABC transporter system (NitABC). Phylogenetic analysis clustered the subunit NitB with Fe3+-ABC transporter permease components from other organisms. The N.europaea strain deficient in nitB (nitB::kan) grew well in either Fe-replete or Fe-limited media and in Fe-limited medium containing the catecholate-type siderophore, enterobactin or the citrate-based dihydroxamate-type siderophore, aerobactin. However, the nitB::kan mutant strain was unable to grow in Fe-limited media containing either the hydroxamate-type siderophores, ferrioxamine and ferrichrome or the mixed-chelating type siderophore, pyoverdine. Exposure of N. europaea cells to a ferrichrome analog coupled to the fluorescent moiety naphthalic diimide (Fhu-NI) led to increase in fluorescence in the wild type but not in nitB::kan mutant cells. Spheroplasts prepared from N.europaea wild type exposed to Fhu-NI analog retained the fluorescence, while spheroplasts of the nitB::kan mutant were not fluorescent. NitABC transports intact Fe3+-ferrichrome complex into the cytoplasm and is an atypical ABC type iron transporter for Fe3+ bound to ferrioxamine, ferrichrome or pyoverdine siderophores into the cytoplasm. The mechanisms to transport iron in either the Fe3+ or Fe2+ forms or Fe3+ associated with enterobactin or aerobactin siderophores into the cell across the cytoplasmic membrane are as yet undetermined.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adhikari P, Berish SA, Nowalk AJ, Veraldi KL, Morse SA, Mietzner TA (1996) The fbpABC locus of Neisseria gonorrhoeae functions in the periplasm-to-cytosol transport of iron. J Bacteriol 178:2145–2149
Anderson DS, Adhikari P, Weaver KD, Crumbliss AL, Mietzner TA (2007) The Haemophilus influenzae hFbpABC Fe3+ transporter: analysis of the membrane permease and development of a gallium-based screen for mutants. J Bacteriol 189:5130–5141
Andrews SC, Robinson AK, Rodriguez-Quinones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237
Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795
Chain P et al (2003) Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol 185:2759–2773
Ensign SA, Hyman MR, Arp DJ (1993) In vitro activation of ammonia monooxygenase from Nitrosomonas europaea by copper. J Bacteriol 175:1971–1980
Escolar L, Perez-Martin J, de Lorenzo V (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181:6223–6229
Gong S, Bearden SW, Geoffroy VA, Fetherston JD, Perry RD (2001) Characterization of the Yersinia pestis Yfu ABC inorganic iron transport system. Infect Immun 69:2829–2837
Guerinot ML (1994) Microbial iron transport. Annu Rev Microbiol 48:743–772
Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580
Hommes NG, Sayavedra-Soto LA, Arp DJ (1996) Mutagenesis of hydroxylamine oxidoreductase in Nitrosomonas europaea by transformation and recombination. J Bacteriol 178:3710–3714
Hooper AB, Erickson RH, Terry KR (1972) Electron transport systems of Nitrosomonas: isolation of a membrane-envelope fraction. J Bacteriol 110:430–438
Klotz MG et al (2006) Complete genome sequence of the marine, chemolithoautotrophic, ammonia-oxidizing bacterium Nitrosococcus oceani ATCC 19707. Appl Environ Microbiol 72:6299–6315
Köster W (1991) Iron(III) hydroxamate transport across the cytoplasmic membrane of Escherichia coli. Biol Met 4:23–32
Köster W (2001) ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B12. Res Microbiol 152:291–301
Köster W (2005) Cytoplasmic membrane iron permease systems in the bacterial cell envelope. Front Biosci 10:462–477
Kovach ME et al (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175–176
Meijler MM, Arad-Yellin R, Cabantchik ZI, Shanzer A (2002) Synthesis and evaluation of iron chelators with masked hydrophilic moieties. J Am Chem Soc 124:12666–12667
Morrissey JA, Cockayne A, Hill PJ, Williams P (2000) Molecular cloning and analysis of a putative siderophore ABC transporter from Staphylococcus aureus. Infect Immun 68:6281–6288
Norton JM et al (2008) Complete genome sequence of Nitrosospira multiformis, an ammonia-oxidizing bacterium from the soil environment. Appl Environ Microbiol 74:3559–3572
Pressler U, Staudenmaier H, Zimmermann L, Braun V (1988) Genetics of the iron dicitrate transport system of Escherichia coli. J Bacteriol 170:2716–2724
Quatrini R, Jedlicki E, Holmes DS (2005) Genomic insights into the iron uptake mechanisms of the biomining microorganism Acidithiobacillus ferrooxidans. J Ind Microbiol Biotechnol 32:606–614
Quatrini R, Lefimil C, Veloso FA, Pedroso I, Holmes DS, Jedlicki E (2007) Bioinformatic prediction and experimental verification of Fur-regulated genes in the extreme acidophile Acidithiobacillus ferrooxidans. Nucleic Acids Res 35:2153–2166
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor
Schryvers AB, Stojiljkovic I (1999) Iron acquisition systems in the pathogenic Neisseria. Mol Microbiol 32:1117–1123
Shea CM, McIntosh MA (1991) Nucleotide sequence and genetic organization of the ferric enterobactin transport system: homology to other periplasmic binding protein-dependent systems in Escherichia coli. Mol Microbiol 5:1415–1428
Stein LY, Arp DJ (1998) Loss of ammonia monooxygenase activity in Nitrosomonas europaea upon exposure to nitrite. Appl Environ Microbiol 64:4098–4102
Stein LY et al (2007) Whole-genome analysis of the ammonia-oxidizing bacterium, Nitrosomonas eutropha C91: implications for niche adaptation. Environ Microbiol 9:2993–3007
Stephens DL, Choe MD, Earhart CF (1995) Escherichia coli periplasmic protein FepB binds ferrienterobactin. Microbiology 141(Pt 7):1647–1654
Suzuki I, Kwok SC (1969) Oxidation of ammonia by spheroplasts of Nitrosomonas europaea. J Bacteriol 99:897–898
Wei X, Sayavedra-Soto LA, Arp DJ (2004) The transcription of the cbb operon in Nitrosomonas europaea. Microbiology 150:1869–1879
Wei X, Vajrala N, Hauser L, Sayavedra-Soto LA, Arp DJ (2006) Iron nutrition and physiological responses to iron stress in Nitrosomonas europaea. Arch Microbiol 186:107–118
Acknowledgments
We sincerely thank Dr. Joseph Englander (Weizmann Institute of Science, Rehovot, Israel) for kindly providing the fluorescently labeled ferrichrome analog and for his valuable suggestions. We thank Dr. Conrad Schoch (GenBank, National Center for Biotechnology Information (NCBI), Bethesda, MD) for help with phylogenetic analysis. This research was supported by grant DE-FG03-01ER63149 to D. J. A. and the Oregon Agricultural Experiment Station.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Erko Stackebrandt.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Vajrala, N., Sayavedra-Soto, L.A., Bottomley, P.J. et al. Role of Nitrosomonas europaea NitABC iron transporter in the uptake of Fe3+-siderophore complexes. Arch Microbiol 192, 899–908 (2010). https://doi.org/10.1007/s00203-010-0620-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-010-0620-6