siderophore-independent iron uptake by iron-limited cells of the cyanobacterium Anabaena flos-aquae

Journal of Phycology

Volumn 46, Issue 5, 2010, Pages 947-957

  Wirtz, Nikki L ^a   Treble, Ron G ^a   Weger, Harold G ^a  

^a UNIVERSITY OF REGINA   (Canada)

Author keywords

Anabaena; Cyanobacteria; Iron limitation; Iron uptake; Siderophores

Indexed keywords

ANABAENA; ANABAENA FLOS-AQUAE; CYANOBACTERIA;

EID: 77957337492     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2010.00881.x     Document Type: Article

References (59)

1. Allen M M. Simple conditions for growth of unicellular blue-green algae on plates. J. Phycol. 1968, 4:1-4.
2. Barbeau K, Rue E L, Trick C G, Bruland K W, Butler A. Photochemical reactivity of siderophores produced by marine heterotrophic bacteria and cyanobacteria based on characteristic Fe(III) binding groups. Limnol. Oceanogr. 2003, 48:1069-78.
3. Beiderbeck H, Taraz K, Budzikiewicz H, Walsby A E. Bacterial constituents part XCI - Anachelin, the siderophore of the cyanobacterium Anabaena cylindrica CCAP 1403/2A. Z. Naturforsch. C 2000, 55:681-7.
4. Boyd P W. Environmental factors controlling phytoplankton processes in the Southern Ocean. J. Phycol. 2002, 38:844-61.
5. Budzikiewicz H, Munzinger M, Taraz K, Meyer J M. Bacterial constituents. 69. Schizokinen, the siderophore of the plant deleterious bacterium Ralstonia (Pseudomonas) solanacearum ATCC 11696. Z. Naturforsch C 1997, 52:496-503.
6. Chaberak S, Courtney R C, Martell A E. Stability of metal chelates. V. N,N-Dihydroxyethylglycine. J. Am. Chem. Soc. 1953, 75:2185-90.
7. Collins C M, Anderson A M, Weger H G. Iron acquisition by the green alga Selenastrum minutum: growth in iron-limited chemostats and effects of chelator stability constant. Arch. Hydrobiol. 2001, 151:283-99.
8. Eckhardt U, Buckhout T J. Analysis of the mechanism of iron assimilation Chlamydomonas reinhardtii: a model system for strategy I plants. J. Plant Nutr. 2000, 23:1797-807.
9. Fadeev E A, Luo M K, Groves J T. Synthesis, structure, and molecular dynamics of gallium complexes of schizokinen and the amphiphilic siderophore acinetoferrin. J. Am. Chem. Soc. 2004, 126:12065-75.
10. Fan S-M. Photochemical and biochemical controls on reactive oxygen and iron speciation in the pelagic surface ocean. Mar. Chem. 2008, 109:152-64.
11. Ferguson A D, Deisenhofer J. TonB-dependent receptors-structural perspectives. Biochem. Biophys. Acta Biomembr. 2002, 1565:318-32.
12. Finden D A S, Tipping E, Jaworski G H M, Reynolds C S. Light-induced reduction of natural iron(III) oxide and its relevance to phytoplankton. Nature 1984, 309:783-4.
13. Garg S, Rose A L, Godrant A, Waite T D. Iron uptake by the ichthyotoxic Chattonella marina (Raphidophyceae): impact of superoxide generation. J. Phycol. 2007, 43:978-91.
14. Goldman S J, Lammers P J, Berman M S, Sanders-Loehr J. Siderophore-mediated iron uptake in different strains of Anabaena sp. J. Bacteriol. 1983, 156:1144-50.
15. Gress C D, Treble R G, Matz C J, Weger H G. Biological availability of iron to the freshwater cyanobacterium Anabaena flos-aquae. J. Phycol. 2004, 40:879-86.
16. Hassler C S, Twiss M R. Bioavailability of iron sensed by a phytoplanktonic Fe-bioreporter. Environ. Sci. Technol. 2006, 40:2544-51.
17. Hirose K. Metal-organic matter interaction: ecological roles of ligands in oceanic DOM. Appl. Geochem. 2007, 22:1636-45.
18. Hughes E D, Gorham P R, Zehnder A. Toxicity of a unialgal culture of Microcystis aeruginosa. Can. J. Microbiol. 1958, 4:225-36.
19. Ito Y, Butler A. Structure of synechobactins, new siderophores of the marine cyanobacterium Synechococcus sp. PCC 7002. Limnol. Oceanogr. 2005, 50:1918-23.
20. Itou Y, Okada S, Murakami M. Two structural isomeric siderophores from the freshwater cyanobacterium Anabaena cylindrica (NIES-19). Tetrahedron 2001, 57:9093-9.
21. Jeanjean R, Talla E, Latifi A, Havaux M, Janicki A, Zhang C C. A large gene cluster encoding peptide synthetases and polyketide synthases is involved in production of siderophores and oxidative stress response in the cyanobacterium Anabaena sp. strain PCC 7120. Environ. Microbiol. 2008, 10:2574-85.
22. Kraemer S M. Iron oxide dissolution and solubility in the presence of siderophores. Aquat. Sci. 2004, 66:3-18.
23. Kustka A B, Shaked Y, Milligan A J, King D W, Morel F M M. Extracellular production of superoxide by marine diatoms: contrasting effects on iron redox chemistry and bioavailability. Limnol. Oceanogr. 2005, 50:1172-80.
24. Lynnes J A, Derzaph T L M, Weger H G. Iron limitation results in induction of ferricyanide reductase and ferric chelate reductase activities in Chlamydomonas reinhardtii. Planta 1998, 204:360-5.
25. Martell A E, Smith R M. NIST Critically Selected Stability Constants of Metal Complexes 2004, NIST Standard Reference Database 46 Version 8.0, National Institute of Standards, Gaithersburg, Maryland
26. Martin J D, Ito Y, Homann V V, Haygood M G, Butler A. Structure and membrane affinity of new amphiphilic siderophores produced by Ochrobactrum sp. SP18. J. Biol. Inorg. Chem. 2006, 11:633-41.
27. Martinez J S, Butler A. Marine amphiphilic siderophores: marinobactin structure, uptake, and microbial partitioning. J. Inorg. Biochem. 2007, 101:1692-8.
28. Martinez J S, Carter-Franklin J N, Mann E L, Martin J D, Haygood M G, Butler A. Structure and membrane affinity of a suite of amphiphilic siderophores produced by a marine bacterium. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:3754-9.
29. Martinez J S, Zhang G P, Holt P D, Jung H T, Carrano C J, Haygood M G, Butler A. Self-assembling amphiphilic siderophores from marine bacteria. Science 2000, 287:1245-7.
30. Metsärinne S, Rantanen P, Aksela R, Tuhkanen T. Biological and photochemical degradation rates diethylenetriaminepentaacetic acid (DTPA) in the presence and absence of Fe(III). Chemosphere 2004, 55:379-88.
31. Morel F M M, Kustka A B, Shaked Y. The role of unchelated Fe in the iron nutrition of phytoplankton. Limnol. Oceanogr. 2008, 53:400-4.
32. Moslavac S, Bredemeier R, Mirus O, Granvogl B, Eichacker L A, Schleiff E. Proteomic analysis of the outer membrane of Anabaena sp. strain PCC 7120. J. Proteome Res. 2005, 4:1330-8.
33. Mullis K B, Pollack J R, Neilands J B. Structure of schizokinen, an iron-transport compound from Bacillus megaterium. Biochemistry 1971, 10:4894-8.
34. Nagai T, Imai A, Matsushige K, Fukushima T. Effect of iron complexation with dissolved organic matter on the growth of cyanobacteria in a eutrophic lake. Aquat. Microb. Ecol. 2006, 44:231-9.
35. Nakon R, Krishnamoorthy C R. Free-metal ion depletion by " Good's" buffers. Science 1983, 221:749-50.
36. Nicolaisen K, Moslavac S, Samborski A, Valdebenito M, Hantke K, Maldener I, Muro-Pastor A M, Flores E, Schleiff E. Alr0397 is an outer membrane transporter for the siderophore schizokinen in Anabaena sp strain PCC 7120. J. Bacteriol. 2008, 190:7500-7.
37. North R L, Guildford S J, Smith R E H, Havens S M, Twiss M R. Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie. Limnol. Oceanogr. 2007, 52:315-28.
38. Palenik B, Brahamsha B, Larimer F W, Land M, Hauser L, Chain P, Lamerdin J, Waterbury J. The genome of a motile marine Synechococcus. Nature 2003, 424:1037-42.
39. Paz Y, Shimoni E, Weiss M, Pick U. Effects of iron deficiency on iron binding and internalization into acidic vacuoles in Dunaliella salina. Plant Physiol. 2007, 144:1407-15.
40. Plowman J E, Loehr T M, Goldman S J, Sanders-Loehr J. Structure and siderophore activity of ferric schizokinen. J. Inorg. Biochem. 1984, 20:183-97.
41. Porra R J, Thompson W A, Kriedemann P E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 1989, 975:384-94.
42. Ratledge C. Iron, mycobacteria and tuberculosis. Tuberculosis 2004, 84:110-30.
43. Rose A L, Salmon T P, Lukondeh T, Neilan B A, Waite T D. Use of superoxide as an electron shuttle for iron acquisition by the marine cyanobacterium Lyngbya majuscula. Environ. Sci. Technol. 2005, 39:3708-15.
44. Salmon T P, Rose A L, Neilan B A, Waite T D. The FeL model of iron acquisition: nondissociative reduction of ferric complexes in the marine environment. Limnol. Oceanogr. 2006, 51:1744-54.
45. Schwyn B, Neilands J B. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 1987, 160:47-56.
46. Shaked Y, Kustka A B, Morel F M M. A general kinetic model for iron acquisition by eukaryotic phytoplankton. Limnol. Oceanogr. 2005, 50:872-82.
47. Silva A M N, Kong X L, Parkin M C, Cammack R, Hider R C. Iron(III) citrate speciation in aqueous solution. Dalton Trans. 2009, 2009:8616-25.
48. Šima J, Makáňová J. Photochemistry of iron (III) complexes. Coordination Chem. Rev. 1997, 160:161-89.
49. Simpson F B, Neilands J B. Siderochromes in Cyanophyceae: isolation and characterization of schizokinen from Anabaena sp. J. Phycol. 1976, 12:44-8.
50. Stintzi A, Barnes C, Xu J, Raymond K N. Microbial iron transport via a siderophore shuttle: a membrane iron transport paradigm. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:10691-6.
51. Sunda W G. Bioavailability and bioaccumulation of iron in the sea. The Biogeochemistry of Iron in Seawater 2001, 41-84. Turner D RHunter K A. Eds, John Wiley & Sons, Chichester, UK
52. Vrede T, Tranvik L J. Iron constraints on planktonic primary production in oligotrophic lakes. Ecosystems 2006, 9:1094-105.
53. Wang W-X, Dei R C H. Bioavailability of iron complexed with organic colloids to the cyanobacteria Synechococcus and Trichodesmium. Aquat. Microb. Ecol. 2003, 33:247-59.
54. Weger H G. Ferric and cupric reductase activities in the green alga Chlamydomonas reinhardtii: experiments using iron-limited chemostats. Planta 1999, 207:377-84.
55. Weger H G, Matz C J, Magnus R S, Walker C N, Fink M B, Treble R G. Differences between two green algae in biological availability of iron bound to strong chelators. Can. J. Bot. 2006, 84:400-11.
56. Weger H G, Middlemiss J K, Petterson C D. Ferric chelate reductase activity as affected by the iron-limited growth rate in four species of unicellular green algae (Chlorophyta). J. Phycol. 2002, 38:513-9.
57. Wilhelm S W, MacAuley K, Trick C G. Evidence for the importance of catechol-type siderophores in the iron-limited growth of a cyanobacterium. Limnol. Oceanogr. 1998, 43:992-7.
58. Wilhelm S W, Trick C G. Iron-limited growth of cyanobacteria: multiple siderophore production is a common response. Limnol. Oceanogr. 1994, 39:1979-84.
59. Yoshida M, Kuma K, Iwade S, Isoda Y, Takata H, Yamada M. Effect of aging time on the availability of freshly precipitated ferric hydroxide to coastal marine diatoms. Mar. Biol. 2006, 149:379-92.