The Ferrojan horse hypothesis: Iron-virus interactions in the ocean

Frontiers in Marine Science

Volumn 3, Issue JUN, 2016, Pages

  Bonnain, Chelsea ^a   Breitbart, Mya ^a   Buck, Kristen N ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Bacteria; Infection; Iron; Ligand; Marine; Phage; Siderophore; Virus

Indexed keywords

EID: 85008940770     PISSN: None     EISSN: 22967745     Source Type: Journal    
DOI: 10.3389/fmars.2016.00082     Document Type: Article

References (119)

1. Aguilar-Islas, A. M., Wu, J., Rember, R., Johansen, A. M., and Shank, L. M. (2010). Dissolution of aerosol-derived iron in seawater: leach solution chemistry, aerosol type, and colloidal iron fraction. Mar. Chem. 120, 25-33. doi: 10.1016/j.marchem.2009.01.011
2. Andriolo, J. M., Hensleigh, R. M., McConnell, C. A., Pedulla, M., Hailer, K., Kasinath, R., et al. (2014). Iron-doped apatite nanoparticles for improvement of phage therapy. J. Vac. Sci. Technol. B 32:06FD01. doi: 10.1116/1.4894460
3. Barasch, J., and Mori, K. (2004). Cell biology-iron thievery. Nature 432, 811-813. doi: 10.1038/432811a
4. Barber, M. F., and Elde, N. C. (2014). Escape from bacterial iron piracy through rapid evolution of transferrin. Science 346, 1362-1366. doi: 10.1126/science.1259329
5. Bartual, S. G., Otero, J. M., Garcia-Doval, C., Llamas-Saiz, A. L., Kahn, R., Fox, G. C., et al. (2010). Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proc. Natl. Acad. Sci. U.S.A. 107, 20287-20292. doi: 10.1073/pnas.1011218107
6. Bergquist, B. A., Wu, J., and Boyle, E. A. (2007). Variability in oceanic dissolved iron is dominated by the colloidal fraction. Geochim. Cosmochim. Acta 71, 2960-2974. doi: 10.1016/j.gca.2007.03.013
7. Biller, D. V., and Bruland, K. W. (2012). Analysis of Mn, Fe, Co, Ni, Cu, Zn, Cd, and Pb in seawater using the Nobias-chelate PA1 resin and magnetic sector inductively coupled plasma mass spectrometry (ICP-MS). Mar. Chem. 130, 12-20. doi: 10.1016/j.marchem.2011.12.001
8. Bonhivers, M., Ghazi, A., Boulanger, P., and Letellier, L. (1996). FhuA, a transporter of the Escherichia coli outer membrane, is converted into a channel upon binding of bacteriophage T5. EMBO J. 15, 1850-1856.
9. Boyd, P. W., and Ellwood, M. J. (2010). The biogeochemical cycle of iron in the ocean. Nat. Geosci. 3, 675-682. doi: 10.1038/ngeo964
10. Boyd, P. W., Ibisanmi, E., Sander, S. G., Hunter, K. A., and Jackson, G. A. (2010). Remineralization of upper ocean particles: implications for iron biogeochemistry. Limnol. Oceanogr. 55, 1271-1288. doi: 10.4319/lo.2010.55.3.1271
11. Brand, L. E. (1991). Minimum iron requirements of marine-phytoplankton and the implications for the biogeochemical control of new productuon. Limnol. Oceanogr. 36, 1756-1771.
12. Braun, V. (2009). FhuA (TonA), the career of a protein. J. Bacteriol. 191, 3431-3436. doi: 10.1128/JB.00106-09
13. Braun, V., Bos, C., Braun, M., and Killmann, H. (2001). Outer membrane channels and active transporters for the uptake of antibiotics. J. Infect. Dis. 183, S12-S16. doi: 10.1086/318840
14. Braun, V., and Endriss, F. (2007). Energy-coupled outer membrane transport proteins and regulatory proteins. Biometals 20, 219-231. doi: 10.1007/s10534-006-9072-5
15. Braun, V., Hancock, R. E. W., Hantke, K., and Hartmann, A. (1976). Functional organization of outer membrane of Escherichia coli-phage and colicin receptors as components of iron uptake systems. J. Supramol. Struct. 5, 37-58. doi: 10.1002/jss.400050105
16. Braun, V., Schaller, K., and Wolff, H. (1973). Common receptor protein for phage T5 and colicin M in outer membrane of Escherichia coli B. Biochim. Biophys. Acta 323, 87-97. doi: 10.1016/0005-2736(73)90433-1
17. Breitbart, M. (2012). Marine viruses: truth or dare. Annu. Rev. Mar. Sci. 4, 425-448. doi: 10.1146/annurev-marine-120709-142805
18. Breitbart, M., Thompson, L. R., Suttle, C. A., and Sullivan, M. B. (2007). Exploring the vast diversity of marine viruses. Oceanography 20, 135-139. doi: 10.5670/oceanog.2007.58
19. Browning, C., Shneider, M. M., Bowman, V. D., Schwarzer, D., and Leiman, P. G. (2012). Phage pierces the host cell membrane with the iron-loaded spike. Structure 20, 326-339. doi: 10.1016/j.str.2011.12.009
20. Bruland, K. W., Donat, J. R., and Hutchins, D. A. (1991). Interactive influences of bioactive trace-metals on biological production in oceanic waters. Limnol. Oceanogr. 36, 1555-1577. doi: 10.4319/lo.1991.36.8.1555
21. Brum, J. R., Schenck, R. O., and Sullivan, M. B. (2013). Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses. ISME J. 7, 1738-1751. doi: 10.1038/ismej.2013.67
22. Buck, K. N., Sohst, B., and Sedwick, P. N. (2015). The organic complexation of dissolved iron along the US GEOTRACES (GA03) North Atlantic Section. Deep-Sea Res. Part II-Top. Stud. Oceanogr. 116, 152-165. doi: 10.1016/j.dsr2.2014.11.016
23. Butler, A. (2005). Marine siderophores and microbial iron mobilization. Biometals 18, 369-374. doi: 10.1007/s10534-005-3711-0
24. Byrne, R. H., and Breland, J. A. (1989). High-precision multiwavelength pH determinations in seawater using cresol red. Deep-Sea Res. Part A-Oceanogr. Res. Pap. 36, 803-810. doi: 10.1016/0198-0149(89)90152-0
25. Chuprov-Netochin, R. N., Faizullina, N. M., Sykilinda, N. N., Simakova, M. N., Mesyanzhinov, V. V., and Miroshnikov, K. A. (2010). The beta-helical domain of bacteriophage T4 controls the folding of the fragment of long tail fibers in a chimeric protein. Russ. J. Bioorganic Chem. 36, 172-178. doi: 10.1134/S1068162010020056
26. Cornelis, P. (2010). Iron uptake and metabolism in pseudomonads. Appl. Microbiol. Biotechnol. 86, 1637-1645. doi: 10.1007/s00253-010-2550-2
27. Cullen, J. T., Bergquist, B. A., and Moffett, J. W. (2006). Thermodynamic characterization of the partitioning of iron between soluble and colloidal species in the Atlantic Ocean. Mar. Chem. 98, 295-303. doi: 10.1016/j.marchem.2005.10.007
28. Daughney, C. J., Chatellier, X., Chan, A., Kenward, P., Fortin, D., Suttle, C. A., et al. (2004). Adsorption and precipitation of iron from seawater on a marine bacteriophage (PWH3A-P1). Mar. Chem. 91, 101-115. doi: 10.1016/j.marchem.2004.06.003
29. Demogines, A., Abraham, J., Choe, H., Farzan, M., and Sawyer, S. L. (2013). Dual host-virus arms races shape an essential housekeeping protein. PLoS Biol. 11:e1001571. doi: 10.1371/journal.pbio.1001571
30. Drakesmith, H., and Prentice, A. M. (2012). Hepcidin and the iron-infection axis. Science 338, 768-772. doi: 10.1126/science.1224577
31. Ducklow, H. (2000). "Bacterial production and biomass in the oceans, " in Microbial Ecology of the Oceans, ed D. L. Kirchman (New York, NY: Wiley-Liss Inc.), 85-120.
32. Emerson, D. (2016). The irony of iron-biogenic iron oxides as an iron source to the ocean. Front. Microbiol. 6:1502. doi: 10.3389/fmicb.2015.01502
33. Finn, R. D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R. Y., Eddy, S. R., et al. (2014). Pfam: the protein families database. Nucleic Acids Res. 42, D222-D230. doi: 10.1093/nar/gkt1223
34. Fishwick, M. P., Sedwick, P. N., Lohan, M. C., Worsfold, P. J., Buck, K. N., Church, T. M., et al. (2014). The impact of changing surface ocean conditions on the dissolution of aerosol iron. Global Biogeochem. Cycles 28, 1235-1250. doi: 10.1002/2014GB004921
35. Fitzsimmons, J. N., and Boyle, E. A. (2014). Both soluble and colloidal iron phases control dissolved iron variability in the tropical North Atlantic Ocean. Geochim. Cosmochim. Acta 125, 539-550. doi: 10.1016/j.gca.2013.10.032
36. Fitzsimmons, J. N., Bundy, R. M., Al-Subiai, S. N., Barbeau, K. A., and Boyle, E. A. (2015). The composition of dissolved iron in the dusty surface ocean: an exploration using size-fractionated iron-binding ligands. Mar. Chem. 173, 125-135. doi: 10.1016/j.marchem.2014.09.002
37. Fuhrman, J. (1999). Marine viruses: biogeochemical and ecological effects. Nature 399, 541-548. doi: 10.1038/21119
38. Gauglitz, J. M., Inishi, A., Ito, Y., and Butler, A. (2014). Microbial tailoring of acyl peptidic siderophores. Biochemistry 53, 2624-2631. doi: 10.1021/bi500266x
39. Gerringa, L. J. A., Rijkenberg, M. J. A., Schoemann, V., Laan, P., and de Baar, H. J. W. (2015). Organic complexation of iron in the West Atlantic Ocean. Mar. Chem. 177, 434-446. doi: 10.1016/j.marchem.2015.04.007
40. 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
41. Gledhill, M., and van den Berg, C. M. G. (1994). Determination of complexation of iron (III) with natural organic complexing ligands in seawater using cathodic stripping voltammetry. Mar. Chem. 47, 41-54. doi: 10.1016/0304-4203(94)90012-4
42. Gobler, C. J., Hutchins, D. A., Fisher, N. S., Cosper, E. M., and Sanudo-Wilhelmy, S. A. (1997). Release and bioavailability of C, N, P Se, and Fe following viral lysis of a marine chrysophyte. Limnol. Oceanogr. 42, 1492-1504. doi: 10.4319/lo.1997.42.7.1492
43. Gordon, R. M., Martin, J. H., and Knauer, G. A. (1982). Iron in Northeast Pacific waters. Nature 299, 611-612. doi: 10.1038/299611a0
44. Hantke, K., and Braun, V. (1975). Membrane receptor dependent iron transport in Escherichia coli. FEBS Lett. 49, 301-305. doi: 10.1016/0014-5793(75)80771-X
45. Hantke, K., and Braun, V. (1978). Functional interaction of TonA-TonB receptor system in Escherichia-coli. J. Bacteriol. 135, 190-197.
46. Hassler, C. S., Alasonati, E., Nichols, C. A. M., and Slaveykova, V. I. (2011). Exopolysaccharides produced by bacteria isolated from the pelagic Southern Ocean-role in Fe binding, chemical reactivity, and bioavailability. Mar. Chem. 123, 88-98. doi: 10.1016/j.marchem.2010.10.003
47. Hershey, A. D., and Chase, M. (1952). Independent functions of viral protein and nucleic acid in growth of bacteriophage. J. Gen. Physiol. 36, 39-56. doi: 10.1085/jgp.36.1.39
48. Hider, R. C., and Kong, X. (2010). Chemistry and biology of siderophores. Nat. Prod. Rep. 27, 637-657. doi: 10.1039/b906679a
49. Humphrey, W., Dalke, A., and Schulten, K. (1996). VMD: visual molecular dynamics. J. Mol. Graphics 14, 33-38. doi: 10.1016/0263-7855(96)00018-5
50. 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. doi: 10.1071/EN07012
51. Johnson, K. S., Gordon, R. M., and Coale, K. H. (1997). What controls dissolved iron concentrations in the world ocean? Mar. Chem. 57, 137-161.
52. Jover, L. F., Effler, T. C., Buchan, A., Wilhelm, S. W., and Weitz, J. S. (2014). The elemental composition of virus particles: implications for marine biogeochemical cycles. Nat. Rev. Microbiol. 12, 519-528. doi: 10.1038/nrmicro3289
53. Kadner, R. J., Heller, K., Coulton, J. W., and Braun, V. (1980). Genetic control of hydroxamate-mediated iron uptake in Escherichia coli. J. Bacteriol. 143, 256-264.
54. King, J. (1968). Assembly of tail of bacteriophage T4. J. Mol. Biol. 32, 231-262. doi: 10.1016/0022-2836(68)90007-7
55. Kuma, K., Nishioka, J., and Matsunaga, K. (1996). Controls on iron(III) hydroxide solubility in seawater: the influence of pH and natural organic chelators. Limnol. Oceanogr. 41, 396-407. doi: 10.4319/lo.1996.41.3.0396
56. Laglera, L. M., Battaglia, G., and van den Berg, C. M. G. (2007). Determination of humic substances in natural waters by cathodic stripping voltammetry of their complexes with iron. Anal. Chim. Acta 599, 58-66. doi: 10.1016/j.aca.2007.07.059
57. Laglera, L. M., Battaglia, G., and van den Berg, C. M. G. (2011). Effect of humic substances on the iron speciation in natural waters by CLE/CSV. Mar. Chem. 127, 134-143. doi: 10.1016/j.marchem.2011.09.003
58. Laglera, L. M., and van den Berg, C. M. G. (2009). Evidence for geochemical control of iron by humic substances in seawater. Limnol. Oceanogr. 54, 610-619. doi: 10.4319/lo.2009.54.2.0610
59. Leiman, P. G., Arisaka, F., van Raaij, M. J., Kostyuchenko, V. A., Aksyuk, A. A., Kanamaru, S., et al. (2010). Morphogenesis of the T4 tail and tail fibers. Virol. J. 7, 1-28. doi: 10.1186/1743-422X-7-355
60. Leiman, P. G., and Shneider, M. M. (2012). Contractile tail machines of bacteriophages. Viral Mol. Mach. 726, 93-114. doi: 10.1007/978-1-4614-0980-9_5
61. Luckey, M., Wayne, R., and Neilands, J. B. (1975). In vitro competition between ferrichrome and phage for outer membrane T5 receptor complex of Escherichia coli. Biochem. Biophys. Res. Commun. 64, 687-693. doi: 10.1016/0006-291X(75)90375-7
62. Lundrigan, M. D., Lancaster, J. H., and Earhart, C. F. (1983). UC-1, a new bacteriophage that uses the TonA polypeptide as its receptor. J. Virol. 45, 700-707.
63. Luria, S. E., and Delbruck, M. (1943). Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28, 491-511.
64. Maldonado, M. T., and Price, N. M. (1999). Utilization of iron bound to strong organic ligands by plankton communities in the subarctic Pacific Ocean. Deep-Sea Res. Part II-Top. Stud. Oceanogr. 46, 2447-2473. doi: 10.1016/S0967-0645(99)00071-5
65. Mancuso Nichols, C. A., Garon, S., Bowman, J. P., Raguenes, G., and Guezennec, J. (2004). Production of exopolysaccharides by Antarctic marine bacterial isolates. J. Appl. Microbiol. 96, 1057-1066. doi: 10.1111/j.1365-2672.2004.02216.x
66. Martin, J. H., Gordon, R. M., Fitzwater, S., and Broenkow, W. W. (1989). VERTEX-Phytoplankton iron studies in the Gulf of Alaska. Deep-Sea Res. Part A-Oceanogr. Res. Pap. 36, 649-680. doi: 10.1016/0198-0149(89)90144-1
67. Martinez, J. S., Carter-Franklin, J. N., Mann, E. L., Martin, J. D., Haygood, M. G., and Butler, A. (2003). Structure and membrane affinity of a suite of amphiphilic siderophores produced by a marine bacterium. Proc. Natl. Acad. Sci. U.S.A. 100, 3754-3759. doi: 10.1073/pnas.0637444100
68. Matzanke, B. F., Bohnke, R., Mollmann, U., Reissbrodt, R., Schunemann, V., and Trautwein, A. X. (1997). Iron uptake and intracellular metal transfer in mycobacteria mediated by xenosiderophores. Biometals 10, 193-203. doi: 10.1023/A:1018351728081
69. Mawji, E., Gledhill, M., Milton, J. A., Tarran, G. A., Ussher, S., Thompson, A., et al. (2008). Hydroxamate siderophores: occurrence and importance in the Atlantic Ocean. Environ. Sci. Technol. 42, 8675-8680. doi: 10.1021/es801884r
70. Mawji, E., Schlitzer, R., Dodas, E. M., Abadie, C., Abouchami, W., Anderson, R. F., et al. (2015). The GEOTRACES intermediate data product 2014. Mar. Chem. 177, 1-8. doi: 10.1016/j.marchem.2015.04.005
71. May, P. M., Linder, P. W., and Williams, D. R. (1977). Computer simulation of metal-ion equilibria in biofluids: models for the low-molecular-weight complex distribution of calcium(II), magnesium(II), manganese(II), iron(III), copper(II), zinc(II), and lead(II) ions in human blood plasma. J. Chem. Soc. Dalton Trans. 6, 588-595. doi: 10.1039/dt9770000588
72. Mioni, C. E., Poorvin, L., and Wilhelm, S. W. (2005). Virus and siderophore-mediated transfer of available Fe between heterotrophic bacteria: characterization using an Fe-specific bioreporter. Aquat. Microb. Ecol. 41, 233-245. doi: 10.3354/ame041233
73. Morel, F. M. M., and Price, N. M. (2003). The biogeochemical cycles of trace metals in the oceans. Science 300, 944-947. doi: 10.1126/science.1083545
74. Neilands, J. B. (1957). Some aspects of microbial metabolism. Bacteriol. Rev. 21, 101-111.
75. Neilands, J. B. (1979). Ironic function of bacteriophage receptors. Trends Biochem. Sci. 4, 115-118. doi: 10.1016/0968-0004(79)90396-7
76. Nishioka, J., Takeda, S., Wong, C. S., and Johnson, W. K. (2001). Size-fractionated iron concentrations in the northeast Pacific Ocean: distribution of soluble and small colloidal iron. Mar. Chem. 74, 157-179. doi: 10.1016/S0304-4203(01)00013-5
77. Parada, V., Herndl, G. J., and Weinbauer, M. G. (2006). Viral burst size of heterotrophic prokaryotes in aquatic systems. J. Mar. Biol. Assoc. U.K. 86, 613-621. doi: 10.1017/S002531540601352X
78. Parsons, R. J., Breitbart, M., Lomas, M. W., and Carlson, C. A. (2012). Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J. 6, 273-284. doi: 10.1038/ismej.2011.101
79. Pawelek, P. D., Croteau, N., Ng-Thow-Hing, C., Khursigara, C. M., Moiseeva, N., Allaire, M., et al. (2006). Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science 312, 1399-1402. doi: 10.1126/science.1128057
80. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., et al. (2004). UCSF chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612. doi: 10.1002/jcc.20084
81. Poon, A. P. W., and Dhillon, T. S. (1987). The attachment sites of T5-host range temperate coliphages. Virology 158, 431-434. doi: 10.1016/0042-6822(87)90215-7
82. Poorvin, L., Rinta-Kanto, J., Hutchins, D., and Wilhelm, S. (2004). Viral release of iron and its bioavailability to marine plankton. Limnol. Oceanogr. 49, 1734-1741. doi: 10.4319/lo.2004.49.5.1734
83. Rabsch, W., Ma, L., Wiley, G., Najar, F. Z., Kaserer, W., Schuerch, D. W., et al. (2007). FepA-and TonB-dependent bacteriophage H8: receptor binding and genomic sequence. J. Bacteriol. 189, 5658-5674. doi: 10.1128/JB.00437-07
84. 2-evolving organisms. Photosyn. Res. 60, 111-149. doi: 10.1023/A:1006282714942
85. Redfield, A. C. (1958). The biological control of chemical factors in the environment. Am. Sci. 46, 205-221.
86. Rohwer, F., Segall, A., Steward, G., Seguritan, V., Breitbart, M., Wolven, F., et al. (2000). The complete genomic sequence of the marine phage Roseophage SIO1 shares homology with nonmarine phages. Limnol. Oceanogr. 45, 408-418. doi: 10.4319/lo.2000.45.2.0408
87. Rohwer, F., and Segall, A. M. (2015). In retrospect: a century of phage lessons. Nature 528, 46-48. doi: 10.1038/528046a
88. Rohwer, F., and Thurber, R. V. (2009). Viruses manipulate the marine environment. Nature 459, 207-212. doi: 10.1038/nature08060
89. Rohwer, F., Youle, M., Maughan, H., and Hisakawa, N. (2014). Life in Our Phage World: A Centennial Field Guide to the Earth's Most Diverse Inhabitants. San Diego, CA: Wholon.
90. Rue, E., and Bruland, K. (2001). Domoic acid binds iron and copper: a possible role for the toxin produced by the marine diatom Pseudo-nitzschia. Mar. Chem. 76, 127-134. doi: 10.1016/S0304-4203(01)00053-6
91. Rue, E. L., and Bruland, K. W. (1995). Complexation of iron(III) by natural organic-ligands in the central north Pacific as determined by a new competitive ligand equilibration adsorptive cathodic stripping voltammetric method. Mar. Chem. 50, 117-138. doi: 10.1016/0304-4203(95)00031-L
92. Rue, E. L., and Bruland, K. W. (1997). The role of organic complexation on ambient iron chemistry in the equatorial Pacific Ocean and the response of a mesoscale iron addition experiment. Limnol. Oceanogr. 42, 901-910. doi: 10.4319/lo.1997.42.5.0901
93. Salmond, G. P. C., and Fineran, P. C. (2015). A century of the phage: past, present and future. Nat. Rev. Microbiol. 13, 777-786. doi: 10.1038/nrmicro3564
94. Samson, J. E., Magadan, A. H., Sabri, M., and Moineau, S. (2013). Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11, 675-687. doi: 10.1038/nrmicro3096
95. Sandy, M., and Butler, A. (2009). Microbial iron acquisition: marine and terrestrial siderophores. Chem. Rev. 109, 4580-4595. doi: 10.1021/cr9002787
96. Shaked, Y., and Lis, H. (2012). Disassembling iron availability to phytoplankton. Front. Microbiol. 3:123. doi: 10.3389/fmicb.2012.00123
97. Shire, D. M., and Kustka, A. B. (2015). Luxury uptake, iron storage and ferritin abundance in Prochlorococcus marinus (Synechococcales) strain MED4. Phycologia 54, 398-406. doi: 10.2216/14-109.1
98. Host receptors for bacteriophage adsorption
99. Stern, A., and Sorek, R. (2011). The phage-host arms race: shaping the evolution of microbes. Bioessays 33, 43-51. doi: 10.1002/bies.201000071
100. Stolpe, B., and Hassellov, M. (2010). Nanofibrils and other colloidal biopolymers binding trace elements in coastal seawater: significance for variations in element size distributions. Limnol. Oceanogr. 55, 187-202. doi: 10.4319/lo.2010.55.1.0187
101. Sullivan, M. B., Coleman, M. L., Weigele, P., Rohwer, F., and Chisholm, S. W. (2005). Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol. 3:e144. doi: 10.1371/journal.pbio.0030144
102. Suttle, C. A. (2007). Marine viruses-major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801-812. doi: 10.1038/nrmicro1750
103. Tam, W., Pell, L. G., Bona, D., Tsai, A., Dai, X. X., Edwards, A. M., et al. (2013). Tail tip proteins related to bacteriophage lambda gpL coordinate an iron-sulfur cluster. J. Mol. Biol. 425, 2450-2462. doi: 10.1016/j.jmb.2013.03.032
104. Thomassen, E., Gielen, G., Schutz, M., Schoehn, G., Abrahams, J. P., Miller, S., et al. (2003). The structure of the receptor-binding domain of the bacteriophage T4 short tail fibre reveals a knitted trimeric metal-binding fold. J. Mol. Biol. 331, 361-373. doi: 10.1016/S0022-2836(03)00755-1
105. Thuroczy, C. E., Gerringa, L. J. A., Klunder, M. B., Middag, R., Laan, P., Timmermans, K. R., et al. (2010). Speciation of Fe in the Eastern North Atlantic Ocean. Deep-Sea Res. Part I-Oceanogr. Res. Pap. 57, 1444-1453. doi: 10.1016/j.dsr.2010.08.004
106. Tortell, P. D., Maldonado, M. T., Granger, J., and Price, N. M. (1999). Marine bacteria and biogeochemical cycling of iron in the oceans. FEMS Microbiol. Ecol. 29, 1-11. doi: 10.1111/j.1574-6941.1999.tb00593.x
107. Tortell, P. D., Maldonado, M. T., and Price, N. M. (1996). The role of heterotrophic bacteria in iron-limited ocean ecosystems. Nature 383, 330-332. doi: 10.1038/383330a0
108. Twining, B. S., and Baines, S. B. (2013). The trace metal composition of marine phytoplankton. Annu. Rev. Mar. Sci. 5, 191-215. doi: 10.1146/annurev-marine-121211-172322
109. van den Berg, C. M. G. (2005). Organic iron complexation is real, the theory is used incorrectly. Comment on 'Measuring marine iron(III) complexes by CLE-AdSV'. Environ. Chem. 2, 88-89. doi: 10.1071/EN05029
110. Van Valen, L. (1973). A new evolutionary law. Evol. Theor. 1, 1-30.
111. von der Heyden, B. P., Hauser, E. J., Mishra, B., Martinez, G. A., Bowie, A. R., Tyliszczak, T., et al. (2014). Ubiquitous presence of Fe(II) in aquatic colloids and its association with organic carbon. Environ. Sci. Technol. Lett. 1, 387-392. doi: 10.1021/ez500164v
112. Vraspir, J. M., and Butler, A. (2009). Chemistry of marine ligands and siderophores. Annu. Rev. Mar. Sci. 1, 43-63. doi: 10.1146/annurev.marine.010908.163712
113. Wayne, R., and Neilands, J. B. (1975). Evidence for common binding-sites for ferrichrome compounds and bacteriophage Phi-80 in cell-envelope of Escherichia coli. J. Bacteriol. 121, 497-503.
114. Wheeler, T. J., Clements, J., and Finn, R. D. (2014). Skylign. BMC Bioinform. 15:7. doi: 10.1186/1471-2105-15-7
115. Wilhelm, S. W., and Suttle, C. A. (1999). Viruses and nutrient cycles in the sea. Bioscience 49, 781-783. doi: 10.2307/1313569
116. Wilhelm, S. W., Weinbauer, M. G., Suttle, C. A., and Jeffrey, W. H. (1998). The role of sunlight in the removal and repair of viruses in the sea. Limnol. Oceanogr. 43, 586-592. doi: 10.4319/lo.1998.43.4.0586
117. Wommack, K. E., and Colwell, R. R. (2000). Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69-114. doi: 10.1128/MMBR.64.1.69-114.2000
118. Wommack, K. E., Nasko, D. J., Chopyk, J., and Sakowski, E. G. (2015). Counts and sequences, observations that continue to change our understanding of viruses in nature. J. Microbiol. 53, 181-192. doi: 10.1007/s12275-015-5068-6
119. Yamashita, E., Nakagawa, A., Takahashi, J., Tsunoda, K.-I., Yamada, S., and Takeda, S. (2011). The host-binding domain of the P2 phage tail spike reveals a trimeric iron-binding structure. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67, 837-841. doi: 10.1107/s1744309111005999