Consideration of the bioavailability of iron in the North American Great Lakes: Development of novel approaches toward understanding iron biogeochemistry

Authors

  • R. Michael L. McKay Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403
  • George S. Bullerjahn Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403
  • David Porta Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403
  • Erik T. Brown Large Lakes Observatory, University of Minnesota, Duluth, MN 55812
  • Robert M. Sherrell Institute of Marine and Coastal Sciences and Department of Geological Sciences, Rutgers University, New Brunswick, NJ 08901
  • Tanya M. Smutka Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN 55108
  • Robert W. Sterner Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN 55108
  • Michael R. Twiss Department of Biology, Clarkson University, Potsdam, NY 13699
  • Steven W. Wilhelm Department of Microbiology, The University of Tennessee, Knoxville, TN 37996

Keywords:

bioreporter, ferredoxin, flavodoxin, fluorescence, Lake Superior, phytoplankton, trace metal speciation

Abstract

There is increasing recognition that iron distribution and availability is significant in terms of global oceanic production. Low availability of iron and other nutritive trace metals may also constrain productivity in the North American Great Lakes. Despite its importance, the biogeochemistry of iron in the water column of lacustrine systems remains poorly characterized. In addressing the current state of iron biogeochemistry, a workshop organized a decade ago at the Bermuda Biological Station for Research brought together a cross-disciplinary team of chemists and biologists who sought to synthesize current knowledge and identify research priorities in this field. Key among goals identified during the workshop, and one that remains today for the most part unfulfilled, was to ‘develop techniques to quantify those fractions of Fe that are accessible to phytoplankton.’ Here we review recent progress toward meeting this objective, drawing on specific examples from Lake Superior where these approaches have been applied.

References

Aiken, G. R., McKnight, D. M., Wershaw, R. L. and MacCarthy, P. 1985. Humic Substances in Soil, Sediment, and Water. Geochemistry, Isolation, and Characterization, New York, NY: John Wiley & Sons.

Auclair, J. C. 1995. Implications of increased UV-B induced photoreduction: iron(II) enrichment stimulates picocyanobacterial growth and the microbial food web in clear-water acidic Canadian Shield lakes. Can. J. Fish. Aquat. Sci., 52: 1782–1788.

Bachmann, T. T. 2003. Transforming cyanobacteria into bioreporters of biological relevance. Trends Biotechnol., 21: 247–249. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=12788542http://www4.infotrieve.com/newmedline/detail.asp?NameID=12788542&Session=&searchQuery=Trends+Biotechnol%2E%5BJournal+Name%5D+AND+21%5BVolume%5D+AND+247%5BPage+Number%5D+AND+2003%5BPublication+Date%5D+AND+Bachmann%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1016%2FS0167-7799%2803%2900114-8

Banse, K. 1991. Rates of phytoplankton cell division in the field and in iron enrichment experiments. Limnol. Oceanogr., 36: 1886–1898.

Behrenfeld, M. J., Bale, A. J., Kolber, Z. S., Aiken, J. and Falkowski, P. G. 1996. Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature (Lond.), 383: 508–511. http://dx.doi.org/10.1038%2F383508a0

Boyd, P. W., Aiken, J. and Kolber, Z. 1997. Comparison of radiocarbon and fluorescence based (pump and probe) measurements of phytoplankton photosynthetic characteristics in the Northeast Atlantic Ocean. Mar. Ecol. Prog. Ser., 149: 215–226.

Boyd, P. W., Watson, A., Law, C. S., Abraham, E., Trull, T., Murdoch, R., Bakker, D. C. E., Bowie, A. R., Buesler, K. O., Chang, H., Charette, M., Croot, P., Downing, K., Frew, R., Gall, M., Hadfield, R., Hall, J., Harvey, M., Jameson, G., La Roche, J., Liddicoat, M., Ling, R., Maldonado, M., McKay, R. M., Nodder, S., Pickmere, S., Pridmore, R., Rintoull, S., Safi, K., Sutton, P., Strzepek, R., Tannenberger, K., Turner, S., Waite, A. and Zeldis, J. 2000. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature (Lond.), 407: 695–702. http://dx.doi.org/10.1038%2F35037500

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.

Byrne, R. H. and Kester, D. R. 1976. Solubility of hydrous ferric oxide and iron speciation in sea water. Mar. Chem., 4: 255–274. http://dx.doi.org/10.1016%2F0304-4203%2876%2990012-8

Byrne, R. H., Luo, Y.-R. and Young, R. W. 2000. Iron hydrolysis and solubility revisited: observations and comments on iron hydrolysis characterizations. Mar. Chem., 70: 23–35. http://dx.doi.org/10.1016%2FS0304-4203%2800%2900012-8

Campbell, P. G. C. 1995. “Interactions between trace metals and aquatic organisms: a critique of the free-ion activity model”. In Metal Speciation and Bioavailability in Aquatic Systems, Edited by: Tessier, A. and Turner, D. R. pp. 45–102. New York: John Wiley & Sons Ltd..

Campbell, P. G. C., Twiss, M. R. and Wilkinson, K. J. 1997. Accumulation of natural organic matter on the surface of living cells–implication for the interaction of aquatic biota with toxic solutes. Can. J. Fish. Aquat. Sci., 54: 2543–2554. http://dx.doi.org/10.1139%2Fcjfas-54-11-2543

Carpenter, S. R. 1996. Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology, 77: 677–680.

Carrick, H. J. and Schelske, C. L. 1997. Have we overlooked the importance of small phytoplankton in productive waters?. Limnol. Oceanogr., 42: 1613–1621.

Chalfie, M. 1995. Green fluorescent protein. Photochem. Photobiol., 62: 651–656. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=7480149http://www4.infotrieve.com/newmedline/detail.asp?NameID=7480149&Session=&searchQuery=Photochem%2E+Photobiol%2E%5BJournal+Name%5D+AND+62%5BVolume%5D+AND+651%5BPage+Number%5D+AND+1995%5BPublication+Date%5D+AND+Chalfie%5BAuthor+Name%5D&count=1

Chatterjee, J. and Meighen, E. A. 1995. Biotechnological applications of bacterial bioluminescence (lux) genes. Photochem. Photobiol., 62: 641–650.

Coale, K. H., Johnson, K. S., Fitzwater, S. E., Gordon, R. M., Tanner, S., Chavez, F. P., Ferioli, L., Sakamoto, C., Rogers, P., Millero, F., Steinberg, P., Nightingale, P., Cooper, D., Cochlan, W. P., Landry, M. R., Constantinou, J., Rollwagen, G., Trasvina, A. and Kudela, R. 1996. A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean. Nature (Lond.), 383: 495–501. http://dx.doi.org/10.1038%2F383495a0

Coale, K. H., Wang, X., Tanner, S. J. and Johnson, K. S. 2003. Phytoplankton growth and biological response to iron and zinc addition in the Ross Sea and Antarctic Circumpolar Current along 170°. W. Deep-Sea Res. II, 50: 635–653.

Croot, P. L., Bowie, A. R., Frew, R. D., Maldonado, M., Hall, J. A., Safi, K. A., La Roche, J., Boyd, P. W. and Low, C. S. 2001. Retention of dissolved iron and Fe-II in an iron induced Southern Ocean phytoplankton bloom. Geophys. Res. Lett., 28: 3425–3428. http://dx.doi.org/10.1029%2F2001GL013023

Cubitt, A. B., Heim, R., Adams, S. R., Boyd, A. E., Gross, L. A. and Tsien, R. Y. 1995. Understanding, improving and using green fluorescent proteins. Trends Biochem. Sci., 20: 448–455. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=8578587http://www4.infotrieve.com/newmedline/detail.asp?NameID=8578587&Session=&searchQuery=Trends+Biochem%2E+Sci%2E%5BJournal+Name%5D+AND+20%5BVolume%5D+AND+448%5BPage+Number%5D+AND+1995%5BPublication+Date%5D+AND+Cubitt%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1016%2FS0968-0004%2800%2989099-4

Cullen, J. J. 1991. Hypotheses to explain high-nutrient conditions in the open sea. Limnol. Oceanogr., 36: 1578–1599.

Cullen, J. J., Yang, X. and MacIntyre, H. L. 1992. “Nutrient limitation of marine photosynthesis”. In Primary Productivity and Biogeochemical Cycles in the Sea, Edited by: Falkowski, P. G. and Woodhead, A. D. pp. 69–88. New York: Plenum Press.

Cullen, J. J. and Davis, R. F. 2003. The blank can make a big difference in oceanographic measurements. Limnol. Oceanogr. Bull., 12: 29–35.

Daunert, S., Barrett, G., Feliciano, J. S., Shetty, R. S., Shrestha, S. and Smith-Spencer, W. 2000. Genetically-engineered whole-cell sensing systems: coupling biological recognition with reporter genes. Chem. Rev., 100: 2705–2738. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=11749302http://www4.infotrieve.com/newmedline/detail.asp?NameID=11749302&Session=&searchQuery=Chem%2E+Rev%2E%5BJournal+Name%5D+AND+100%5BVolume%5D+AND+2705%5BPage+Number%5D+AND+2000%5BPublication+Date%5D+AND+Daunert%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1021%2Fcr990115p

Davey, M. and Geider, R. J. 2001. Impact of iron limitation on the photosynthetic apparatus of the diatom Chaetoceros muelleri (Bacillariophyceae). J. Phycol., 37: 987–1000. http://dx.doi.org/10.1046%2Fj.1529-8817.2001.99169.x

Davison, W. and Zhang, H. 1994. In situ speciation measurements of trace components in natural waters using thin-film gels. Nature (Lond.), 367: 546–548. http://dx.doi.org/10.1038%2F367546a0

Dolan, D. M., McGunagle, K. P., Perry, S. and Voldner, E. 1993. Source investigation for Lake Superior, Windsor, Ontario: International Joint Commission.

Donat, J. R. and Bruland, K. W. 1990. A comparison of two voltammetric techniques for determining zinc speciation in northeast Pacific Ocean waters. Mar. Chem., 28: 301–323. http://dx.doi.org/10.1016%2F0304-4203%2890%2990050-M

Doucette, G. J., Erdner, D. L., Peleato, M. L., Hartman, J. J. and Anderson, D. M. 1996. Quantitative analysis of iron-stress related proteins in Thalassiosira weissflogii: measurement of flavodoxin and ferredoxin using HPLC. Mar. Ecol. Prog. Ser., 130: 269–276.

Downing, J. A., Osenberg, C. W. and Sarnelle, O. 1999. Meta-analysis of marine nutrient-enrichment experiments: variation in the magnitude of nutrient limitation. Ecology, 80: 1157–1167.

Durham, K. A., Porta, D., Twiss, M. R., McKay, R. M. L. and Bullerjahn, G. S. 2002. Construction and initial characterization of a luminescent Synechococcus sp. PCC 7942 Fe-dependent bioreporter. FEMS Microbiol. Lett., 209: 215–221.

Durham, K. A., Porta, D., McKay, R. M. L. and Bullerjahn, G. S. 2003. Expression of the iron-responsive irpA gene from the cyanobacterium Synechococcus sp. strain PCC 7942. Arch. Microbiol., 179: 131–134.

Entsch, B., Sim, R. G. and Hatcher, B. G. 1983. Indications from photosynthetic components that iron is a limiting nutrient in primary producers on coral reefs. Mar. Biol., 73: 17–30. http://dx.doi.org/10.1007%2FBF00396281

Erdner, D. L. and Anderson, D. M. 1999. Ferredoxin and flavodoxin as biochemical indicators of iron limitation during open-ocean iron enrichment. Limnol. Oceanogr., 44: 1609–1615.

Erdner, D. L., Price, N. M., Doucette, G. J., Peleato, M. L. and Anderson, D. M. 1999. Characterization of ferredoxin and flavodoxin as molecular markers of iron limitation in marine phytoplankton. Mar. Ecol. Prog. Ser., 184: 43–53.

Evans, J. C. and Prepas, E. E. 1997. Relative importance of iron and molybdenum in restricting phytoplankton biomass in high phosphorus saline lakes. Limnol. Oceanogr., 42: 461–472.

Fahnenstiel, G. L. and Carrick, H. J. 1992. Phototrophic picoplankton in Lakes Huron and Michigan: abundance, distribution, composition, and contribution to biomass and production. Can. J. Fish. Aquat. Sci., 49: 379–388.

Falciatore, A., Casotti, R., Leblanc, C., Abrescia, C. and Bowler, C. 1999. Transformation of a non-selectable reporter gene in marine diatoms. Mar. Biotechnol., 1: 239–251. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=10383998http://www4.infotrieve.com/newmedline/detail.asp?NameID=10383998&Session=&searchQuery=Mar%2E+Biotechnol%2E%5BJournal+Name%5D+AND+1%5BVolume%5D+AND+239%5BPage+Number%5D+AND+1999%5BPublication+Date%5D+AND+Falciatore%5BAuthor+Name%5D&count=1

Falciatore, A., Ribera d'Alcala, M., Croot, P. and Bowler, C. 2000. Perception of environmental signals by a marine diatom. Science, 288: 2363–2366. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=10875921http://www4.infotrieve.com/newmedline/detail.asp?NameID=10875921&Session=&searchQuery=Science%5BJournal+Name%5D+AND+288%5BVolume%5D+AND+2363%5BPage+Number%5D+AND+2000%5BPublication+Date%5D+AND+Falciatore%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1126%2Fscience.288.5475.2363

Falkowski, P. G. and Kolber, Z. 1995. Variations in chlorophyll fluorescence yields in phytoplankton in the world oceans. Aust. J. Plant Physiol., 22: 341–355.

Falkowski, P. G., Wyman, K., Ley, A. C. and Mauzerall, D. C. 1986. Relationship of steady-state photosynthesis to fluorescence in eucaryotic algae. Biochim. Biophys. Acta, 849: 183–192.

Falkowski, P. G., Ziemann, D., Kolber, Z. and Bienfang, P. K. 1991. Nutrient pumping and phytoplankton response in a sub-tropical mesoscale eddy. Nature (Lond.), 352: 55–58. http://dx.doi.org/10.1038%2F352055a0

Falkowski, P. G., Greene, R. M. and Geider, R. J. 1992. Physiological limitations on phytoplankton productivity in the ocean. Oceanography, 5: 84–91.

Field, M. P. and Sherrell, R. M. 2003. Direct determination of ultra-trace levels of metals in fresh water using desolvating micronebulization and HR-ICP-MS: application to Lake Superior waters. J. Anal. At. Spectrom., 18: 254–259. http://dx.doi.org/10.1039%2Fb210628k

Flegal, A. R., Nriagu, J. O., Niemeyer, S. and Coale, K. H. 1989. Isotopic tracers of lead contamination in the Great Lakes. Nature (Lond.), 339: 455–458. http://dx.doi.org/10.1038%2F339455a0

Francko, D. A. 1990. “Alteration of bioavailability and toxicity by phototransformation of organic acids”. In Organic Acids in Aquatic Systems, Edited by: Purdue, E. M. and Gjessing, E. T. pp. 167–177. New York: John Wiley & Sons.

Francko, D. A. and Heath, R. T. 1982. UV-sensitive complex phosphorus: association with dissolved humic material and iron in a bog lake. Limnol. Oceanogr., 27: 564–569.

Geider, R. J. and La Roche, J. 1994. The role of iron in phytoplankton photosynthesis, and the potential for iron-limitation of primary productivity in the sea. Photosynth. Res., 39: 275–301. http://dx.doi.org/10.1007%2FBF00014588

Geider, R. J., La Roche, J., Greene, R. M. and Olaizola, M. 1993. Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation. J. Phycol., 29: 755–766. http://dx.doi.org/10.1111%2Fj.0022-3646.1993.00755.x

Ghassemian, M. and Straus, N. A. 1996. Fur regulates the expression of iron-stress genes in the cyanobacterium Synechococcus sp. strain PCC 7942. Microbiology (UK), 142: 1469–1476.

Giess, U., Vinnemeier, J., Kunert, A., Lindner, I., Gemmer, B., Lorenz, M., Hagemann, M. and Schoor, A. 2001. Detection of the isiA gene across cyanobacterial strains: potential for probing iron deficiency. Appl. Environ. Microbiol., 67: 5247–5253. http://dx.doi.org/10.1128%2FAEM.67.11.5247-5253.2001

Gillor, O., Hadas, O., Post, A. F. and Belkin, S. 2002. Phosphorus bioavailability monitoring by a bioluminescent cyanobacterial sensor strain. J. Phycol., 38: 107–115. http://dx.doi.org/10.1046%2Fj.1529-8817.2002.01069.x

Gillor, O., Harush, A., Hadas, O., Post, A. F. and Belkin, S. 2003. A Synechococcus PglnA::luxAB fusion for estimation of nitrogen bioavailability to freshwater cyanobacteria. Appl. Environ. Microbiol., 69: 1465–1474. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=12620830http://www4.infotrieve.com/newmedline/detail.asp?NameID=12620830&Session=&searchQuery=Appl%2E+Environ%2E+Microbiol%2E%5BJournal+Name%5D+AND+69%5BVolume%5D+AND+1465%5BPage+Number%5D+AND+2003%5BPublication+Date%5D+AND+Gillor%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1128%2FAEM.69.3.1465-1474.2003

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. http://dx.doi.org/10.1016%2F0304-4203%2894%2990012-4

Gledhill, M., van den Berg, C. M. G., Nolting, R. F. and Timmermans, K. R. 1998. Variability in the speciation of iron in the northern North Sea. Mar. Chem., 59: 283–300. http://dx.doi.org/10.1016%2FS0304-4203%2897%2900097-2

Guildford, S. J., Healey, F. P. and Hecky, R. E. 1987. Depression of primary productivity by humic matter and suspended sediment in limnocorral experiments at Southern Indian Lake. Can. J. Fish. Aquat. Sci., 44: 1408–1417.

Harvey, G. R. and Boran, D. A. 1985. “Geochemistry of humic substances in seawater”. In Humic Substances in Soil, Sediment, and Water. Geochemistry, Isolation, and Characterization, Edited by: Aiken, G. R., McKnight, D. M., Wershaw, R. L. and MacCarthy, P. pp. 233–247. New York: John Wiley & Sons.

Hudson, R. J. M. and Morel, F. M. M. 1993. Trace metal transport by marine microorganisms: implications of metal coordination kinetics. Deep-Sea Res., 40: 129–151.

Hutchins, D. A. 1995. Iron and the marine phytoplankton community. Prog. Phycol. Res., 11: 1–49.

Hutchins, D. A. and Bruland, K. W. 1994. Grazer-mediated regeneration and assimilation of Fe, Zn, and Mn from planktonic prey. Mar. Ecol. Prog. Ser., 110: 259–269.

Hutchins, D. A. and Bruland, K. W. 1998. Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime. Nature (Lond.), 393: 561–564. http://dx.doi.org/10.1038%2F31203

Hutchins, D. A., DiTullio, G. R., Zhang, Y. and Bruland, K. W. 1998. An iron limitation mosaic in the California upwelling regime. Limnol. Oceanogr., 43: 1037–1054.

Hutchins, D. A., Witter, A. E., Butler, A. and Luther, G. W. III. 1999. Competition among marine phytoplankton for different chelated iron species. Nature (Lond.), 400: 858–861. http://dx.doi.org/10.1038%2F23680

Hutchins, D. A., Hare, C. E., Weaver, R. S., Zhang, Y., Firme, G. F., DiTullio, G. R., Alm, M. B., Riseman, S. F., Maucher, J. M., Geesey, M. E., Trick, C. G., Smith, G. J., Rue, E. L., Conn, J. and Bruland, K. W. 2002. Phytoplankton iron limitation in the Humboldt Current and Peru Upwelling. Limnol. Oceanogr., 47: 997–1011.

Imai, A., Fukushima, T. and Matsushige, K. 1999. Effects of iron limitation and aquatic humic substances on the growth of Microcystis aeruginosa. Can. J. Fish. Aquat. Sci., 56: 1929–1937. http://dx.doi.org/10.1139%2Fcjfas-56-10-1929

Inda, L. A. and Peleato, M. L. 2002. Immunoquantification of flavodoxin and ferredoxin from Scenedesmus vacuolatus as iron stress molecular markers. Eur. J. Phycol., 37: 486–493. http://dx.doi.org/10.1017%2FS0967026202003864

Jackson, T. A. and Hecky, R. E. 1980. Depression of primary productivity by humic matter in lake and reservoir waters of the boreal forest zone. Can. J. Fish. Aquat. Sci., 37: 2300–2317.

Jones, G. J., Palenik, B. P. and Morel, F. M. M. 1987. Trace metal reduction by phytoplankton: the role of plasmalemma redox enzymes. J. Phycol., 23: 237–244.

Kawaguchi, T., Lewitus, A. J., Aelion, C. M. and McKellar, H. N. 1997. Can urbanization limit iron availability to estuarine algae?. J. Exp. Mar. Biol. Ecol., 213: 53–69. http://dx.doi.org/10.1016%2FS0022-0981%2897%2900009-9

Kemp, A. L. W. and Johnston, L. M. 1979. Diagenesis of organic matter in the sediments of Lakes Ontario, Erie and Huron. J. Great Lakes Res., 5: 1–10.

Khang, Y.-H., Yang, Z. K. and Burlage, R. S. 1997. Measurement of iron-dependence of pupA promoter activity by a pup-lux bioreporter. J. Microbiol. Biotechnol., 7: 352–355.

Kohler, S., Belkin, S. and Schmid, R. D. 2000. Reporter gene bioassays in environmental analysis. Fresenius J. Anal. Chem., 366: 769–779. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=11225788http://www4.infotrieve.com/newmedline/detail.asp?NameID=11225788&Session=&searchQuery=Fresenius+J%2E+Anal%2E+Chem%2E%5BJournal+Name%5D+AND+366%5BVolume%5D+AND+769%5BPage+Number%5D+AND+2000%5BPublication+Date%5D+AND+Kohler%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1007%2Fs002160051571

Kolber, Z. and Falkowski, P. G. 1993. Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol. Oceanogr., 38: 1646–1665.

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.

Kuma, K., Katsumoto, A., Kawakami, H., Takatori, F. and Matsunaga, K. 1998. Spatial variability of Fe(III) hydroxide solubility in the water column of the northern North Pacific Ocean. Deep-Sea Res., 45: 91–113. http://dx.doi.org/10.1016%2FS0967-0637%2897%2900067-8

Kunert, A., Hagemann, M. and Erdmann, N. 2000. Construction of promoter probe vectors for Synechocystis PCC 6803 using the light-emitting reporter systems Gfp and LuxAB. J. Microbiol. Meth., 41: 185–194. http://dx.doi.org/10.1016%2FS0167-7012%2800%2900162-7

La Roche, J., Geider, R. J., Graziano, L. M., Murray, H. and Lewis, K. 1993. Induction of specific proteins in eukaryotic algae grown under iron-, phosphorus-, or nitrogen-deficient conditions. J. Phycol., 29: 767–777. http://dx.doi.org/10.1111%2Fj.0022-3646.1993.00755.x

La Roche, J., Murray, H., Orellana, M. and Newton, J. 1995. Flavodoxin expression as an indicator of iron limitation in marine diatoms. J. Phycol., 31: 520–530.

La Roche, J., Boyd, P. W., McKay, R. M. L. and Geider, R. J. 1996. Flavodoxin as an in situ marker for iron stress in phytoplankton. Nature (Lond.), 382: 802–805. http://dx.doi.org/10.1038%2F382802a0

Lewis, B. L., Holt, P. D., Taylor, S. W., Wilhelm, S. W., Trick, C. G., Butler, A. and Luther, G. W. III. 1995. Voltametric estimation of iron (III) thermodynamic stability constants for catecholate siderophores isolated from marine bacteria and cyanobacteria. Mar. Chem., 50: 179–188. http://dx.doi.org/10.1016%2F0304-4203%2895%2900034-O

Lin, C. K. and Schelske, C. L. 1981. Seasonal variation of potential nutrient limitation to chlorophyll production in southern Lake Huron. Can. J. Fish. Aquat. Sci., 38: 1–9.

Loper, J. E. and Lindow, S. E. 1994. A biological sensor for iron available to bacteria in their habitats on plant surfaces. Appl. Environ. Microbiol., 60: 1934–1941.

Loper, J. E. and Lindow, S. E. 1996. “Reporter gene systems useful in evaluating in situ gene expression by soil- and plant-associated bacteria”. In Manual of Environmental Microbiology, Edited by: Hurst, C. J., Knudsen, G. R., McInerney, M. J., Stetzenbach, L. D. and Walter, M. V. pp. 482–492. Washington, DC: ASM Press.

Loper, J. E. and Lindow, S. E. 1997. Availability of iron to Pseudomonas fluorescens in rhizosphere and bulk soil evaluated with an ice nucleation reporter gene. Appl. Environ. Microbiol., 63: 99–105. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=8979343http://www4.infotrieve.com/newmedline/detail.asp?NameID=8979343&Session=&searchQuery=Appl%2E+Environ%2E+Microbiol%2E%5BJournal+Name%5D+AND+63%5BVolume%5D+AND+99%5BPage+Number%5D+AND+1997%5BPublication+Date%5D+AND+Loper%5BAuthor+Name%5D&count=1

Maldonado, M. T. and Price, N. M. 2000. Nitrate regulation of Fe reduction and transport by Fe-limited Thalassiosira oceanica.. Limnol. Oceanogr., 45: 814–826.

Maldonado, M. T., Boyd, P. W., La Roche, J., Strzepek, R., Waite, A., Bowie, A. R., Croot, P. L., Frew, R. D. and Price, N. M. 2001. Iron uptake and physiological response of phytoplankton during a mesoscale Southern Ocean iron enrichment. Limnol. Oceanogr., 46: 1802–1808.

Martin, J. H., Coale, K. H., Johnson, K. S., Fitzwater, S. E., Gordon, R. M., Tanner, S. J., Hunter, C. N., Elrod, V. A., Nowicki, J. L., Coley, T. L., Barber, R. T., Lindley, S., Watson, A. J., Vanscoy, K., Law, C. S., Liddicoat, M. I., Ling, R., Stanton, T., Stockel, J., Collins, C., Anderson, A., Bidigare, R., Ondrusek, M., Latasa, M., Millero, F. J., Lee, K., Yao, W., Zhang, J. Z., Friederich, G., Sakomoto, C., Chavez, F., Buck, K., Kolber, Z., Greene, R., Falkowski, P., Chisholm, S. W., Hoge, F., Swift, R., Yungel, J., Turner, S., Nightingale, P., Hatton, A., Liss, P. and Tindale, N. W. 1994. Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature (Lond.), 371: 123–129. http://dx.doi.org/10.1038%2F371123a0

Matta, J. L., Govind, N. S. and Trench, R. K. 1992. Polyclonal antibodies against iron-superoxide dismutase from Escherichia coli B cross-react with superoxide dismutases from Symbiodinium microadriaticum (Dinophyceae). J. Phycol., 28: 343–346. http://dx.doi.org/10.1111%2Fj.0022-3646.1992.00343.x

McKay, R. M. L., Geider, R. J. and La Roche, J. 1997. Physiological and biochemical response of the photosynthetic apparatus of two marine diatoms to Fe stress. Plant Physiol., 114: 615–622. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=12223732http://www4.infotrieve.com/newmedline/detail.asp?NameID=12223732&Session=&searchQuery=Plant+Physiol%2E%5BJournal+Name%5D+AND+114%5BVolume%5D+AND+615%5BPage+Number%5D+AND+1997%5BPublication+Date%5D+AND+McKay%5BAuthor+Name%5D&count=1

McKay, R. M. L., La Roche, J., Yakunin, A. F., Durnford, D. G. and Geider, R. J. 1999. Accumulation of ferredoxin and flavodoxin in a marine diatom in response to Fe. J. Phycol., 35: 510–519. http://dx.doi.org/10.1046%2Fj.1529-8817.1999.3530510.x

McKay, R. M. L., Villareal, T. A. and La Roche, J. 2000. Vertical migration by Rhizosolenia spp. (Bacillariophyceae): implications for Fe acquisition. J. Phycol., 36: 669–674.

McKnight, D. M., Kimball, B. A. and Bencala, K. E. 1988. Iron photoreduction and oxidation in an acidic mountain stream. Science, 240: 637–640.

Michel, K.-P., Pistorius, E. K. and Golden, S. S. 2001. Unusual regulatory elements for iron deficiency induction of the idiA gene of Synechococcus elongatus PCC 7942. J. Bacteriol., 183: 5015–5024. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=11489854http://www4.infotrieve.com/newmedline/detail.asp?NameID=11489854&Session=&searchQuery=J%2E+Bacteriol%2E%5BJournal+Name%5D+AND+183%5BVolume%5D+AND+5015%5BPage+Number%5D+AND+2001%5BPublication+Date%5D+AND+Michel%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1128%2FJB.183.17.5015-5024.2001

Millero, F. J. 1998. Solubility of Fe(III) in seawater. Earth Planet. Sci. Lett., 154: 323–329. http://dx.doi.org/10.1016%2FS0012-821X%2897%2900179-9

Millero, F. J., Sotolongo, S. and Izaguirre, M. 1987. The oxidation kinetics of Fe(II) in seawater. Geochim. Cosmochim. Acta, 51: 793–801. http://dx.doi.org/10.1016%2F0016-7037%2887%2990093-7

Millero, F. J., Yao, W. and Aicher, J. A. 1995. The speciation of Fe(II) and Fe (III) in natural waters. Mar. Chem., 50: 21–39. http://dx.doi.org/10.1016%2F0304-4203%2895%2900024-L

Mioni, C. E., Howard, A. M., DeBruyn, J. M., Bright, N. G., Twiss, M. R., Applegate, B. M. and Wilhelm, S. W. 2003. Characterization and field trials of a bioluminescent bacterial reporter of iron bioavailability. Mar. Chem., 83: 31–46. http://dx.doi.org/10.1016%2FS0304-4203%2803%2900094-X

Moffett, J. W. 1995. Temporal and spatial variability of copper complexation by strong chelators in the Sargasso Sea. Deep Sea Res., 42: 1273–1295. http://dx.doi.org/10.1016%2F0967-0637%2895%2900060-J

Moseley, J. L., Allinger, T., Herzog, S., Hoerth, P., Wehinger, E., Merchant, S. and Hippler, M. 2002. Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. Europ. Molecul. Biol. Org. J., 21: 6709–6720.

Neilson, M., L'Italien, S., Glumac, V., Williams, D. and Bertram, P. 1995. “Nutrients: trends and system response”. In SOLEC Working Paper Chicago, IL EPA 905-R-95-015

Nichols, D. B., Satchwell, M. F., Alexander, J. E., Martin, N. M., Baesl, M. T. and Boyer, G. L. 2001. “Iron nutrition in the brown tide alga, Aureococcus anophagefferens: characterization of a ferric chelate reductase activity”. In Harmful Algal Blooms 2000, Edited by: Hallegraeff, G. M., Blackburn, S. I., Bolch, C. J. and Lewis, R. J. pp. 340–343. Rome: Intergovernmental Oceanographic Commission of UNESCO.

Nriagu, J. O., Lawson, G., Wong, H. K. T. and Azcue, J. M. 1993. A protocol for minimizing contamination in the analysis of trace metals in Great Lakes waters. J. Great Lakes Res., 19: 175–182.

Nriagu, J. O., Lawson, G., Wong, H. K. T. and Cheam, V. 1996. Dissolved trace metals in Lakes Superior, Erie and Ontario. Environ. Sci. Technol., 30: 178–187. http://dx.doi.org/10.1021%2Fes950221i

Paul, J. H., Pichard, S. L., Kang, J. B., Watson, G. M. F. and Tabita, F. R. 1999. Evidence for a clade-specific temporal and spatial separation in ribulose bisphosphate carboxylase gene expression in phytoplankton populations off Cape Hatteras and Bermuda. Limnol. Oceanogr., 44: 12–23.

Porta, D., Bullerjahn, G. S., Durham, K. A., Wilhelm, S. W., Twiss, M. R. and McKay, R. M. L. 2003. Physiological characterization of a Synechococcus sp. (Cyanophyceae) strain PCC 7942 iron-dependent bioreporter for freshwater environments. J. Phycol., 39: 64–73.

Prakash, A., Rashid, M. A., Jensen, A. and Subba, RaoD. V. 1973. Influence of humic substances on the growth of marine phytoplankton: diatoms. Limnol. Oceanogr., 18: 516–524.

Putt, M., Harris, G. P. and Cuhel, R. L. 1987. Photoinhibition of DCMU-enhanced fluorescence in Lake Ontario phytoplankton. Can. J. Fish. Aquat. Sci., 44: 2144–2154.

Qian, J., Xue, H., Sigg, L. and Albrecht, A. 1998. Complexation of cobalt by natural ligands in freshwater. Environ. Sci. Technol., 32: 2043–2050. http://dx.doi.org/10.1021%2Fes971018l

Raven, J. A. 1990. Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and of C assimilation pathway. New Phytol., 116: 1–18.

Riethman, H. C., Bullerjahn, G., Reddy, K. J. and Sherman, L. A. 1988. Regulation of cyanobacterial pigment-protein composition and organization by environmental factors. Photosynth. Res., 18: 133–162. http://dx.doi.org/10.1007%2FBF00042982

Roessler, P. G. 2000. More tools for diatom molecular biology research. J. Phycol., 36: 259–260.

Rossmann, R. and Barres, J. 1988. Trace element concentrations in near-surface waters of the Great Lakes and methods of collection, storage, and analysis. J. Great Lakes Res., 14: 188–204.

Rue, E. L. and Bruland, K. W. 1995. Complexation of Fe(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. http://dx.doi.org/10.1016%2F0304-4203%2895%2900031-L

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.

Saito, M. and Moffett, J. W. 2001. Complexation of cobalt by natural organic ligands in the Sargasso Sea as determined by a new high-sensitivity electrochemical cobalt speciation method suitable for open ocean work. Mar. Chem., 75: 49–68. http://dx.doi.org/10.1016%2FS0304-4203%2801%2900025-1

Schelske, C. L. 1962. Iron, organic matter, and other factors limiting primary productivity in a marl lake. Science, 136: 45–46.

Schelske, C. L. 1984. “In situ and natural phytoplankton assemblage bioassays”. In Algae as Ecological Indicators, Edited by: Schubert, L. E. pp. 15–47. London: Academic Press, Inc..

Schelske, C. L., Hooper, F. P. and Haertl, E. J. 1962. Responses of a marl lake to chelated iron and fertilizer. Ecology, 43: 646–653.

Schelske, C. L., Feldt, L. E., Santiago, M. A. and Stoermer, E. F. Nutrient enrichment and its effect on phytoplankton production and species composition. Lake Superior 15th Conference on Great Lakes Research. April 5–7 1972, Madison, WI. Proceedings, pp.149–165.

Schelske, C. L., Rothman, E. D. and Simmons, M. S. 1978. Comparison of bioassay procedures for growth-limiting nutrients in the Laurentian Great Lakes. Mitt. Internat. Verein. Limnol., 21: 65–80.

Schelske, C. L. and Sicko-Goad, L. 1990. Effect of chelated trace metals on phosphorus uptake and storage in natural assemblages of Lake Michigan phytoplankton. J. Great Lakes Res., 16: 82–89.

Schmidt, W. 1999. Mechanisms and regulation of reduction-based iron uptake in plants. New Phytol., 141: 1–26. http://dx.doi.org/10.1046%2Fj.1469-8137.1999.00331.x

Schreiber, U. 1998. Chlorophyll fluorescence: new instruments for special applications, Photosynthesis: Mechanisms and Effects, Vol. V 4253–4258. Dordrecht, , The Netherlands: Kluwer Academic Publishers.

Sedwick, P. N., DiTullio, G. R. and Mackey, D. J. 2000. Iron and manganese in the Ross Sea, Antarctica: seasonal iron limitation in Antarctic shelf waters. J. Geophys. Res., 105: 11321–11336. http://dx.doi.org/10.1029%2F2000JC000256

Sen, A., Dwivedi, K., Rice, K. A. and Bullerjahn, G. S. 2000. Growth phase and metal-dependent regulation of the dpsA gene in Synechococcus sp. strain PCC 7942. Arch. Microbiol., 173: 352–357. http://dx.doi.org/10.1007%2Fs002030000153

Shaked, Y., Erel, Y. and Sukenik, A. 2002. Phytoplankton-mediated redox cycle of iron in the epilimnion of Lake Kinneret. Environ. Sci. Technol., 36: 460–467. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=11871562http://www4.infotrieve.com/newmedline/detail.asp?NameID=11871562&Session=&searchQuery=Environ%2E+Sci%2E+Technol%2E%5BJournal+Name%5D+AND+36%5BVolume%5D+AND+460%5BPage+Number%5D+AND+2002%5BPublication+Date%5D+AND+Shaked%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1021%2Fes010896n

Snel, J. F. H. and Dassen, H. H. A. 2000. Measurement of light and pH dependence of single-cell photosynthesis by fluorescence microscopy. J. Fluorescence., 10: 269–273. http://dx.doi.org/10.1023%2FA%3A1009401211264

Steinberg, C. and Muenster, U. 1985. “Geochemistry and ecological role of humic substances in lakewater”. In Humic Substances in Soil, Sediment, and Water. Geochemistry, Isolation, and Characterization, Edited by: Aiken, G. R., McKnight, D. M., Wershaw, R. L. and MacCarthy, P. pp. 105–145. New York: John Wiley & Sons.

Sterner, R. W., Smutka, T. M., McKay, R. M. L., Qin, X., Brown, E. T. and Sherrell, R. M. 2004. Phosphorus and trace metal limitation of algae and bacteria in Lake Superior. Limnol. Oceanogr., 49: 495–507.

Stevens, D. R. and Purton, S. 1997. Genetic engineering of eukaryotic algae: progress and prospects. J. Phycol., 33: 713–722. http://dx.doi.org/10.1111%2Fj.0022-3646.1997.00713.x

Stockner, J. G. and Antia, N. J. 1986. Algal picoplankton from marine and freshwater ecosystems: a multidisciplinary perspective. Can. J. Fish. Aquat. Sci., 43: 2472–2503.

Stoermer, E. F., Ladewski, B. G. and Schelske, C. L. 1978. Population responses of Lake Michigan phytoplankton to nitrogen and phosphorus. Hydrobiologia, 57: 249–265.

Straus, N. A. 1994. “Iron deprivation: physiology and gene regulation”. In The Molecular Biology of Cyanobacteria, Edited by: Bryant, D. A. pp. 731–750. Dordrecht, , The Netherlands: Kluwer Academic Publishers.

Sunda, W. G. 1988/89. Trace metal interactions with marine phytoplankton. Biol. Oceanogr., 6: 411–442.

Sunda, W. G. and Huntsman, S. A. 1995. Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar. Chem., 50: 189–206. http://dx.doi.org/10.1016%2F0304-4203%2895%2900035-P

Suzuki, Y., Kuma, K. and Matsunaga, K. 1995. Bioavailable iron species in seawater measured by macroalga (Laminaria japonica) uptake. Mar. Biol., 123: 173–178. http://dx.doi.org/10.1007%2FBF00350337

Timmermans, K. R., Davey, M. S., van der Wagt, B., Snoek, J., Geider, R. J., Veldhuis, M. J. W., Gerringa, L. J. A. and de Baar, H. J. W. 2001a. Co-limitation by iron and light of Chaetoceros brevis, C. dichaeta and C. calcitrans (Bacillariophyceae). Mar. Ecol. Prog. Ser., 217: 287–297.

Timmermans, K. R., Gerringa, L. J. A., de Baar, H. J. W., van der Wagt, B., Veldhuis, M. J. W., de Jong, J. T. M. and Croot, P. L. 2001b. Growth of large and small Southern Ocean diatoms in relation to availability of iron in natural seawater. Limnol. Oceanogr., 46: 260–266.

Tsuda, A., Takeda, S., Saito, H., Nishioka, J., Nojiri, Y., Kudo, I., Kiyosawa, H., Shiomoto, A., Imai, K., Ono, T., Shimamoto, A., Tsumune, D., Yoshimura, T., Aono, T., Hinuma, A., Kinugasa, M., Suzuki, K., Sohrin, Y., Noiri, Y., Tani, H., Deguchi, Y., Tsurushima, N., Ogawa, H., Fukami, K., Kuma, K. and Saino, T. 2003. A mesoscale iron enrichment in the western subarctic Pacific induces a large centric diatom bloom. Science, 300: 958–961. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=12738858http://www4.infotrieve.com/newmedline/detail.asp?NameID=12738858&Session=&searchQuery=Science%5BJournal+Name%5D+AND+300%5BVolume%5D+AND+958%5BPage+Number%5D+AND+2003%5BPublication+Date%5D+AND+Tsuda%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1126%2Fscience.1082000

Twiss, M. R., Auclair, J.-C. and Charlton, M. N. 2000. An investigation into iron-stimulated phytoplankton productivity in epipelagic Lake Erie during thermal stratification using trace metal techniques. Can. J. Fish. Aquat. Sci., 57: 86–95. http://dx.doi.org/10.1139%2Fcjfas-57-1-86

Twiss, M. R. and Moffett, J. W. 2002. Comparison of copper speciation in coastal marine waters measured using analytical voltammetry and Diffusion Gradient in Thin-Film techniques. Environ. Sci. Technol., 36: 1061–1068. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=11917992http://www4.infotrieve.com/newmedline/detail.asp?NameID=11917992&Session=&searchQuery=Environ%2E+Sci%2E+Technol%2E%5BJournal+Name%5D+AND+36%5BVolume%5D+AND+1061%5BPage+Number%5D+AND+2002%5BPublication+Date%5D+AND+Twiss%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1021%2Fes0016553

Twiss, M. R., Rattan, K. J., Sherrell, R. M. and McKay, R. M. L. Sensitivity of phytoplankton to copper in Lake Superior. J. Great Lakes Res, in press

Van den Berg, C. M. G. 1995. Evidence for organic complexation of iron in seawater. Mar. Chem., 50: 139–157. http://dx.doi.org/10.1016%2F0304-4203%2895%2900032-M

van der Lelie, D., Corbisier, P., Baeyens, W., Wuertz, S., Diels, L. and Mergeay, M. 1994. The use of biosensors for environmental monitoring. Res. Microbial., 145: 67–74. http://dx.doi.org/10.1016%2F0923-2508%2894%2990073-6

Villareal, T. A. and Morton, S. L. 2002. Use of cell-specific PAM-fluorometry to characterize host shading in the epiphytic dinoflagellate Gambierdiscus toxicus. Mar. Ecol., 23: 127–140. http://dx.doi.org/10.1046%2Fj.1439-0485.2002.02777.x

Webb, R., Troyan, T., Sherman, D. and Sherman, L. A. 1994. MapA, an iron-regulated, cytoplasmic membrane protein in the cyanobacterium Synechococcus sp. strain PCC7942. J. Bacteriol., 176: 4906–4913.

Webb, E. A., Moffett, J. W. and Waterbury, J. B. 2001. Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodesmium and Crocosphaera spp.): identification of the IdiA protein. Appl. Environ. Microbiol., 67: 5444–5452. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=11722891http://www4.infotrieve.com/newmedline/detail.asp?NameID=11722891&Session=&searchQuery=Appl%2E+Environ%2E+Microbiol%2E%5BJournal+Name%5D+AND+67%5BVolume%5D+AND+5444%5BPage+Number%5D+AND+2001%5BPublication+Date%5D+AND+Webb%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1128%2FAEM.67.12.5444-5452.2001

Weger, H. G. 1999. Ferric and cupric reductase activities in the green alga Chlamydomonas reinhardtii: experiments using iron-limited chemostats. Planta, 207: 377–384. http://dx.doi.org/10.1007%2Fs004250050495

Weger, H. G., Middlemiss, J. K. and Petterson, C. D. 2002. Ferric chelate reductase activity as affected by the iron-limited growth rate in four species of unicellular green algae (Chlorophyta). J. Phycol., 38: 513–519. http://dx.doi.org/10.1046%2Fj.1529-8817.2002.t01-1-01158.x

Wells, M. L., Mayer, L. M. and Guillard, R. R. L. 1991. Evaluation of iron as a triggering factor for red tide blooms. Mar. Ecol. Prog. Ser., 69: 93–102.

Wells, M. L., Price, N. M. and Bruland, K. W. 1995. Iron chemistry in seawater and its relationship to phytoplankton: a workshop report. Mar. Chem., 48: 157–182. http://dx.doi.org/10.1016%2F0304-4203%2894%2900055-I

Wetzel, R. G. 1966. Productivity and nutrient relationships in marl lakes of northern Indiana. Verh. Internat. Verein. Limnol., 16: 321–332.

Wetzel, R. G. 1983. Limnology, NY: Saunders College Publishing.

Wilhelm, S. W. and Suttle, C. A. 1999. Viruses and nutrient cycles in the sea. BioScience., 49: 781–788.

Wilhelm, S. W., DeBruyn, J. M., Gillor, O., Twiss, M. R., Livingston, K., Bourbonniere, R. A., Pickell, L. D., Trick, C. G., Dean, A. L. and McKay, R. M. L. 2003. Effect of phosphorus amendments on present day plankton communities in pelagic Lake Erie. Aquat. Microb. Ecol., 32: 275–285.

Witter, A. E., Hutchins, D. A., Butler, A. and Luther, G. W. 2000. Determination of conditional stability constants and kinetic constants for strong model Fe-binding ligands in seawater. Mar. Chem., 69: 1–17. http://dx.doi.org/10.1016%2FS0304-4203%2899%2900087-0

Wu, J. and Luther, G. W. III. 1995. Complexation of Fe(III) by natural organic ligands in the Northwest Atlantic Ocean by a competitive ligand equilibration method and a kinetic approach. Mar. Chem., 50: 159–177. http://dx.doi.org/10.1016%2F0304-4203%2895%2900033-N

Xia, L., Qin, X. and McKay, R. M. L. 2003. Physiological and biochemical response of freshwater cryptomonads (Cryptophyceae) to Fe deficiency. J. Basic Microbiol., 43: 121–130. http://dx.doi.org/10.1002%2Fjobm.200390012

Xue, H., Kistler, D. and Sigg, L. 1995. Competition of copper and zinc for strong ligands in a eutrophic Lake. Limnol. Oceanogr., 40: 1142–1152.

Xue, H. and Sunda, W. G. 1997. Comparison of [Cu2 +] measurements in lake water determined by ligand exchange and cathodic stripping voltammetry and ion-selective electrode. Environ. Sci. Technol., 31: 1902–1909. http://dx.doi.org/10.1021%2Fes960551i

Yakunin, A. F., Hallenbeck, P. C., Troshina, O. Y. and Gogotov, I. N. 1993a. Purification and properties of a bacterial-type ferredoxin from the nitrogen-fixing cyanobacterium Anabaena variabilis ATCC 29413. Biochim. Biophys. Acta, 1163: 124–130. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=8387824http://www4.infotrieve.com/newmedline/detail.asp?NameID=8387824&Session=&searchQuery=Biochim%2E+Biophys%2E+Acta%5BJournal+Name%5D+AND+1163%5BVolume%5D+AND+124%5BPage+Number%5D+AND+1993%5BPublication+Date%5D+AND+Yakunin%5BAuthor+Name%5D&count=1

Yakunin, A. F., Hallenbeck, P. C., Troshina, O. Y. and Gogotov, I. N. 1993b. Purification and properties of a flavodoxin from the heterocystous cyanobacterium Anabaena sphaerica. Biochim. Biophys. Acta, 1164: 305–310. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=8343530http://www4.infotrieve.com/newmedline/detail.asp?NameID=8343530&Session=&searchQuery=Biochim%2E+Biophys%2E+Acta%5BJournal+Name%5D+AND+1164%5BVolume%5D+AND+305%5BPage+Number%5D+AND+1993%5BPublication+Date%5D+AND+Yakunin%5BAuthor+Name%5D&count=1

Yong-Ho, K., Yang, Z. K. and Burlage, R. S. 1997. Measurement of iron-dependence of pupA promoter activity by a pup-lux bioreporter. J. Microbiol. Biotechnol., 7: 352–355.

Zaslavskaia, L. A., Lippmeier, J. C., Shih, C., Ehrhardt, D., Grossman, A. R. and Apt., K. E. 2001. Trophic conversion of an obligate photoautotrophic organism through metabolic engineering. Science, 292: 2073–2075. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=11408656http://www4.infotrieve.com/newmedline/detail.asp?NameID=11408656&Session=&searchQuery=Science%5BJournal+Name%5D+AND+292%5BVolume%5D+AND+2073%5BPage+Number%5D+AND+2001%5BPublication+Date%5D+AND+Zaslavskaia%5BAuthor+Name%5D&count=1http://dx.doi.org/10.1126%2Fscience.160015

Zhang, H., Van den Berg, C. M. G. and Wollast, R. 1990. The determination of interactions of cobalt(II) with organic compounds in seawater using cathodic stripping voltammetry. Mar. Chem., 28: 285–300. http://dx.doi.org/10.1016%2F0304-4203%2890%2990049-I

Published

2004-10-01