Physiological characterization of a Synechococcus sp. (Cyanophyceae) strain PCC 7942 iron-dependent bioreporter for freshwater environments

Journal of Phycology

Volumn 39, Issue 1, 2003, Pages 64-73

  Porta, David ^a   Bullerjahn, George S ^a   Durham, Kathryn A ^a   Wilhelm, Steven W ^b   Twiss, Michael R ^c   McKay, R Michael L ^a,d  

^a BOWLING GREEN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

^c RYERSON UNIVERSITY   (Canada)

^d CLARKSON UNIVERSITY   (United States)

Author keywords

Bioreporter; Cyanobacteria; Flavodoxin; Iron; isiAB; Lake Huron; Luminescent; Synechococcus

Indexed keywords

BIOAVAILABILITY; CYANOBACTERIUM; FRESHWATER ECOSYSTEM; IRON;

NORTH AMERICA;

CYANOBACTERIA; LAURENTIA; SYNECHOCOCCUS; SYNECHOCOCCUS SP.; VIBRIO HARVEYI;

EID: 0037327104     PISSN: 00223646     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1529-8817.2003.02068.x     Document Type: Article

References (60)

1. Allen, M. M. 1968. Simple conditions for growth of unicellular blue-green algae on plates. J. Phycol. 4:1-4.
2. Andersson, C. R., Tsinoremas, N. F., Shelton, J., Lebedeva, N. V., Yarrow, J., Min, H. & Golden, S. S. 2000. Application of bioluminescence to the study of circadian rhythms in cyanobacteria. In Ziegler, M. M. & Baldwin, T. O. [Eds.] Bioluminescence and Chemiluminescence. Academic Press, San Diego, CA, pp. 527-42.
3. Berman-Frank, I., Cullen, J. T., Shaked, Y., Sherrell, R. M. & Falkowski, P. G. 2001. Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnol. Oceanogr. 46:1249-60.
4. Blouin, K., Walker, S. G., Smit, J. & Turner, R. F. B. 1996. Characterization of in vivo reporter systems for gene expression and biosensor applications based on luxAB luciferase genes. Appl. Environ. Microbiol. 62:2013-21.
5. Boyd, P. W., Watson, A. J., Law, C. S., Abraham, E. R., Trull, T., Murdoch, R., Bakker, D. C. E., Bowie, A. R., Buesseler, K. O., Chang, H., Charette, M., Croot, P., Downing, K., Frew, R., Gall, M., Hadfield, M., Hall, J., Harvey, M., Jameson, G., La Roche, J., Liddicoat, M., Ling, R., Maldonado, M. T., McKay, R. M., Nodder, S., Pickmere, S., Pridmore, R., Rintoul, S., Safi, K., Sutton, P., Strzepek, R., Tanneberger, K., Turner, S., Waite, A. & Zeldis, J. 2000. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature (Lond.) 407:695-702.
6. Butler, W. L. & Kitajima, M. 1975. Fluorescence quenching in photosystem II of chloroplasts. Biochim. Biophys. Acta 376:116-25.
7. 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. & 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.
8. DiTullio, G. R., Hutchins, D. A. & Bruland, K. W. 1993. Interaction of iron and major nutrients controls phytoplankton growth and species composition in the tropical North Pacific Ocean. Limnol. Oceanogr. 38:495-508.
9. Doucette, G. J., Erdner, D. L., Peleato, M. L., Hartman, J. J. & 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. 130:269-76.
10. Durham, K. A., Porta, D., Twiss, M. R., McKay, R. M. L. & Bullerjahn, G. S. 2002. Construction and initial characterization of a luminescent Synechococcus sp. PCC 7942 Fe-dependent bioreporter. FEMS Microbiol. Lett. 209:215-21.
11. Erdner, D. L., Price, N. M., Doucette, G. J., Peleato, M. L. & Anderson, D. M. 1999. Characterization of ferredoxin and flavodoxin as markers of iron limitation in marine phytoplankton. Mar. Ecol. Prog. Ser. 184:43-53.
12. Falk, S., Samson, G., Bruce, D., Huner, N. P. A. & Laudenbach, D. E. 1995. Functional analysis of the iron-stress induced CP 43′ polypeptide of PS II in the cyanobacterium Synechococcus sp. PCC 7942. Photosynth. Res. 45:51-60.
13. Geiss, U., Vinnemeier, J., Kunert, A., Lindner, I., Gemmer, B., Lorenz, M., Hagemann, M. & Schoor, A. 2001. Detection of the isiA gene across cyanobacterial strains: potential for probing iron deficiency. Appl. Environ. Microbiol. 67:5247-53.
14. Ghassemian, M. & Straus, N. A. 1996. Fur regulates the expression of iron-stress genes in the cyanobacterium Synechococcus sp. strain PCC 7942. Microbiology 142:1469-76.
15. Gillor, O., Hadas, O., Post, A. F. & Belkin, S. 2002. Phosphorus bioavailability monitoring by a bioluminescent cyanobacterial sensor strain. J. Phycol. 38:107-15.
16. Greene, R. M., Geider, R. J. & Falkowski, P. G. 1991. Effect of iron limitation on photosynthesis in a marine diatom. Limnol. Oceanogr. 36:1772-82.
17. Greene, R. M., Kolber, Z. S., Swift, D. G., Tindale, N. W. & Falkowski, P. G. 1994. Physiological limitation of phytoplankton photosynthesis in the eastern equatorial Pacific determined from variability in the quantum yield of fluorescence. Limnol. Oceanogr. 39:1061-74.
18. Hay, A. G., Rice, J. F., Applegate, B. M., Bright, N. G. & Sayler, G. S. 2000. A bioluminescent whole-cell reporter for detection of 2,4-dichlorophenoxyacetic acid and 2,4-dichlorophenol in soil. Appl. Environ. Microbiol. 66:4589-94.
19. Hudson, R. J. M. & Morel, F. M. M. 1989. Distinguishing between extra- and intracellular iron in marine phytoplankton. Limnol. Oceanogr. 34:1113-20.
20. Hutchins, D. A. 1995. Iron and the marine phytoplankton community. Prog. Phycol. Res. 11:1-49.
21. Hutchins, D. A. & Bruland, K. W. 1998. Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime. Nature (Lond.) 393:561-4.
22. Hutchins, D. A., DiTullio, G. R., Zhang, Y. & Bruland, K. W. 1998. An iron limitation mosaic in the California upwelling regime. Limnol. Oceanogr. 43:1037-54.
23. Hutchins, D. A., Witter, A. E., Butler, A. & Luther, III, G. W. 1999. Competition among marine phytoplankton for diferent chelated iron species. Nature (Lond.) 400:858-61.
24. Kawaguchi, T., Lewitus, A. J., Aelion, C. M. & McKellar, H. N. 1997. Can urbanization limit iron availability to estuarine algae? J. Exp. Mar. Biol. Ecol. 213:53-69.
25. Kerry, A., Laudenbach, D. E. & Trick, C. G. 1988. Influence of iron limitation and nitrogen source on growth and siderophore production by cyanobacteria. J. Phycol. 24:566-71.
26. Kimura, E. & Koike, T. 1998. Recent development of zinc-fluorophores. Chem. Soc. Rev. 27:179-84.
27. Kondo, T. & Ishiura, M. 1994. Circadian rhythms of cyanobacteria: monitoring the biological clocks of individual colonies by bioluminescence. J. Bacteriol. 176:1881-5.
28. Kudo, I. & Harrison, P. J. 1997. Effect of iron nutrition on the marine cyanobacterium Synechococcus grown on different N sources and irradiances. J. Phycol. 33:232-40.
29. La Roche, J., Murray, H., Orellana, M. & Newton, J. 1995. Flavodoxin expression as an indicator of iron limitation in marine diatoms. J. Phycol. 31:520-30.
30. La Roche, J., Boyd, P. W., McKay, R. M. L. & Geider, R. J. 1996. Flavodoxin as an in situ marker for iron stress in phytoplankton. Nature (Lond.) 382:802-5.
31. Liu, Y., Golden, S. S., Kondo, T., Ishiura, M. & Johnson, C. H. 1995. Bacterial luciferase as a reporter of circadian gene expression in cyanobacteria. J. Bacteriol. 177:2080-6.
32. Martin, J. H., Gordon, R. M. & Fitzwater, S. E. 1991. The case for iron. Limnol. Oceanogr. 36:1793-802.
33. McKay, R. M. L., Geider, R. J. & LaRoche, J. 1997. Physiological and biochemical response of the photosynthetic apparatus of two marine diatoms to Fe stress. Plant Physiol. 114:615-22.
34. McKay, R. M. L., La Roche, J., Yakunin, A. F., Durnford, D. G. & Geider, R. J. 1999. Accumulation of ferredoxin and flavodoxin in a marine diatom in response to Fe. J. Phycol. 35:510-9.
35. McKay, R. M. L., Villareal, T. A. & La Roche, J. 2000. Vertical migration by Rhizosolenia spp. (Bacillariophyceae): implications for Fe acquisition. J. Phycol. 36:669-74.
36. McKay, R. M. L., Twiss, M. R. & Nalewajko, C. 2001. Trace metal constraints on carbon, nitrogen and phosphorus acquisition and assimilation by phytoplankton. In Rai, L.C. & Gaur, J. P. [Eds.] Algal Adaptation to Environmental Stresses. Physiological, Biochemical and Molecular Mechanisms. Springer, Berlin, pp. 111-34.
37. Morel, F. M. M., Westall, J. C., Reuter, J. G. & Chaplick, J. P. 1975. Description of the algal growth media "Aquil" and "Fraquil." Technical Note No. 16. In Parsons, R. M. [Ed.] Laboratory for Water Resources and Hydrodynamics. Massachusetts Institute of Technology, Cambridge, MA, 33 pp.
38. Öquist, G. 1971. Changes in pigment composition and photosynthesis induced by iron-deficiency in the Blue-Green Alga Anacystis nidulans. Physiol. Plant. 25:188-91.
39. Price, N. M., Harrison, G. I., Hering, J. G., Hudson, R. J., Nirel, P. M. V., Palenik, B. & Morel, F. M. M. 1989. Preparation and chemistry of the artificial algal culture medium Aquil. Biol. Oceanogr. 6:443-61.
40. Raven, J. A. 1988. The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytol. 109:279-87.
41. 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.
42. Reuter, J. G. & Unsworth, N. L. 1991. Response of marine Synechococcus (Cyanophyceae) cultures to iron nutrition. J. Phycol. 27: 173-8.
43. Rossmann, R. & 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.
44. Rue, E. L. & 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. 42:901-10.
45. Sandmann, G. & Malkin, R. 1983. Iron-sulphur centers and activities of the photosynthetic electron transport chain in iron-deficient cultures of the blue-green alga Aphanocapsa. Plant Physiol. 73:724-8.
46. Sandmann, G., Peleato, M. L., Fillat, M. F., Lazaro, M. C. & Gómez-Moreno, C. 1990. Consequences of the iron-dependent formation of ferredoxin and flavodoxin on photosynthesis and nitrogen fixation on Anabaena strains. Photosyn. Res. 26:119-25.
47. Schelske, C. L. 1962. Iron, organic matter, and other factors limiting primary productivity in a marl lake. Science 136:45-6.
48. Schreiter, P. P. Y., Gillor, O., Post, A., Belkin, S., Schmid, R. D. & Bachmann, T. T. 2001. Monitoring of phosphorus bioavailability in water by an immobilized luminescent cyanobacterial reporter strain. Biosens. Bioelectron. 16:811-8.
49. Sticher, P., Jaspers, M. C. M., Stemmler, K., Harms, H., Zehnder, A. J. B. & van der Meer, J. R. 1997. Development and characterization of a whole-cell bioluminescent sensor for bioavailable middle-chain alkanes in contaminated groundwater samples. Appl. Environ. Microbiol. 63:4053-60.
50. Straus, N. A. 1994. Iron deprivation: physiology and gene regulation. In Bryant, D. A. [Ed.] The Molecular Biology of Cyanobacteria. Kluwer, Dordrecht, The Netherlands, pp. 731-50.
51. Sunda, W. G. 2000. Trace metal-phytoplankton interactions in aquatic systems. In Lovley, D. R. [Ed.] Environmental Microbe-Metal Interactions. ASM, Washington, DC, pp. 79-107.
52. Twiss, M. R., Auclair, J.-C. & Charlton, M. N. 2000. An investigation into iron-stimulated phytoplankton productivity in epipelagic Lake Erie during thermal stratification using trace metal clean techniques. Can. J. Fish. Aquat. Sci. 57:86-95.
53. Twiss, M. R., Errécalde, O., Fortin, C., Campbell, P.G.C., Jumarie, C., Denizeau, F., Berkelaar, E., Hale, B. & van Rees, K. 2001. Coupling the use of computer chemical speciation models and culture techniques in laboratory investigations of trace metal toxicity. Chem. Spec. Bioavailab. 13:1-16.
54. Vinnemeier, J., Kinert, A. & Hagemann, M. 1998. Transcriptional analysis of the isiAB operon in salt-stressed cells of the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol. Lett. 169:323-30.
55. Wells, M., Price, N. & Bruland, K. 1994. Iron limitation and the cyanobacterium Synechococcus in equatorial Pacific waters. Limnol. Oceanogr. 39:1481-6.
56. Welschmeyer, N. A. 1994. Fluorometric analysis of chlorophyll-a in the presence of chlorophyll-b and pheopigments. Limnol. Oceanogr. 39:1985-92.
57. Wetzel, R. G. 1966. Productivity and nutrient relationships in marl lakes of northern Indiana. Verh. Int. Verein. Limnol. 16:321-32.
58. Wilhelm, S. W. & Trick, C. G. 1994. Iron-limited growth of cyanobacteria: multiple siderophore production is a common response. Limnol. Oceanogr. 39:1979-84.
59. Wilhelm, S. W., Maxwell, D. P. & Trick, C. G. 1996. Growth, iron requirements, and siderophore production in iron-limited Synechococcus PCC 7002. Limnol. Oceanogr. 41:89-97.
60. Wu, J. & Luther, III, G. W. 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. 50:159-77.