Iron Stress in Open-Ocean Cyanobacteria (Synechococcus, Trichodesmium, and Crocosphaera spp.): Identification of the IdiA Protein

Applied and Environmental Microbiology

Volumn 67, Issue 12, 2001, Pages 5444-5452

  Webb, E A ^a   Moffett, J W ^a   Waterbury, J B ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; IDIA PROTEIN, SYNECHOCOCCUS; IRON; SEA WATER;

ARTICLE; CULTURE MEDIUM; CYANOBACTERIUM; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; HEAT SHOCK RESPONSE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

CARRIER PROTEINS; CULTURE MEDIA; CYANOBACTERIA; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK RESPONSE; IRON; SEAWATER; SUPPORT, NON-U.S. GOV'T; SYNECHOCOCCUS GROUP;

EID: 0035656732     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.67.12.5444-5452.2001     Document Type: Article

References (58)

1. Adhikari, P., S. D. Kirby, A. J. Nowalk, K. L. Veraldi, A. B. Schryvers, and T. A. Mietzner. 1495. Biochemical characterization of a Haemophilus influenzae periplasmic iron transport operon. J. Biol. Chem. 270:25142-25149.
2. Angerer, A., S. Gaisser, and V. Braun. 1990. Nucleotide sequences of the sfuA, sfuB, and sfuC genes of Serratia marcescens suggest a periplasmic-binding-protein-dependent iron transport mechanism. J. Bacteriol. 172:572-578.
3. Angerer, A., B. Klupp, and V. Braun. 1992. Iron transport systems of Serratia marcescens. J. Bacteriol. 174:1378-1387.
4. Archibald, F. 1983. Lactobacillus plantarum, an organism not requiring iron. FEMS Microbiol. Lett. 19:29.
5. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1999. Short protocols in molecular biology, 4th ed. Wiley, New York, N.Y.
6. Behrenfeld, M. J., and Z. S. Kolber. 1999. Widespread iron limitation of phytoplankton in the south pacific ocean. Science 283:840-843.
7. Boos, W., and J. M. Lucht. 1999. Periplasmic Binding Protein-Dependent ABC Transporters. In F. C. Neidhardt (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press. Washington, D.C.
8. Brahamsha, B. 1996. An abundant cell-surface polypeptide is required for swimming by the nonflagellated marine cyanobacterium Synechococcus. Proc. Natl. Acad. Sci. USA 93:6504-6509.
9. Braun, V., and H. Killmann. 1999. Bacterial solutions to the iron-supply problem. Trends Biochem. Sci. 24:104-109.
10. Capone, D. G., J. P. Zehr, H. W. Paerl, B. Bergman, and E. J. Carpenter. 1997. Trichodesmium, a globally significant marine cyanobacterium. Science 276:1221-1229.
11. Chadd, H. E., I. R. Joint, N. H. Mann, and N. G. Carr. 1996. The marine picoplankter Synechococcus sp. WH 7803 exhibits an adaptive response to restricted iron availability. FEMS Microbiol. Ecol. 21:69-76.
12. Coale, K. H., K. S. Johnson, S. E. Fitzwater, R. M. Gordon, S. Tanner, F. P. Chavez, L. Ferioli, C. Sakamoto, P. Rogers, F. Millero, P. Steinberg, P. Nightingale, D. Cooper, W. P. Cochlan, and R. Kudela. 1996. A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the Equatorial Pacific Ocean. Nature 383:495-501.
13. Dubrac, S., and D. Touati. 2000. Fur positive regulation of iron superoxide dismutase in Escherichia coli: functional analysis of the sodB promoter. J. Bacteriol. 182:3802-3808.
14. Escolar, L., J. Perez-Martin, and V. de Lorenzo. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:6223-6229.
15. Fekkes, P., and A. J. Driessen. 1999. Protein targeting to the bacterial cytoplasmic membrane. Microbiol. Mol. Biol. Rev. 63:161-173.
16. Ferreiros, C., M. T. Criado, and J. A. Gomez. 1999. The Neisserial 37 kDa ferric binding protein (FbpA). Comp. Biochem. Physiol. B 123:1-7.
17. Ghassemian, M., and N. A. Straus. 1996. Fur regulates the expression of iron-stress genes in the cyanobacterium Synechococcus sp. strain PCC 7942. Microbiology 142:1469-1476.
18. Goldman, S. J., P. J. Lammers, M. S. Berman, and J. Sanders-Loehr. 1983. Siderophore-mediated iron uptake in different strains of Anabacna sp. J. Bacteriol. 156:1144-1150.
19. Guerinot, M. L. 1994. Microbial iron transport. Annu. Rev. Microbiol. 48: 743-772.
20. Henikoff, S., and J. G. Henikoff. 1992. Amino acid substitution matrices from protein blocks. Proc. Natl. Acad. Sci. USA 89:10915-10919.
21. Hutchins, D. A., A. E. Witter, A. Butler, and G. W. Luther III. 1999. Competition among marine phytoplankton for different chelated iron species. Nature 400:858-861.
22. Katoh, H., A. R. Grossman, N. Hagino, and T. Ogawa. 2000 A gene of Synechocystis sp. strain PCC 6803 encoding a novel iron transporter. J. Bacteriol. 182:6523-6524.
23. Katoh, H., N. Hagino, A. R. Grossman, and T. Ogawa. 2001. Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 189:2779-2784.
24. Kerry, A., D. E. Laudenbach, and C. G. Trick. 1988. Influence of iron limitation and nitrogen source on growth and siderophore production by cyanobacteria. J. Phycol. 24:566-571.
25. Lammers, P. J., and J. Sanders-Loehr. 1982. Active transport of ferric schizokinen in Anabaena sp. J. Bacteriol. 151:288-294.
26. Larsen, R. A., M. G. Thomas, and K. Postle. 1999. Proton motive force, ExbB and ligand-bound FcpA drive conformational changes in TonB. Mol. Microbiol. 31:1809-1824.
27. Leonhardt, K., and N. A. Straus. 1992. An iron stress operon involved in photosynthetic electron transport in the marine cyanobacterium Synechococcus sp. PCC 7002. J. Gen. Microbiol. 138:1613-1621.
28. Martin, J. H., K. H. Coale, K. S. Johnson, S. E. Fitzwater, R. M. Gordon, S. J. Tanner, C. N. Hunter, V. A. Elrod, J. L. Nowicki, T. L. Coley, R. T. Barber, S. Lindley, A. J. Watson, K. Van Scoy, C. S. Law, M. I. Liddicoat, R. Ling, T. Stanton, J. Stocjel, C. Collins, A. Anderson, R. Bidigare, M. Ondrusek, M. Latasa, F. J. Millero, K. Lee, W. Yao, J. Z. Zhang, D. Friederich, C. Sakamoto, F. Chavez, K. Buck, Z. Kolber, R. Greene, P. Falkowski, S. W. Chisholm, F. Hoge, R. Swift, J. Yungel, S. Turner, P. Nightingale, A. Hatton, P. Liss, and N. W. Tindale. 1994. Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 371:123-129.
29. McKay, D. B., and T. A. Steitz. 1981. Structure of catabolite gene activator protein at 2.9 A resolution suggests binding to left-handed B-DNA. Nature 290:744-749.
30. Michel, K. P., P. Exss-Sonne, G. Scholten-Beck, U. Kahmann, H. G. Ruppel, and E. K. Pistorius. 1998. Immunocytochemical localization of IdiA, a protein expressed under iron or manganese limitation in the mesophilic cyanobacterium Synechococcus PCC 6301 and the thermophilic cyanobacterium Synechococcus elongatus. Planta 205:73-81.
31. Michel, K. P., F. Kruger, A. Puhler, and E. K. Pistorius. 1999. Molecular characterization of idiA and adjacent genes in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942. Microbiology 144:1473-1484.
32. Michel, K. P., H. H. Thole, and E. K. Pistorius. 1996. IdiA, a 34 kDa protein in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942, is required for growth under iron and manganese limitations. Microbiology 142:2635-2645.
33. 2 fixation and growth in natural and cultured populations of the planktonic marine cyanobacterium Trichodesmium spp. Appl. Environ. Microbiol. 60: 1044-1047.
34. Park, Y. I., S. Sandstrom, P. Gustafsson, and G. Oquist. 1999. Expression of the isiA gene is essential for the survival of the cyanobacterium Synechococcus sp. PCC 7942 by protecting photosystem II from excess light under iron limitation. Mol. Microbiol. 32:123-129.
35. Partensky, F., J. Blanchot, and D. Vaulot. 1999. Differential distribution and ecology of Prochlorococcu and Synechococcus in oceanic waters: a review, p. 457-475. In L. Charpy and A. W. D. Larkum (ed.), Marine cyanobacteria, vol. 19. Institut Océanographique, Monte Carlo, Monaco.
36. Partensky, F., W. R. Hess, and D. Vaulot. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63:106-127.
37. Posey, J. E., and F. C. Gherardini. 2000. Lack of a role for iron in the Lyme disease pathogen. Science 288:1651-1653.
38. Reddy, K. J., G. S. Bullerjahn, D. M. Sherman, and L. A. Sherman. 1988. Cloning, nucleotide sequence, and mutagenesis of a gene (irpA) involved in iron-deficient growth of the cyanobacterium Synechococcus sp. strain PCC7942. J. Bacteriol. 170:4466-4476.
39. Reimmann, C., H. M. Patel, L. Serino, M. Barone, C. T. Walsh, and D. Haas. 2001. Essential PchG-dependent reduction in pyochelin biosynthesis of Pseudomonas aeruginosa. J. Bacteriol. 183:813-820.
40. Resch, C. M., and J. Gibson. 1983. Isolation of the carotenoid-containing cell wall of three unicellular cyanobacteria. J. Bacteriol. 155:345-350.
41. Reuter, J. G., D. A. Hutchins, R. W. Smith, and N. L. Unsworth. 1992. Iron nutrition of Trichodesmium, p. 289-306. In E. J. Carpenter, D. G. Capone, and J. G. Reuter (ed.), Marine pelagic cyanobacteria: Trichodesmium and other diazotrophs. Kluwer Academic Publishers, Boston, Mass.
42. Rippka, R., R. W. Castenholz, J. B. Waterbury, and M. Herdman. 2001. Form-genus V. Cyanothece, p. 501. In G. M. Garrity (ed.), Bergey's manual of systematic bacteriology, vol. 2, Springer, New York, N. Y.
43. Rueter, J. G., and O. K. Fujita. 1991. Response of marine Synechococcus (Cyanophyceae) cultures to iron limitation. J. Phycol. 27:173-178.
44. Sanders, J. D., L. D. Cope, and E. J. Hansen. 1994. Identification of a locus involved in the utilization of iron by Haemophilus influenzae. Infect. Immun. 62:4515-4525.
45. Scanlan, D. J., N. H. Mann, and N. G. Carr. 1989. Effect of iron and other nutrient limitations on the pattern of outer membrane proteins in the cyanobacterium Synechococcus PCC7942. Arch. Microbiol. 152:224-228.
46. Stintzi, A., C. Barnes, J. Xu, and K. N. Raymond. 2000. Microbial iron transport via a siderophore shuttle: a membrane ion transport paradigm. Proc. Natl. Acad. Sci. USA 97:10691-10696.
47. Tortell, P. D., M. T. Maldonado, J. Granger, and N. M. Price. 1999. Marine bacteria and biogeochemical cycling of iron in the oceans. FEMS Microbiol. Ecol. 29:1-11.
48. Waterbury, J. B., and R. Rippka. 1989. Subsection I. Order Chroococcaloes, p. 1728-1746. In J. T. Staley (ed.), Bergey's manual of systematic bacteriology, vol. 3. Williams & Wilkins, Baltimore, Md.
49. Waterbury, J. B., S. W. Watson, K. W. Valois, and D. G. Franks. 1986. Biological and ecological characterization of the marine unicellular cyanobaeterium Synechococcus, p. 71-120. In T. Platt and W. K. W. Li (ed.), Photosynthetic picoplankton, vol. 214. Dept. of Fisheries and Oceans, Ottawa, Canada.
50. Waterbury, J. B., and J. M. Willey. 1988. Isolation and growth of marine planktonic cyanobacteria. Methods Enzymol. 167:100-105.
51. Webb, R., T. Troyan, D. Sherman, and L. A. Sherman. 1994. MapA, an iron-regulated, cytoplasmic membrane protein in the cyanobacterium Synechococcus sp. strain PCC7942. J. Bacteriol. 176:4906-4913.
52. Wilhelm, S. W. 1995. Ecology of iron-limited cyanobacteria: a review of physiological responses and implications for aquatic systems. Aquat. Microb. Ecol. 9:295-303.
53. Wilhelm, S. W., K. MacAuley, and C. G. Trick. 1998. Evidence for the importance of catechol-type siderophores in the iron-limited growth of a cyanobacterium. Limnol. Oceanogr. 43:992-997.
54. Wilhelm, S. W., D. P. Maxwell, and C. G. Trick. 1996. Growth, iron requirements, and siderophore production in iron-limited Synechococcus PCC 7002. Limnol. Oceanogr. 41:89-97.
55. Wilhelm, S. W., and C. G. Trick. 1994. Iron-limited growth of cyanobacteria: Multiple siderophore production is a common response. Limnol. Oceanogr. 39(8):1979-1984.
56. Wilhelm, S. W., and C. G. Trick. 1995. Physiological profiles of Synechococcus (Cyanophyceae) in iron-limiting continuous cultures. J. Phycol. 31:79-85.
57. 2 in the subtropical North Pacific Ocean. Nature 412:635-638.
58. Zimmermann, L., A. Angerer, and V. Braun. 1989. Mechanistically novel iron(III) transport system in Serratia marcescens. J. Bacteriol. 171:238-243.