Factors influencing the diversity of iron uptake systems in aquatic microorganisms

Frontiers in Microbiology

Volumn 3, Issue OCT, 2012, Pages

  Desai, Dhwani K ^a   Desai, Falguni D ^a   LaRoche, Julie ^a  

^a GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

Author keywords

Aquatic niches; DN ds ratio; Eukaryotic phytoplankton; Fe limitation; Fe binding ligands; Marine microbes; Metagenomes; Multivariate statistics

Indexed keywords

EID: 84875846099     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00362     Document Type: Article

References (109)

1. Adhikari, P., Kirby, S. D., Nowalk, A. J., Veraldi,K. L., Schryvers, A. B., and Mietzner, T. A. (1995). Biochemical characteri-zation of a Haemophilus influenzae periplasmic iron transport operon. J. Biol. Chem. 270, 25142-25149.
2. Andrews, S. C. (1998). Iron storage in bacteria. Adv. Microb. Physiol. 40, 281-351.
3. Benson, H. P., Boncompagni, E., and Guerinot, M. L. (2005). An iron uptake operon required for proper nodule development in the Bradyrhizobium japonicum-soybean symbiosis. Mol. Plant Microbe Inter-act. 18, 950-959.
4. Boyd, P. W., Watson, A. J., Law, C. S., Abraham, E. R., Trull, T., Mur-doch, R., et al. (2000). A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 407, 695-702.
5. Boye, M., Aldrich, A. P., Van Den Berg,C. M. G.,De Jong,J. T. M., Veldhuis, M., and De Baar, H. J. W. (2003). Horizontal gradient of the chemical speciation of iron in surface waters of the northeast Atlantic Ocean. Mar. Chem. 80, 129-143.
6. Braun, V. (2003). Iron uptake by Escherichia coli. Front. Biosci. 8, S1409-S1421.
7. Buck, K. N., and Bruland, K. W. (2007). The physicochemical speci-ation of dissolved iron in the Bering Sea, Alaska. Limnol. Oceanogr. 52, 1800-1808.
8. Buck, K. N., Selph, K. E., and Barbeau, K. A. (2010). Iron-binding lig-and production and copper spe-ciation in an incubation experi-ment of Antarctic Peninsula shelf waters from the Bransfield Strait, Southern Ocean. Mar. Chem. 122, 148-159.
9. Burnap, R. L., Troyan, T., and Sher-man, L. A. (1993). The highly abun-dant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC7942 (CP43') is encoded by the isiA gene. Plant Physiol. 103, 893-902.
10. Butler, A. (2005). Marine siderophores and microbial iron mobilization. Biometals 18, 369-374.
11. Butterton, J. R., Stoebner, J. A., Payne, S. M., and Calderwood, S. B. (1992). Cloning, sequenc-ing, and transcriptional regula-tion of viuA, the gene encoding the ferric-vibriobactin receptor of Vibrio cholerae. J. Bacteriol. 174, 3729-3738.
12. Cadieux, N., Bradbeer, C., Reeger-Schneider, E., Koster, W., Mohanty, A. K., Wiener, M. C., et al. (2002). Identification of the periplasmic cobalamin-binding protein BtuF of Escherichia coli. J. Bacteriol. 184, 706-717.
13. Challis, G. L. (2005). A widely distributed bacterial pathway for siderophore biosynthesis indepen-dent of non-ribosomal peptide syn-thetases. Chembiochem 6, 601-611.
14. Clarke, K. (2006). PRIMER v6: User Manual/Tutorial, ed. R. Gorley (Ply-mouth: PRIMER-E).
15. Clarke, K. R. (1993). Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117-143.
16. Coale, K. H., Johnson, K. S., Fitzwa-ter, S. E., Gordon, R. M., Tanner, S., Chavez, F. P., et al. (1996). A mas-sive phytoplankton bloom induced by an ecosystem-scale iron fertiliza-tion experiment in the equatorial Pacific Ocean. Nature 383, 495-501.
17. Cohan, F. M. (2002). What are bacter-ial species? Annu. Rev. Microbiol. 56, 457-487.
18. Cope, L. D.,Yogev, R., Muller-Eberhard, U., and Hansen, E. J. (1995). A gene cluster involved in the uti-lization of both free heme and heme:hemopexin by Haemophilus influenzae type b. J. Bacteriol. 177, 2644-2653.
19. Cornelis,P.,and Bodilis,J. (2009).A sur-vey of TonB-dependent receptors in fluorescent pseudomonads. Environ. Microbiol. Rep. 1, 256-262.
20. de Baar, H. J. W., Boyd, P. W., Coale, K. H., Landry, M. R., Tsuda, A., Assmy, P., et al. (2005). Synthesis of iron fer-tilization experiments: from the iron age in the age of enlightenment. J. Geophys. Res. Oceans 110, C09S16. doi: 10.1029/2004JC002601
21. Desai, D. K., Nandi, S., Srivastava, P. K., and Lynn, A. M. (2011). ModEnzA: accurate identification of metabolic enzymes using function specific pro-file HMMs with optimised discrimi-nation threshold and modified emis-sion probabilities. Adv. Bioinformat-ics. doi: 10.1155/2011/743782
22. Dinsdale, E. A., Edwards, R. A., Hall, D., Angly, F., Breitbart, M., Brulc, J. M., et al. (2008). Functional metage-nomic profiling of nine biomes. Nature 452, U628-U629.
23. Duce, R. A., and Tindale, N. W. (1991). Atmospheric transport of iron and its deposition in the ocean. Limnol. Oceanogr. 36, 1715-1726.
24. Dupont, C. L., Butcher, A., Valas, R. E., Bourne, P. E., and Caetano-Anolles, G. (2010). History of biological metal utilization inferred through phylogenomic analysis of protein structures. Proc. Natl. Acad. Sci. U.S.A. 107, 10567-10572.
25. Dupont, C. L., Yang, S., Palenik, B., and Bourne, P. E. (2006). Modern proteomes contain putative imprints of ancient shifts in trace metal geochemistry. Proc. Natl. Acad. Sci. U.S.A. 103, 17822-17827.
26. Eddy, S. (1998). HMMER: Biological Sequence Analysis Using Profile Hid-den Markov Models. Available at: http://hmmer.org
27. Edgar, R. C. (2004). MUSCLE: a mul-tiple sequence alignment method with reduced time and space com-plexity. BMC Bioinformatics 5, 113. doi:10.1186/1471-2105-5-113
28. Enright, A. J., Van Dongen, S., and Ouzounis, C. A. (2002). An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 30, 1575-1584.
29. Fecker, L., and Braun, V. (1983). Cloning and expression of the fhu genes involved in the iron(III)-hydroxamate uptake by Escherichia coli. J. Bacteriol. 156, 1301-1314.
30. Ferreiros, C., Criado, M. T., and Gomez, J. A. (1999). The neisserial 37 kDa ferric binding protein (FbpA). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 123, 1-7.
31. Gall, M. P., Boyd, P. W., Hall, J., Safi, K. A., and Chang, H. (2001). Phy-toplankton processes. Part 1: com-munity structure during the South-ern Ocean Iron RElease Experiment (SOIREE). Deep Sea Res. Part II Top. Stud. Oceanogr. 48, 2551-2570.
32. Gao,Y.,Kaufman,Y. J.,Tanre,D.,Kolber, D., and Falkowski, P. G. (2001). Sea-sonal distributions of aeolian iron fluxes to the global ocean. Geophys. Res. Lett. 28, 29-32.
33. Gianoulis, T. A., Raes, J., Patel, P. V., Bjornson, R., Korbel, J. O., Letu-nic, I., et al. (2009). Quantifying environmental adaptation of meta-bolic pathways in metagenomics. Proc. Natl. Acad. Sci. U.S.A. 106, 1374-1379.
34. Gilbert,J. A.,Field,D.,Swift,P.,Thomas, S., Cummings, D., Temperton, B., et al. (2010). The taxonomic and functional diversity of microbes at a temperate coastal site: amulti-omic' study of seasonal and diel tempo-ral variation. PLoS ONE 5, e15545.doi:10.1371/journal.pone.0015545
35. Gledhill, M., and Buck, K. N. (2012). The organic complexation of iron in the marine environment: a review. Front. Microbiol. 3:69. doi:10.3389/fmicb.2012.00069
36. Gledhill, M., and van den Berg, C. M. G. (1994). Determination of complexation of iron(III) with nat-ural organic complexing ligands in seawater using cathodic stripping voltammetry. Mar. Chem. 47, 41-54.
37. Grass, G., Franke, S., Taudte, N., Nies, D. H., Kucharski, L. M., Maguire, M. E., et al. (2005). The metal per-mease ZupT from Escherichia coli is a transporter with a broad sub-strate spectrum. J. Bacteriol. 187, 1604-1611.
38. Guerinot, M. L. (2000). The ZIP fam-ily of metal transporters. Biochim. Biophys. Acta 1465, 190-198.
39. Hannenhalli, S. S., and Russell, R. B. (2000). Analysis and prediction of functional sub-types from protein sequence alignments. J. Mol. Biol. 303, 61-76.
40. Homann, V. V., Edwards, K. J., Webb, E. A., and Butler, A. (2009a). Siderophores of Marinobacter aquaeolei: petrobactin and its sul-fonated derivatives. Biometals 22, 565-571.
41. Homann, V. V., Sandy, M., Tincu, J. A., Templeton, A. S., Tebo, B. M., and Butler, A. (2009b). Loihichelins A-F, a suite of amphiphilic siderophores produced by the marine bacterium Halomonas LOB-5. J. Nat. Prod. 72, 884-888.
42. Hopkinson, B. M., and Barbeau, K. A. (2012). Iron transporters in marine prokaryotic genomes and metagenomes. Environ. Microbiol. 14, 114-128.
43. Hopkinson, B. M., and Morel, F. M. M. (2009). The role of siderophores in iron acquisition by photosynthetic marine microorganisms. Biometals 22, 659-669.
44. Hopkinson, B. M., Roe, K. L., and Barbeau, K. A. (2008). Heme uptake by Microscilla marina and evidence for heme uptake systems in the genomes of diverse marine bacte-ria. Appl. Environ. Microbiol. 74, 6263-6270.
45. Hunter, K. A., and Boyd, P. W. (2007). Iron-binding ligands and their role in the ocean biogeochemistry of iron. Environ. Chem. 4, 221-232.
46. Ito, Y., and Butler, A. (2005). Structure of synechobactins,new siderophores of the marine cyanobacterium Syne-chococcus sp. PCC 7002. Limnol. Oceanogr. 50, 1918-1923.
47. Ito, Y., Ishida, K., Okada, S., and Murakami, M. (2004). The absolute stereochemistry of anachelins, siderophores from the cyanobac-terium Anabaena cylindrica. Tetrahedron 60, 9075-9080.
48. Jeanjean, R., Talla, E., Latifi, A., Havaux, M., Janicki, A., and Zhang, C. C. (2008). 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. 10, 2574-2585.
49. Jickells, T. D., An, Z. S., Andersen, K. K., Baker, A. R., Bergametti, G., Brooks, N., et al. (2005). Global iron connec-tions between desert dust,ocean bio-geochemistry, and climate. Science 308, 67-71.
50. Johnson, K. S., Gordon, R. M., and Coale, K. H. (1997). What con-trols dissolved iron concentrations in the world ocean? Mar. Chem. 57, 137-161.
51. Johnston, A. W. B., Todd, J. D., Curson, A. R.,Lei,S.,Nikolaidou-Katsaridou, N., Gelfand, M. S., et al. (2007). Living without Fur: the subtlety and complexity of iron-responsive gene regulation in the symbiotic bacterium Rhizobium and other alpha-proteobacteria. Biometals 20, 501-511.
52. Joshi, F. R., Kholiya, S. P., Archana, G., and Desai, A. J. (2008). Siderophore cross-utilization amongst nodule isolates of the cowpea miscellany group and its effect on plant growth in the presence of antago-nistic organisms. Microbiol. Res. 163, 564-570.
53. Kammler, M., Schön, C., and Han-tke, K. (1993). Characterization of the ferrous iron uptake system of Escherichia coli. J. Bacteriol. 175, 6212-6219.
54. Katoh, H., Hagino, N., Grossman, A. R., and Ogawa, T. (2001). Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 183, 2779-2784.
55. King,A. L., Buck, K. N., and Barbeau, K. A. (2012). Quasi-Lagrangian drifter studies of iron speciation and cycling off point conception, California. Mar. Chem. 128, 1-12.
56. Koebnik, R., Bäumler, A. J., Heesemann, J., Braun,V., and Hantke, K. (1993a). The TonB protein of Yersinia ente-rocolitica and its interactions with TonB-box proteins. Mol. Gen. Genet. 237, 152-160.
57. Koebnik, R., Hantke, K., and Braun, V. (1993b). The TonB-dependent fer-richrome receptor FcuA of Yersinia enterocolitica: evidence against a strict co-evolution of receptor struc-ture and substrate specificity. Mol. Microbiol. 7, 383-393.
58. Kosman, D. J. (2003). Molecular mech-anisms of iron uptake in fungi. Mol. Microbiol. 47, 1185-1197.
59. Koster, M., Ovaa, W., Bitter, W., and Weisbeek, P. (1995). Multiple outer membrane receptors for uptake of ferric pseudobactins in Pseudomonas putida WCS358. Mol. Gen. Genet. 248, 735-743.
60. Kryazhimskiy, S., and Plotkin, J. B. (2008). The population genetics of dN/dS. PLoS Genet. 4, e1000304. doi:10.1371/journal.pgen.1000304
61. Kuma, K., Nakabayashi, S., Suzuki, Y., Kudo, I., and Matsunaga, K. (1992). Photo-reduction of Fe (III) by dis-solved organic substances and exis-tence of Fe(II) in seawater dur-ing spring blooms. Mar. Chem. 37, 15-27.
62. LaRoche, J., Boyd, P. W., McKay, R. M. L., and Geider, R. J. (1996). Flavo-doxin as an in situ marker for iron stress in phytoplankton. Nature 382, 802-805.
63. Lewis, L. A., Gray, E., Wang, Y. P., Roe, B. A., and Dyer, D. W. (1997). Molecular characteriza-tion of hpuAB, the haemoglobin-haptoglobin-utilization operon of Neisseria meningitidis. Mol. Micro-biol. 23, 737-749.
64. Liu, H. B., Landry, M. R., Vaulot, D., and Campbell, L. (1999). Prochlorococcus growth rates in the central equatorial Pacific: an application of the fmax approach. J. Geophys. Res. Oceans 104, 3391-3399.
65. Liu,H. B.,Nolla,H. A.,and Campbell,L. (1997). Prochlorococcus growth rate and contribution to primary pro-duction in the equatorial and sub-tropical North Pacific Ocean. Aquat. Microb. Ecol. 12, 39-47.
66. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, et al. (2004). ARB: a software envi-ronment for sequence data. Nucleic Acids Res. 32, 1363-1371.
67. Lynch, D., O'brien, J., Welch, T., Clarke, P., Cuiv, P. O., Crosa, J. H., et al. (2001). Genetic organization of the region encoding regulation, biosyn-thesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. J. Bacteriol. 183, 2576-2585.
68. Macrellis, H. M., Trick, C. G., Rue, E. L., Smith, G., and Bruland, K. W. (2001). Collection and detection of natural iron-binding ligands from seawater. Mar. Chem. 76, 175-187.
69. Martin, J. H., Coale, K. H., Johnson, K. S., Fitzwater, S. E., Gordon, R. M., Tanner, S. J., et al. (1994). Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 371, 123-129.
70. Martinez, J. S., and Butler, A. (2007). Marine amphiphilic siderophores: Marinobactin structure, uptake, and microbial partitioning. J. Inorg. Biochem. 101, 1692-1698.
71. Martinez, J. S., Zhang, G. P., Holt, P. D., Jung, H. T., Carrano, C. J., Haygood, M. G., et al. (2000). Self-assembling amphiphilic siderophores from marine bacteria. Science 287, 1245-1247.
72. Mawji, E., Gledhill, M., Milton, J. A., Tarran, G. A., Ussher, S., Thomp-son, A., et al. (2008). Hydroxam-ate siderophores: occurrence and importance in the Atlantic Ocean. Environ. Sci. Technol. 42, 8675-8680.
73. Mey, A. R., and Payne, S. M. (2001). Haem utilization in Vibrio cholerae involves multiple TonB-dependent haem receptors. Mol. Microbiol. 42, 835-849.
74. Meyer, F., Paarmann, D., D'souza, M., Olson, R., Glass, E. M., Kubal, M., et al. (2008). The metage-nomics RAST server -a public resource for the automatic phylo-genetic and functional analysis of metagenomes. BMC Bioinformat-ics 9, 386. doi:10.1186/1471-2105-9-386
75. Mochizuki, N., Tanaka, R., Grimm, B., Masuda, T., Moulin, M., Smith, A. G., et al. (2010). The cell biology of tetrapyrroles: a life and death strug-gle. Trends Plant Sci. 15, 488-498.
76. Ochsner, U. A., Johnson, Z., and Vasil, M. L. (2000). Genetics and regulation of two distinct haem-uptake systems, phu and has, in Pseudomonas aeruginosa. Microbiol-ogy 146, 185-198.
77. Olsen, G. J., Matsuda, H., Hagstrom, R., and Overbeek, R. (1994). fastD-NAml: a tool for construction of phylogenetic trees of DNA sequences using maximum likeli-hood. Comput. Appl. Biosci. 10, 41-48.
78. Palenik, B., Grimwood, J., Aerts, A., Rouze,P.,Salamov,A.,Putnam,N.,et al. (2007). The tiny eukaryote Ostre-ococcus provides genomic insights into the paradox of plankton specia-tion. Proc. Natl.Acad. Sci. U.S.A. 104, 7705-7710.
79. Palenik, B., Ren, Q. H., Dupont, C. L., Myers,G. S.,Heidelberg,J. F.,Badger, J. H., et al. (2006). Genome sequence of Synechococcus CC9311: insights into adaptation to a coastal environ-ment. Proc. Natl. Acad. Sci. U.S.A. 103, 13555-13559.
80. Plessner, O., Klapatch, T., and Guerinot, M. L. (1993). Siderophore uti-lization by Bradyrhizobium japon-icum. Appl. Environ. Microbiol. 59, 1688-1690.
81. Poole, K., and McKay, G. A. (2003). Iron acquisition and its control in Pseudomonas aeruginosa: many roads lead to Rome. Front. Biosci. 8, D661-D686.
82. Raes,J.,Letunic,I.,Yamada,T.,Jensen,L. J., and Bork, P. (2011). Toward mol-ecular trait-based ecology through integration of biogeochemical, geo-graphical and metagenomic data. Mol. Syst. Biol. 7, 473.
83. Rakin, A., Saken, E., Harmsen, D., and Heesemann, J. (1994). The pes-ticin receptor of Yersinia enterocol-itica: a novel virulence factor with dual function. Mol. Microbiol. 13, 253-263.
84. Reid, R. T., Live, D. H., Faulkner, D. J., and Butler, A. (1993). A siderophore from a marine bacterium with an exceptional ferric ion affinity con-stant. Nature 366, 455-458.
85. Rue, E. L., and Bruland, K. W. (1995). Complexation of iron(III) by nat-ural organic ligands in the Central North Pacific as determined by a new competitive ligand equilibra-tion/adsorptive cathodic stripping voltammetric method. Mar. Chem. 50, 117-138.
86. Rusch, D. B., Halpern, A. L., Sutton, G., Heidelberg, K. B., Williamson, S., Yooseph, S., et al. (2007). The sorcerer II global ocean sampling expedition: Northwest Atlantic through Eastern Trop-ical Pacific. PLoS Biol. 5, e77. doi:10.1371/journal.pbio.0050077
87. Rusch, D. B., Martiny, A. C., Dupont, C. L., Halpern, A. L., and Ven-ter, J. C. (2010). Characterization of Prochlorococcus clades from iron-depleted oceanic regions. Proc. Natl. Acad. Sci. U.S.A. 107, 16184-16189.
88. Sanders, J. D., Cope, L. D., Muller-Eberhard, U., and Hansen, E. J. (1994). Identification of a locus involved in the utilization of iron by Haemophilus influenzae. Infect. Immun. 62, 4515-4525.
89. Schroder, I., Johnson, E., and De Vries, S. (2003). Microbial ferric iron reductases. FEMS Microbiol. Rev. 27, 427-447.
90. Seshadri, R., Kravitz, S. A., Smarr, L., Gilna, P., and Frazier, M. (2007). CAMERA: a community resource for metagenomics. PLoS Biol. 5, e75. doi:10.1371/journal.pbio.0050075
91. Smith, D. P., Kitner, J. B., Norbeck,A. D., Clauss, T. R., Lipton, M. S., Schwal-bach, M. S., et al. (2010). Tran-scriptional and translational reg-ulatory responses to iron limita-tion in the globally distributed marine bacterium Candidatus Pelag-ibacter ubique. PLoS ONE 5, e10487. doi:10.1371/journal.pone.0010487
92. Srivastava, P. K., Desai, D. K., Nandi, S., and Lynn, A. M. (2007). HMM-ModE -improved classification using profile hidden Markov mod-els by optimising the discrimination threshold and modifying emission probabilities with negative training sequences. BMC Bioinformatics 8, 104. doi:10.1186/1471-2105-8-104
93. Stojiljkovic, I., and Hantke, K. (1994). Transport of haemin across the cytoplasmic membrane through a haemin-specific periplasmic binding-protein-dependent trans-port system in Yersinia enterocolitica. Mol. Microbiol. 13, 719-732.
94. Szklarczyk, D., Franceschini, A., Kuhn, M., Simonovic, M., Roth, A., Minguez, P., et al. (2011). The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 39, D561-D568.
95. Tai, V., Poon, A. F. Y., Paulsen, I. T., and Palenik, B. (2011). Selec-tion in coastal Synechococcus (Cyanobacteria) populations evaluated from environmental metagenomes. PLoS ONE 6, e24249. doi:10.1371/journal.pone.0024249
96. Thompson, A. W., Huang, K., Saito, M. A., and Chisholm, S. W. (2011). Transcriptome response of high-and low-light-adapted Prochlorococcus strains to chang-ing iron availability. ISME J. 5, 1580-1594.
97. Thompson, J. M., Jones, H. A., and Perry, R. D. (1999). Molecular char-acterization of the hemin uptake locus (hmu) from Yersinia pestis and analysis of hmu mutants for hemin and hemoprotein utilization. Infect. Immun. 67, 3879-3892.
98. Toulza, E., Tagliabue, A., Blain, S., and Piganeau, G. (2012). Analy-sis of the Global Ocean Sam-pling (GOS) Project for trends in iron uptake by surface ocean microbes. PLoS ONE 7, e30931. doi:10.1371/journal.pone.0030931
99. Tsuda,A.,Takeda,S.,Saito,H.,Nishioka, J., Nojiri, Y., Kudo, I., et al. (2003). A mesoscale iron enrichment in the Western Subarctic Pacific induces a large centric diatom bloom. Science 300, 958-961.
100. Vanderpool, C. K., and Armstrong, S. K. (2003). Heme-responsive transcrip-tional activation of Bordetella bhu genes. J. Bacteriol. 185, 909-917.
101. Velasquez, I., Nunn, B. L., Ibisanmi, E., Goodlett, D. R., Hunter, K. A., and Sander, S. G. (2011). Detec-tion of hydroxamate siderophores in coastal and Sub-Antarctic waters off the South Eastern Coast of New Zealand. Mar. Chem. 126, 97-107.
102. Vichi, M., Masina, S., and Navarra, A. (2007a). A generalized model of pelagic biogeochem-istry for the global ocean ecosystem. Part II: numerical simulations. J. Mar. Syst. 64, 110-134.
103. Vichi, M., Pinardi, N., and Masina, S. (2007b). A generalized model of pelagic biogeochemistry for the global ocean ecosystem. Part I: theory. J. Mar. Syst. 64, 89-109.
104. Waterbury, J. B., Watson, S. W., Guil-lard,R. R. L.,and Brand,L. E. (1979). Widespread occurrence of a unicel-lular, marine, planktonic cyanobac-terium. Nature 277, 293-294.
105. Webb, E. A., Moffett, J. W., and Water-bury,J. B. (2001). Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodesmium, and Crocosphaera spp.): identification of the IdiA pro-tein. Appl. Environ. Microbiol. 67, 5444-5452.
106. Wexler, M., Todd, J. D., Kolade, O., Bellini, D., Hemmings, A. M., Saw-ers, G., et al. (2003). Fur is not the global regulator of iron uptake genes in Rhizobium leguminosarum. Microbiology 149, 1357-1365.
107. Wilhelm, S. W., and Trick, C. G. (1994). Iron-limited growth of cyanobacteria: multiple siderophore production is a com-mon response. Limnol. Oceanogr. 39, 1979-1984.
108. Worsham, P. L., and Konisky, J. (1985). Locus affecting regulation of the col-icin I receptor by iron. J. Bacteriol. 161, 428-431.
109. Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591.