Trichodesmium, a globally significant marine cyanobacterium

Science

Volumn 276, Issue 5316, 1997, Pages 1221-1229

  Capone, Douglas G ^a   Zehr, Jonathan P ^b   Paerl, Hans W ^c   Bergman, Birgitta ^d   Carpenter, Edward J ^e  

^a UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL SCIENCE   (United States)

^b RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^c University of North Carolina at Chapel Hill   (United States)

^d STOCKHOLM UNIVERSITY   (Sweden)

^e STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; AEROBIC METABOLISM; ARTICLE; CYANOBACTERIUM; ECOSYSTEM; NITROGEN FIXATION; PHOTOSYNTHESIS; PRIORITY JOURNAL;

COLONIES; CYANOBACTERIA; NITROGEN FIXATION; PRIMARY PRODUCTION;

TRICHODESMIUM;

EID: 0030619210     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.276.5316.1221     Document Type: Article

References (158)

1. 2, which characterize filamentous cyanobacteria of the orders Nostocales and Stigonematales [R. W. Castenholz and J. B. Waterbury, in Bergey's Manual of Determinative Bacteriology, J. T. Staley, Ed. (Williams and Wilkins, Baltimore, 1989), pp. 1710-1727].
2. The Red Sea obtained its name from the coloration imparted by T. erythraeum (71) [H. J. Carter, Ann. Mag, Nat. Hist 3, 182 (1863)]. Darwin, while aboard the H.M.S. Beagle [C. Darwin, Journal of Researches into the Natural History and Geology of the Countries Visited During the Voyages of the H.M.S. Beagle Round the World Under the Command of Capt. Fitz Roy, R.N. (Clowes, London, 1845)], as well as Captain J. Cook and his naturalist, J. Banks, aboard the H.M.S. Endeavour, each commented on Trichodesmium's appearance and abundance in tropical seas [J. C. Beaglehole, Ed., The Endeavor Journals of Joseph Banks 1768-1771 (Angus and Robertson, Sydney, Australia, 1962), vol. II: The Journals of Captain James Cook on His Voyages of Discovery, vol. I: The Voyage of the Endeavor 1768-1771 (Cambridge Univ. Press, Cambridge, 1955), pp. 404-405]. Because of its buoyancy and tendency to form colonies, it is easily observed near the sea surface by the naked eye. The colonies, long referred to by mariners as "sea sawdust," aggregate at the surface during periods of low wind stress to form conspicuous surface slicks or blooms.
3. The Red Sea obtained its name from the coloration imparted by T. erythraeum (71) [H. J. Carter, Ann. Mag, Nat. Hist 3, 182 (1863)]. Darwin, while aboard the H.M.S. Beagle [C. Darwin, Journal of Researches into the Natural History and Geology of the Countries Visited During the Voyages of the H.M.S. Beagle Round the World Under the Command of Capt. Fitz Roy, R.N. (Clowes, London, 1845)], as well as Captain J. Cook and his naturalist, J. Banks, aboard the H.M.S. Endeavour, each commented on Trichodesmium's appearance and abundance in tropical seas [J. C. Beaglehole, Ed., The Endeavor Journals of Joseph Banks 1768-1771 (Angus and Robertson, Sydney, Australia, 1962), vol. II: The Journals of Captain James Cook on His Voyages of Discovery, vol. I: The Voyage of the Endeavor 1768-1771 (Cambridge Univ. Press, Cambridge, 1955), pp. 404-405]. Because of its buoyancy and tendency to form colonies, it is easily observed near the sea surface by the naked eye. The colonies, long referred to by mariners as "sea sawdust," aggregate at the surface during periods of low wind stress to form conspicuous surface slicks or blooms.
4. The Red Sea obtained its name from the coloration imparted by T. erythraeum (71) [H. J. Carter, Ann. Mag, Nat. Hist 3, 182 (1863)]. Darwin, while aboard the H.M.S. Beagle [C. Darwin, Journal of Researches into the Natural History and Geology of the Countries Visited During the Voyages of the H.M.S. Beagle Round the World Under the Command of Capt. Fitz Roy, R.N. (Clowes, London, 1845)], as well as Captain J. Cook and his naturalist, J. Banks, aboard the H.M.S. Endeavour, each commented on Trichodesmium's appearance and abundance in tropical seas [J. C. Beaglehole, Ed., The Endeavor Journals of Joseph Banks 1768-1771 (Angus and Robertson, Sydney, Australia, 1962), vol. II: The Journals of Captain James Cook on His Voyages of Discovery, vol. I: The Voyage of the Endeavor 1768-1771 (Cambridge Univ. Press, Cambridge, 1955), pp. 404-405]. Because of its buoyancy and tendency to form colonies, it is easily observed near the sea surface by the naked eye. The colonies, long referred to by mariners as "sea sawdust," aggregate at the surface during periods of low wind stress to form conspicuous surface slicks or blooms.
5. The Red Sea obtained its name from the coloration imparted by T. erythraeum (71) [H. J. Carter, Ann. Mag, Nat. Hist 3, 182 (1863)]. Darwin, while aboard the H.M.S. Beagle [C. Darwin, Journal of Researches into the Natural History and Geology of the Countries Visited During the Voyages of the H.M.S. Beagle Round the World Under the Command of Capt. Fitz Roy, R.N. (Clowes, London, 1845)], as well as Captain J. Cook and his naturalist, J. Banks, aboard the H.M.S. Endeavour, each commented on Trichodesmium's appearance and abundance in tropical seas [J. C. Beaglehole, Ed., The Endeavor Journals of Joseph Banks 1768-1771 (Angus and Robertson, Sydney, Australia, 1962), vol. II: The Journals of Captain James Cook on His Voyages of Discovery, vol. I: The Voyage of the Endeavor 1768-1771 (Cambridge Univ. Press, Cambridge, 1955), pp. 404-405]. Because of its buoyancy and tendency to form colonies, it is easily observed near the sea surface by the naked eye. The colonies, long referred to by mariners as "sea sawdust," aggregate at the surface during periods of low wind stress to form conspicuous surface slicks or blooms.
6. E. J. Carpenter, in Nitrogen in the Marine Environment, E. J. Carpenter and D. G. Capone, Eds. (Academic Press, New York, 1983), pp. 65-103.
7. _, Mar. Biol. Lett. 4, 69 (1983); J. R. Gallon et al., Arch. Hydrobiol. Suppl. 117, 215 (1996).
8. _, Mar. Biol. Lett. 4, 69 (1983); J. R. Gallon et al., Arch. Hydrobiol. Suppl. 117, 215 (1996).
9. See (74) for a summary of historical data on N limitation. Iron (Fe) availability has been shown to limit the growth of phytoplankton in some oceanic regions characterized as high nutrient, low chlorophyll (HNLC) [J. Martin et al., Nature 371, 123 (1994)].
10. 2 fixation also occurred [R. W. F. Hardy and U. D. Havelka, Science 188, 633 (1975)].
11. 2 fixation also occurred [R. W. F. Hardy and U. D. Havelka, Science 188, 633 (1975)].
12. 2 fixation to nonphotosynthetic periods (that is, at night] [P. Fay et al., Nature 220, 810 (1968); P. Fay, Microbiol. Rev. 56, 340 (1992); J. R. Gallon, New Phytol. 122, 571 (1992); B. Bergman, J. R. Gallon, A. N. Rai, L. Stal, FEMS Microbiol. Rev. 19, 139 (1997)].
13. 2 fixation to nonphotosynthetic periods (that is, at night] [P. Fay et al., Nature 220, 810 (1968); P. Fay, Microbiol. Rev. 56, 340 (1992); J. R. Gallon, New Phytol. 122, 571 (1992); B. Bergman, J. R. Gallon, A. N. Rai, L. Stal, FEMS Microbiol. Rev. 19, 139 (1997)].
14. 2 fixation to nonphotosynthetic periods (that is, at night] [P. Fay et al., Nature 220, 810 (1968); P. Fay, Microbiol. Rev. 56, 340 (1992); J. R. Gallon, New Phytol. 122, 571 (1992); B. Bergman, J. R. Gallon, A. N. Rai, L. Stal, FEMS Microbiol. Rev. 19, 139 (1997)].
15. 2 fixation to nonphotosynthetic periods (that is, at night] [P. Fay et al., Nature 220, 810 (1968); P. Fay, Microbiol. Rev. 56, 340 (1992); J. R. Gallon, New Phytol. 122, 571 (1992); B. Bergman, J. R. Gallon, A. N. Rai, L. Stal, FEMS Microbiol. Rev. 19, 139 (1997)].
16. G. E. Fogg, Ecol. Bull. 26, 11 (1978); B. F. Taylor et al., Arch. Microbiol. 88, 205 (1973).
17. G. E. Fogg, Ecol. Bull. 26, 11 (1978); B. F. Taylor et al., Arch. Microbiol. 88, 205 (1973).
18. J. P. Zehr and L. A. McReynolds, Appl. Environ. Microbiol. 55, 2522 (1989); J. P. Zehr et al., ibid. 56, 3527 (1990).
19. J. P. Zehr and L. A. McReynolds, Appl. Environ. Microbiol. 55, 2522 (1989); J. P. Zehr et al., ibid. 56, 3527 (1990).
20. H. W. Paerl, J. C. Priscu, D. L. Brawner, ibid. 55, 2965 (1989).
21. B. Bergman and E. J. Carpenter, J. Phycol. 27, 158 (1991).
22. C. Fredriksson and B. Bergman, Microbiology 141, 2471 (1995).
23. Two cultures are currently available, both apparently strains of T. erythraeum [J. P. Zehr, S. Braun, Y. Chen, M. T. Mellon, J. Exp. Mar. Biol. Ecol. 203, 158 (1996)]: strain NIBB 1067, isolated by K. Ohki and Y. Fujita [Mar. Ecol. Prog. Ser. 7, 185 (1982)], and Trichodesmium IMS 101, isolated by Prufert-Bebout et al. (14). The former has been resistant to transplantation, whereas the latter has been disseminated to several laboratories. Additional isolates may now be available.
24. Two cultures are currently available, both apparently strains of T. erythraeum [J. P. Zehr, S. Braun, Y. Chen, M. T. Mellon, J. Exp. Mar. Biol. Ecol. 203, 158 (1996)]: strain NIBB 1067, isolated by K. Ohki and Y. Fujita [Mar. Ecol. Prog. Ser. 7, 185 (1982)], and Trichodesmium IMS 101, isolated by Prufert-Bebout et al. (14). The former has been resistant to transplantation, whereas the latter has been disseminated to several laboratories. Additional isolates may now be available.
25. L. Prufert-Bebout, H. W. Paerl, C. Lassen, Appl. Environ. Microbiol. 59, 1367 (1993).
26. The abundance and location of intracellular structures such as gas vacuoles, as well as the form and size of cells and of aggregates or colonies, varies substantially; taxonomic identifications are based on such characteristics [K. Anagnostides and J. Komarek, Arch. Hydrobiol. Suppl. 80, 327 (1988)]. Detailed cytomorphological analysis of natural populations of Trichodesmium in the Caribbean and Sargasso seas, which concluded that there are several distinct morphotypes of Trichodesmium [S. Janson et al., J. Phycol. 31, 463 (1995)], is supported by both nifH (16) [J. Ben-Porath, E. J. Carpenter, J. P. Zehr, ibid. 29, 806 (1993)] and 16S rDNA (S. Janson, K. Virgin, B. Bergman, S. Giovannoni, in preparation) sequence analysis.
27. The abundance and location of intracellular structures such as gas vacuoles, as well as the form and size of cells and of aggregates or colonies, varies substantially; taxonomic identifications are based on such characteristics [K. Anagnostides and J. Komarek, Arch. Hydrobiol. Suppl. 80, 327 (1988)]. Detailed cytomorphological analysis of natural populations of Trichodesmium in the Caribbean and Sargasso seas, which concluded that there are several distinct morphotypes of Trichodesmium [S. Janson et al., J. Phycol. 31, 463 (1995)], is supported by both nifH (16) [J. Ben-Porath, E. J. Carpenter, J. P. Zehr, ibid. 29, 806 (1993)] and 16S rDNA (S. Janson, K. Virgin, B. Bergman, S. Giovannoni, in preparation) sequence analysis.
28. The abundance and location of intracellular structures such as gas vacuoles, as well as the form and size of cells and of aggregates or colonies, varies substantially; taxonomic identifications are based on such characteristics [K. Anagnostides and J. Komarek, Arch. Hydrobiol. Suppl. 80, 327 (1988)]. Detailed cytomorphological analysis of natural populations of Trichodesmium in the Caribbean and Sargasso seas, which concluded that there are several distinct morphotypes of Trichodesmium [S. Janson et al., J. Phycol. 31, 463 (1995)], is supported by both nifH (16) [J. Ben-Porath, E. J. Carpenter, J. P. Zehr, ibid. 29, 806 (1993)] and 16S rDNA (S. Janson, K. Virgin, B. Bergman, S. Giovannoni, in preparation) sequence analysis.
29. J. P. Zehr, K. Ohki, Y. Fujita, J. Bacteriol. 173, 7053 (1991); G. Sroga, U. Landegren, B. Bergman, M. Lagerstrom-Fermer, FEMS Microbiol. Lett. 136, 137 (1996).
30. J. P. Zehr, K. Ohki, Y. Fujita, J. Bacteriol. 173, 7053 (1991); G. Sroga, U. Landegren, B. Bergman, M. Lagerstrom-Fermer, FEMS Microbiol. Lett. 136, 137 (1996).
31. A. Wilmotte, J.-M. Neefs, R. De Wachter, Microbiology 140, 2159 (1994).
32. J. P. Zehr, D. Harris, B. Dominici, J. Salerno, FEMS Microbiol. Lett., in press.
33. J. P. Zehr, M. Wyman, V. Miller, L. Duguay, D. G. Capone, Appl. Environ. Microbiol. 59, 669 (1993).
34. D. G. Capone, J. M. O'Neil, J. Zehr, E. J. Carpenter, ibid. 56, 3532 (1990).
35. M. Wyman, J. P. Zehr, D. G. Capone, ibid. 62, 1073 (1996).
36. K. Ohki, J. P. Zehr, Y. Fujita, J. Gen. Microbiol. 138, 2679 (1992).
37. 2 production equals respiration.
38. 2 by PS I and a source of adenosine triphosphate (76)]; uptake hydrogenase [S. Saino and A. Hattori, Mar. Biol. (Berlin) 70, 251 (1982)]; elevated cytochrome oxidase [B. Bergman, P. J. A. Siddiqui, E. J. Carpenter, G. A. Peschek, Appl. Environ. Microbiol. 59, 3239 (1993)]; photorespiration [W. Li, H. Glover, I. Morris, Limnol. Oceanogr. 25, 447 (1980)]; and superoxide dismutase activity (K. Cunningham and D. G. Capone, in preparation).
39. 2 by PS I and a source of adenosine triphosphate (76)]; uptake hydrogenase [S. Saino and A. Hattori, Mar. Biol. (Berlin) 70, 251 (1982)]; elevated cytochrome oxidase [B. Bergman, P. J. A. Siddiqui, E. J. Carpenter, G. A. Peschek, Appl. Environ. Microbiol. 59, 3239 (1993)]; photorespiration [W. Li, H. Glover, I. Morris, Limnol. Oceanogr. 25, 447 (1980)]; and superoxide dismutase activity (K. Cunningham and D. G. Capone, in preparation).
40. 2 by PS I and a source of adenosine triphosphate (76)]; uptake hydrogenase [S. Saino and A. Hattori, Mar. Biol. (Berlin) 70, 251 (1982)]; elevated cytochrome oxidase [B. Bergman, P. J. A. Siddiqui, E. J. Carpenter, G. A. Peschek, Appl. Environ. Microbiol. 59, 3239 (1993)]; photorespiration [W. Li, H. Glover, I. Morris, Limnol. Oceanogr. 25, 447 (1980)]; and superoxide dismutase activity (K. Cunningham and D. G. Capone, in preparation).
41. G. E. Fogg, in Algal Physiology and Biochemistry, W. D. P. Stewart, Ed. (Blackwell, Oxford, 1974), pp. 650-682.
42. 2 gradients in actively photosynthesizing Trichodesmium colonies at times revealed distinct internal hypoxic or anoxic microzones (27) [H. W. Paerl and B. M. Bebout, Science 241, 442 (1988)].
43. 2 gradients in actively photosynthesizing Trichodesmium colonies at times revealed distinct internal hypoxic or anoxic microzones (27) [H. W. Paerl and B. M. Bebout, Science 241, 442 (1988)].
44. 2 gradients in actively photosynthesizing Trichodesmium colonies at times revealed distinct internal hypoxic or anoxic microzones (27) [H. W. Paerl and B. M. Bebout, Science 241, 442 (1988)].
45. 2 gradients in actively photosynthesizing Trichodesmium colonies at times revealed distinct internal hypoxic or anoxic microzones (27) [H. W. Paerl and B. M. Bebout, Science 241, 442 (1988)].
46. H. W. Paerl and B. M. Bebout, in Marine Pelagic Cyanobacteria: Trichodesmium and Other Diazotrophs, E. J. Carpenter, D. G. Capone, J. Rueter, Eds. (Kluwer Academic, Dordrecht, Netherlands, 1992), pp. 43-59.
47. 2 concentrations for nitrogenase activity.
48. 2 concentrations for nitrogenase activity.
49. Bryceson and Fay (79) first suggested spatial segregation of nitrogenase activity and photosynthesis in cells along a trichome, noting the absence of carboxysomes (sites of RuBisCO) in three to five zones along trichomes of T. erythraeum, which also had higher reducing potentials. Recent immunolocalization studies of several species of field-collected Trichodesmium (78) [C. Fredriksson and B. Bergman, Protoplasma 197, 76 (1997)] and the Trichodesmium IMS 101 isolate (C. Fredriksson, H. Paerl, B. Bergman, in preparation) reported that within individual trichomes, nitrogenase is localized along each trichome in subsets of several cells with distinct ultrastructural features.
50. T. Saino and A. Hattori, Deep Sea Res. 25, 1259 (1978). Subsequent examination of nitrogenase protein dynamics in field populations found active protein only present in the cells during the day (20). Nitrogenase synthesis was initiated in the morning, and activity commenced with the onset of photosynthesis. The daily cycle of synthesis is regulated at the level of transcription, as nifH transcripts were detected before the beginning of the light period preceding the appearance of the protein and were present only until midday in natural populations and in Trichodesmium sp. IMS 101; this indicated that the diel cycle of synthesis was cued by a factor other than light (21). Moreover, there appears to be a subcellular process that results in cessation of activity during the late afternoon. The extant Fe protein component of nitrogenase is converted to an inactive form through an as yet uncharacterized posttranslational protein modification mechanism and "turned off." Immunolocalization studies confirmed that nitrogenase was synthesized and degraded over the day-night cycle (72).
51. 2 fixation in constant light for one cycle in a filamentous benthic oscillatorian that normally confines nitrogenase activity to dark periods.
52. 2 fixation in constant light for one cycle in a filamentous benthic oscillatorian that normally confines nitrogenase activity to dark periods.
53. 2 fixation in constant light for one cycle in a filamentous benthic oscillatorian that normally confines nitrogenase activity to dark periods.
54. Y. Chen, J. P. Zehr, M. Mellon, J. Phycol. 32, 96 (1996). A daily cycle of nitrogenase induction and activity persisted for up to six cycles in constant light with a free-running clock of about 26 hours. A diel variation in the compensation point has also been reported; this may be driven by an endogenous rhythm in respiration, because photosynthetic parameters do not exhibit a comparable daily cycle under continuous illumination (75).
55. 2 uptake (3, 4).
56. It had been speculated that molybdenum was a primary limiting factor for Trichodesmium [R. W. Howarth and J. J. Cole, Science 229, 653 (1985)], although no substantial evidence has been provided. In contrast, because nitrogenase is an Fe-rich protein, the cell quota for Fe of Trichodesmium is considerably higher than in other phytoplankton (35). Trichodesmium is capable of rapid Fe uptake, although it does not appear to produce siderophores (35). Fe additions can stimulate Trichodesmium growth and activity [J. G. Rueter et al., J. Phycol. 26, 30 (1990); H. W. Paerl, L. Prufert-Bebout, C. Guo, Appl. Environ. Microbiol. 60, 1044 (1994)]. Trichodesmium growth in situ also requires phosphorus, and the source of its phosphorus requirement has been the focus of some attention (4, 36).
57. It had been speculated that molybdenum was a primary limiting factor for Trichodesmium [R. W. Howarth and J. J. Cole, Science 229, 653 (1985)], although no substantial evidence has been provided. In contrast, because nitrogenase is an Fe-rich protein, the cell quota for Fe of Trichodesmium is considerably higher than in other phytoplankton (35). Trichodesmium is capable of rapid Fe uptake, although it does not appear to produce siderophores (35). Fe additions can stimulate Trichodesmium growth and activity [J. G. Rueter et al., J. Phycol. 26, 30 (1990); H. W. Paerl, L. Prufert-Bebout, C. Guo, Appl. Environ. Microbiol. 60, 1044 (1994)]. Trichodesmium growth in situ also requires phosphorus, and the source of its phosphorus requirement has been the focus of some attention (4, 36).
58. It had been speculated that molybdenum was a primary limiting factor for Trichodesmium [R. W. Howarth and J. J. Cole, Science 229, 653 (1985)], although no substantial evidence has been provided. In contrast, because nitrogenase is an Fe-rich protein, the cell quota for Fe of Trichodesmium is considerably higher than in other phytoplankton (35). Trichodesmium is capable of rapid Fe uptake, although it does not appear to produce siderophores (35). Fe additions can stimulate Trichodesmium growth and activity [J. G. Rueter et al., J. Phycol. 26, 30 (1990); H. W. Paerl, L. Prufert-Bebout, C. Guo, Appl. Environ. Microbiol. 60, 1044 (1994)]. Trichodesmium growth in situ also requires phosphorus, and the source of its phosphorus requirement has been the focus of some attention (4, 36).
59. J. G. Rueter et al., in (27), pp. 289-306.
60. D. M. Karl et al., ibid., pp. 219-237.
61. C. VanBaalen and R. M. Brown, Arch. Microbiol. 69, 79 (1969); A. Walsby, Br. Phycol. J. 13, 103 (1978); E. Gantt et al., Protoplasma 119, 188 (1984). Trichodesmium gas vesicles, which can survive pressures at depth in excess of 200 m, have the highest collapse pressure of any cyanobacterial vesicles yet examined.
62. C. VanBaalen and R. M. Brown, Arch. Microbiol. 69, 79 (1969); A. Walsby, Br. Phycol. J. 13, 103 (1978); E. Gantt et al., Protoplasma 119, 188 (1984). Trichodesmium gas vesicles, which can survive pressures at depth in excess of 200 m, have the highest collapse pressure of any cyanobacterial vesicles yet examined.
63. C. VanBaalen and R. M. Brown, Arch. Microbiol. 69, 79 (1969); A. Walsby, Br. Phycol. J. 13, 103 (1978); E. Gantt et al., Protoplasma 119, 188 (1984). Trichodesmium gas vesicles, which can survive pressures at depth in excess of 200 m, have the highest collapse pressure of any cyanobacterial vesicles yet examined.
64. T. Villareal and E. J. Carpenter. Limnol. Oceanogr. 35, 1832 (1990); K. M. Romans, E. J. Carpenter, B. Bergman, J. Phycol. 30, 935 (1994).
65. T. Villareal and E. J. Carpenter. Limnol. Oceanogr. 35, 1832 (1990); K. M. Romans, E. J. Carpenter, B. Bergman, J. Phycol. 30, 935 (1994).
66. max = 595 nm), thereby reducing absorption at lower wavelengths (80).
67. max = 595 nm), thereby reducing absorption at lower wavelengths (80).
68. max = 595 nm), thereby reducing absorption at lower wavelengths (80).
69. max = 595 nm), thereby reducing absorption at lower wavelengths (80).
70. V. P. Devassy, P. M. Bhattathiri, S. Z. Qasim, Indian J. Mar. Sci. 7, 168 (1978); R. Santhanam et al., ibid. 23, 27 (1994); (36). For a summary of historical reports of extensive blooms over the last several decades, see E. J. Carpenter and D. G. Capone, in (27), pp. 211-217.
71. V. P. Devassy, P. M. Bhattathiri, S. Z. Qasim, Indian J. Mar. Sci. 7, 168 (1978); R. Santhanam et al., ibid. 23, 27 (1994); (36). For a summary of historical reports of extensive blooms over the last several decades, see E. J. Carpenter and D. G. Capone, in (27), pp. 211-217.
72. 2. Trichodesmium blooms have also been observed from the U.S. space shuttle [for example, D. A. Kuchler and D. Jupp, Int. J. Remote Sens. 9, 1299 (1988)].
73. 2. Trichodesmium blooms have also been observed from the U.S. space shuttle [for example, D. A. Kuchler and D. Jupp, Int. J. Remote Sens. 9, 1299 (1988)].
74. A. Subramaniam and E. J. Carpenter, Int. J. Remote Sens. 15, 1559 (1994).
75. R. L. Oliver and G. G. Ganf, J. Plankton Res. 10, 1155 (1988). Trichodesmium, with its UV-absorbing compounds and phycobiliproteins, displays higher absorption than eukaryotic phytoplankton in the UV and blue regions of the spectrum (80).
76. Episodic phytoplankton blooms may contribute to feedback in the warm water pool climate system in the Pacific [D. A. Siegel et al., J. Geophys. Res. 100, 4885 (1995)]. Cyanobacterial blooms in the Baltic Sea increase sea surface temperature locally by 1.5°C [M. Kahru, J.-M. Leppanen, O. Rud, Mar. Ecol. Prog. Ser. 191, 1 (1993)]. Phytoplankton biomass may influence the flux of moisture [S. Sathyendranath et al., Nature 349, 54 (1991)]. The dense accumulation of planktonic biomass at the interface may increase viscosity [I. R. Jenkinson, Oceanol. Acta 16, 317 (1993)] providing turbulent damping and increasing diffusion rates across the air-sea interface.
77. Episodic phytoplankton blooms may contribute to feedback in the warm water pool climate system in the Pacific [D. A. Siegel et al., J. Geophys. Res. 100, 4885 (1995)]. Cyanobacterial blooms in the Baltic Sea increase sea surface temperature locally by 1.5°C [M. Kahru, J.-M. Leppanen, O. Rud, Mar. Ecol. Prog. Ser. 191, 1 (1993)]. Phytoplankton biomass may influence the flux of moisture [S. Sathyendranath et al., Nature 349, 54 (1991)]. The dense accumulation of planktonic biomass at the interface may increase viscosity [I. R. Jenkinson, Oceanol. Acta 16, 317 (1993)] providing turbulent damping and increasing diffusion rates across the air-sea interface.
78. Episodic phytoplankton blooms may contribute to feedback in the warm water pool climate system in the Pacific [D. A. Siegel et al., J. Geophys. Res. 100, 4885 (1995)]. Cyanobacterial blooms in the Baltic Sea increase sea surface temperature locally by 1.5°C [M. Kahru, J.-M. Leppanen, O. Rud, Mar. Ecol. Prog. Ser. 191, 1 (1993)]. Phytoplankton biomass may influence the flux of moisture [S. Sathyendranath et al., Nature 349, 54 (1991)]. The dense accumulation of planktonic biomass at the interface may increase viscosity [I. R. Jenkinson, Oceanol. Acta 16, 317 (1993)] providing turbulent damping and increasing diffusion rates across the air-sea interface.
79. Episodic phytoplankton blooms may contribute to feedback in the warm water pool climate system in the Pacific [D. A. Siegel et al., J. Geophys. Res. 100, 4885 (1995)]. Cyanobacterial blooms in the Baltic Sea increase sea surface temperature locally by 1.5°C [M. Kahru, J.-M. Leppanen, O. Rud, Mar. Ecol. Prog. Ser. 191, 1 (1993)]. Phytoplankton biomass may influence the flux of moisture [S. Sathyendranath et al., Nature 349, 54 (1991)]. The dense accumulation of planktonic biomass at the interface may increase viscosity [I. R. Jenkinson, Oceanol. Acta 16, 317 (1993)] providing turbulent damping and increasing diffusion rates across the air-sea interface.
80. J. O'Neil and M. Roman, in (27), pp. 61-73.
81. S. Hawser et al., J. Appl. Phycol. 4, 79 (1992).
82. Some harpacticoid copepods are able to graze Trichodesmium to >75% of their body weight per day [J. O'Neil and M. Roman, Hydrobiologia 292-293, 235 (1994)] and can consume 33 to 45% of colony N per day [J. O'Neil, P. M. Metzer, P. Gilbert, Mar. Biol. (Berlin) 125, 89 (1996)].
83. Some harpacticoid copepods are able to graze Trichodesmium to >75% of their body weight per day [J. O'Neil and M. Roman, Hydrobiologia 292-293, 235 (1994)] and can consume 33 to 45% of colony N per day [J. O'Neil, P. M. Metzer, P. Gilbert, Mar. Biol. (Berlin) 125, 89 (1996)].
84. 15N-dissotved organic N (P. Gilbert and D. Bronk, ibid., p. 3996).
85. 15N-dissotved organic N (P. Gilbert and D. Bronk, ibid., p. 3996).
86. H. W. Paerl, B. M. Bebout, L. E. Prufert. J. Phycol. 25, 773 (1989).
87. Cruises through regions in which Trichodesmium blooms occur are infrequent, and conventional oceanographic cruises seldom allow time for opportunistic sampling of blooms. Moreover, because of their size and buoyancy, traditional methods of microplankton sampling are strongly biased against accurate assessment of Trichodesmium even under nonbloom conditions. Trichodesmium is often viewed as a nuisance organism in plankton net-based sampling focused on microplankton collection and quantitation, as high densities clog nets. Net sampling, unless performed carefully at low towing speeds and with fine-mesh nets (≤ 100 μm), will disrupt the relatively delicate colonies. Routine protocols for plankton counting, measuring chlorophyll and primary productivity on samples drawn from water bottles, may also impose biases. Because colonies are buoyant, they rapidly rise to the top of water sample bottles (sample water is drawn from the bottom). Relatively small sample volumes are used in most of these procedures (∼300 ml and often less) and would likely undersample large colonial phytoplankton, such as Trichodesmium, that typically occur at concentrations at or below one colony per liter (under nonbloom conditions). Prescreening of water, commonly performed to remove large zooplankton, also removes Trichodesmium colonies, thereby eliminating their contribution to estimates of biomass or C fixation. Moreover, unless discharged by acid treatment, gas vesicles prevent cells from sinking in Utermohl settling chambers (used for counting phytoplankton) or sedimenting during centrifugation. Results from conventional oceanographic phytoplankton surveys in tropical areas should therefore be viewed cautiously with regard to their accuracy in quantitatively estimating Trichodesmium abundance and total C and N fixation unless sampling and handling protocols were specifically adapted to account for these organisms. Recent satellite evidence (41, 42) reinforces the proposition that planktonic diazotrophs are undersampled.
88. 2 fixation, which, for large expanses of the ocean, depended on historical plankton surveys that likely underestimated abundances of Trichodesmium (50).
89. 2 fixation, which, for large expanses of the ocean, depended on historical plankton surveys that likely underestimated abundances of Trichodesmium (50).
90. 2 fixation [R. C. Dugdale and J. J. Goering, Limnol. Oceanogr. 12, 196 (1967)]. Relative to other sources of new N, nitrate from depth is generally considered the most important (82-84).
91. D. G. Capone, Mitt. Int. Ver. Theor. Angew. Limnol. 25, 105 (1996); (82, 85).
92. The oceans likely play a key role in the global C cycle [U. Siegenthaller and J. Sarmiento, Nature 365, 119 (1993)]. It is postulated that the marine biota serve as a "biological pump" for sequestering C into the deep ocean [A. R. Longhurst and W. G. Harrison, Prog. Oceanogr. 22, 47 (1989)].
93. The oceans likely play a key role in the global C cycle [U. Siegenthaller and J. Sarmiento, Nature 365, 119 (1993)]. It is postulated that the marine biota serve as a "biological pump" for sequestering C into the deep ocean [A. R. Longhurst and W. G. Harrison, Prog. Oceanogr. 22, 47 (1989)].
94. 2.
95. 2 fixation.
96. 2 fixation.
97. 2 fixation.
98. 2 fixation.
99. 2 fixation.
100. - uptake may be considered recycled production [B. B. Ward, K. A. Kilpatrick, E. H. Renger, R. W. Eppley, Limnol. Oceanogr. 34, 493 (1989)].
101. - uptake may be considered recycled production [B. B. Ward, K. A. Kilpatrick, E. H. Renger, R. W. Eppley, Limnol. Oceanogr. 34, 493 (1989)].
102. - uptake may be considered recycled production [B. B. Ward, K. A. Kilpatrick, E. H. Renger, R. W. Eppley, Limnol. Oceanogr. 34, 493 (1989)].
103. - flux is computed as the product of
104. 2 dynamics in the upper water column exceed estimates of input fluxes (88); PON export can exceed conventional inputs (36, 89).
105. + (91). However, these processes are unlikely in the highly oligotrophic open ocean (90).
106. + (91). However, these processes are unlikely in the highly oligotrophic open ocean (90).
107. + (91). However, these processes are unlikely in the highly oligotrophic open ocean (90).
108. + (91). However, these processes are unlikely in the highly oligotrophic open ocean (90).
109. + (91). However, these processes are unlikely in the highly oligotrophic open ocean (90).
110. + (91). However, these processes are unlikely in the highly oligotrophic open ocean (90).
111. + (91). However, these processes are unlikely in the highly oligotrophic open ocean (90).
112. Trichodesmium spp. can represent a major fraction (∼60%) of total chlorophyll and are important in primary production and N input in the Caribbean Sea (92). In the Indian Ocean, Trichodesmium can reach a biomass of up to 30 mg of chlorophyll a per cubic meter (79). E. J. Carpenter and K. Romans [Science 254, 1356 (1991)] concluded that Trichodesmium is the most abundant phytoplankton in the tropical North Atlantic. C. S. Davis, S. M. Gallager, and A. R. Solow [ibid. 257, 230 (1992)], using towed video microscopy, found very high abundance of Trichodesmium in North Atlantic waters. Trichodesmium accounted for a mean of 17% of total chlorophyll a throughout the year at the HOT station (58). Richelia intracellularis (a common endosymbiont of diatoms) [T. Villareal, in (27), pp. 163-175] can also contribute substantially to new N inputs (E. J. Carpenter et al., in preparation).
113. Trichodesmium spp. can represent a major fraction (∼60%) of total chlorophyll and are important in primary production and N input in the Caribbean Sea (92). In the Indian Ocean, Trichodesmium can reach a biomass of up to 30 mg of chlorophyll a per cubic meter (79). E. J. Carpenter and K. Romans [Science 254, 1356 (1991)] concluded that Trichodesmium is the most abundant phytoplankton in the tropical North Atlantic. C. S. Davis, S. M. Gallager, and A. R. Solow [ibid. 257, 230 (1992)], using towed video microscopy, found very high abundance of Trichodesmium in North Atlantic waters. Trichodesmium accounted for a mean of 17% of total chlorophyll a throughout the year at the HOT station (58). Richelia intracellularis (a common endosymbiont of diatoms) [T. Villareal, in (27), pp. 163-175] can also contribute substantially to new N inputs (E. J. Carpenter et al., in preparation).
114. 2 fixation were generally low compared with tropical waters.
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120. -1 on the basis of a two-decade data set of tritium penetration.
121. -1 on the basis of a two-decade data set of tritium penetration.
122. -1 on the basis of a two-decade data set of tritium penetration.
123. -1 through the rest of the water column.
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157. 2 fixation, on isolated colonies and scaled to trichome concentrations at specific depth.
158. We thank M. Mulholland, J. Burns, L. Duguay, J. Montoya, and two anonymous reviewers for their comments, A. Parrella for technical assistance, and F. Younger for artwork. We particularly thank A. Subramaniam for discussion and help on the remote sensing images. D.G.C. thanks B. Taylor for introducing him to Trichodesmium. Supported by the NSF Divisions of Ocean Sciences and Environmental Biology.