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Marine Phototrophs in the Twilight Zone

  • Noga Stambler
  • Zvy Dubinsky
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 11)

Phototrophs (photolithoautotrophs) are organisms that use light as their energy source to synthesize organic compounds. These organisms include some bacteria, cyanobacteria, algae, and plants. They harvest light by various pigments, the main of these being chlorophylls, and its energy is transferred to the photosynthetic reaction centers. Even though phototrophs depend on light for their survival, some of these grow under very low light.

In general, the terrestrial light flux, even under the most intense sunlight is too low for single chlorophyll molecules to sustain photosynthesis, since the arrival of photons would be so slow that the S states (Kok et al., 1970, Falkowski and Raven, 1997) would decay spontaneously, not allowing generation of oxygen or carbon reduction. In reality, light is harvested in the photosynthetic apparatus by “antennae,” consisting of hundreds of pigment molecules embedded in the thylakoids or similar membranes. The antennae have a far larger cross section,σ, or probability of intercepting a photon than single pigment molecules. The energy intercepted by the antennae migrates as excitation energy to the few chlorophyll molecules in the photosynthetic reaction centers.

Keywords

Coral Reef Particulate Organic Carbon Coralline Alga Coral Skeleton Green Sulfur Bacterium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Airs, R. L., Borrego, C. M., Garcia-Gil, J., and Keely, B. J. (2001) Identification of the bacteri- ochlorophyll homologues of Chlorobium phaeobacteroides strain UdG6053 grown at low light intensity. Photosynth. Res. 70, 221-230.CrossRefPubMedGoogle Scholar
  2. Aponte, N. E., and Ballantine, D. L. (2001) Depth distribution of algal species on the deep insular fore reef at Lee Stocking Island, Bahamas. Deep Sea Res. Part I Oceanogr. Res. Pap. 48, 2185-2194.CrossRefGoogle Scholar
  3. Baldisserotto, C., Ferroni, L., Andreoli, C., Fasulo, M. P., Bonora, A., and Pancaldi, S. (2005) Dark-acclimation of the chloroplast in Koliella antarctica exposed to a simulated austral night condition. Arct. Antarct. Alp. Res. 37, 146-156.CrossRefGoogle Scholar
  4. Bassham, J. A., Krohne, S., and Lendzian, K. (1978) In vivo control mechanism of the carboxylation reaction, In: H.W. Siegelman and G. Hind, (eds.) Photosynthesis Carbon Assimilation Plenum Press, New York, pp. 77-93.Google Scholar
  5. Beatty, J. T., Overmann, J., Lince, M. T., Manske, A. K., Lang, A. S., Blankenship, R. E., Van Dover, C. L., Martinson, T. A., and Plumley, F. G. (2005) An obligately photosynthetic bacterial anaer-obe from a deep-sea hydrothermal vent. Proc. Natl. Acad. Sci. U.S.A. 102, 9306-9310.CrossRefPubMedGoogle Scholar
  6. Beer, S., and Ilan, M. (1998) In situ measurements of photosynthetic irradiance responses of two Red Sea sponges growing under dim light conditions. Mar. Biol. 131, 613-617.CrossRefGoogle Scholar
  7. Berner, T., and Evenari, M. (1978) Ecophysiological activity of hypolithic desert algae. J. Phycol. 14, 39.Google Scholar
  8. Berner, T., Wishkovsky, A., and Dubinsky, Z. (1986a) Endozoic algae in shelled gastropods - a new symbiotic association in coral reefs. 1. Photosynthetically active zooxanthellae in Strombus tricornis. Coral Reefs 5, 103-106.CrossRefGoogle Scholar
  9. Berner, T., Wishkovsky, A., and Dubinsky, Z. (1986b) Endozoic algae in shelled gastropods - a new symbiotic association in coral reefs. 2. Survey of distribution of endozoic algae in red-sea snails. Coral Reefs 5, 107-109.CrossRefGoogle Scholar
  10. Berner, T., Wyman, K., Dubinsky, Z., and Falkowski, P. G. (1989) Photoadaptation and the “pack-age” effect in Dunaliella tertiolecta (Chlorophyceae). J. Phycol. 25, 70-78.CrossRefGoogle Scholar
  11. Bibby, T. S., Nield, J., Partensky, F., and Barber, J. (2001) Oxyphotobacteria. Antenna ring around photosystem I. Nature 413, 590.CrossRefPubMedGoogle Scholar
  12. Blankenship, R. E., Miller, M., and Olson, J. M. (1995) Antenna complexes from green photosyn-thetic bacteria, In: R.E. Blankenship, M.T. Madigan, and C.E. Bauer, (eds.) Anoxygenic Photosynthetic Bacteria Kluwer Academic Publishing, Dordrecht, pp. 399-435.Google Scholar
  13. Bohannon, J. (2005) Marine biology. Microbe may push photosynthesis into deep water. Science 308, 1855.CrossRefPubMedGoogle Scholar
  14. Brandt, J. (1883) Uber die morphologische und physiologische Bedeutung des Chlorophylls bei Tieren. Zool. Stn. Neapol. 4, 191-302.Google Scholar
  15. Chen, M., Telfer, A., Lin, S., Pascal, A., Larkum, A. W. D., Barber, J., and Blankenship, R. E. (2005) The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina. Photochem. Photobiol. Sci. 4, 1060-1064.CrossRefPubMedGoogle Scholar
  16. Chisholm, J. R. M. (2003) Primary productivityof reef-building crustose coralline algae. Limnol. Oceanogr. 48, 1376-1387.CrossRefGoogle Scholar
  17. Chisholm, S. W. (1992) Phytoplankton size, In: P.G. Falkowski and A.D. Woodhead, (eds.) Primary Productivity and Biogeochemical Cycles in the Sea, Plenum Press, New York, pp. 213-237.Google Scholar
  18. Cole, K. M., and Sheath, R. G. (1990) Biology of Red Algae, Cambridge University Press, New York.Google Scholar
  19. Doty, M. S., Gilbert, W. J., and Abbott, I. A. (1974) Hawaiian marine algae from seaward of the algal ridge. Phycologia 13, 345-357.Google Scholar
  20. Dubinsky, Z. (1992) The functional and optical absorption cross-sections of phytoplankton photo-synthesis, In: P.G. Falkowski and A.D. Woodhead, (eds.) Primary Productivity and Biogeochemical Cycles in the Sea Plenum Press, New York, pp. 31-45.Google Scholar
  21. Dubinsky, Z., Falkowski, P. G., and Wyman, K. (1986) Light harvesting and utilization in phyto-plankton. Plant Cell Physiol. 27, 1335-1349.Google Scholar
  22. Dufresne, A., Salanoubat, M., Partensky, F., Artiguenave, F., Axmann, I. M., Barbe, V., Duprat, S., Galperin, M. Y., Koonin, E. V., Le Gall, F., Makarova, K. S., Ostrowski, M., Oztas, S., Robert, C., Rogozin, I. B., Scanlan, D. J., de Marsac, N. T., Weissenbach, J., Wincker, P., Wolf, Y. I., and Hess, W. R. (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc. Natl. Acad. Sci. U.S.A. 100, 10020-10025.CrossRefPubMedGoogle Scholar
  23. Estrada, M., Marrase, C., Latasa, M., Berdalet, E., Delgado, M., and Riera, T. (1993) Variability of deep chlorophyll maximum characteristics in the Northwestern Mediterranean. Mar. Ecol. Prog. Ser. 92, 289-300.CrossRefGoogle Scholar
  24. Falkowski, P. G., and Owens, T. G. (1978) Effects of light intensity on photosynthesis and dark respi-ration in six species of marine phytoplankton. Mar. Biol. 45, 289-295.CrossRefGoogle Scholar
  25. Falkowski, P. G., and Raven, J. A. (1997) Aquatic Photosynthesis, Blackwell Science, Massachusetts.Google Scholar
  26. Fork, D. C., and Larkum, A. W. D. (1989) Light harvesting in the green-alga Ostreobium sp, a coral symbiont adapted to extreme shade. Mar. Biol. 103, 381-385.CrossRefGoogle Scholar
  27. Gorbunov, M. Y., and Falkowski, P. G. (2002) Photoreceptors in the cnidarian hosts allow symbiotic corals to sense blue moonlight. Limnol. Oceanogr. 47, 309-315.CrossRefGoogle Scholar
  28. Grzymski, J., Schofield, O. M., Falkowski, P. G., and Bernhard, J. M. (2002) The function of plastids in the deep-sea benthic foraminifer, Nonionella stella. Limnol. Oceanogr. 47, 1569-1580.CrossRefGoogle Scholar
  29. Halldal, P. (1968) Photosynthetic capacities and photosynthetic action spectra of endozoic algae of the massive coral Favia. Bull. Mar. Biol. Lab. 134, 411-424.CrossRefGoogle Scholar
  30. Holzwarth, A. R., Griebenow, K., and Schaffner, K. (1992) Chlorosomes, photosynthetic antennae with novel self-organized pigment structures.J. Photochem. Photobiol. A Chem. 65, 61-71.CrossRefGoogle Scholar
  31. Jeffrey, S. W. (1968) Pigment composition of siphonales algae in brain coral Favia. Biol. Bull. 135, 141-148.CrossRefGoogle Scholar
  32. Jeffrey, S. W., Mantoura, R. F. C., and Wright, S. W. (1997) Phytoplankton Pigments in Oceanography, UNESCO Publishing, Paris.Google Scholar
  33. Jerlov, N. G. (1976) Elsevier Oceanography Series, 14. Marine Optics, 231 pp, Elsevier Scientific Publishers, Amsterdam, Oxford, New York.Google Scholar
  34. Jochem, F. J. (1999) Dark survival strategies in marine phytoplankton assessed by cytometric meas-urement of metabolic activity with fluorescein diacetate. Mar. Biol. 135, 721-728.CrossRefGoogle Scholar
  35. Kanwishe, J. W., and Wainwrig, S. A. (1967) Oxygen balance in some reef corals. Biol. Bull. 133, 378-390.CrossRefGoogle Scholar
  36. Kiefer, D. A., Olson, R. J., and Holmhansen, O. (1976) Another look at nitrite and chlorophyll max-ima in central North Pacific. Deep-Sea Res. 23, 1199-1208.Google Scholar
  37. Kirk, J. T. O. (1986) Optical properties of picoplankton suspensions, In: T. Platt and W.K.W. Li, (eds.) Photosynthetic Picoplankton Canada Bulletin Fish. Aquatic Science 214: pp. 501-520.Google Scholar
  38. Kirk, J. T. O. (1994) Light and Photosynthesis in Aquatic Ecosystems, 2nd ed., 509 pp, Cambridge University Press, London, New York.Google Scholar
  39. Kok, B., Forbush, B., and MCGLOIN, M. (1970) Cooperation of charges in photosynthetic O2 evo-lution. 1. A linear 4-step mechanism. Photochem. Photobiol. 11, 453-475.CrossRefGoogle Scholar
  40. Kuhl, M., Chen, M., Ralph, P. J., Schreiber, U., and Larkum, A. W. D. (2005) A niche for cyanobac-teria containing chlorophyll d. Nature 433, 820.CrossRefPubMedGoogle Scholar
  41. Lang, J. C. (1974) Biological zonation at base of areef. Am. Sci. 62, 272-281.Google Scholar
  42. Larkum, A. W. D., and Kuhl, M. (2005) Chlorophylld: the puzzle resolved. Trends Plant Sci. 10, 355-357.CrossRefPubMedGoogle Scholar
  43. Lewin, R. A., and Withers, N. W. (1975) Extraordinary pigment composition of a prokaryotic alga. Nature 256, 735-737.CrossRefGoogle Scholar
  44. Littler, M. M., Littler, D. S., Blair, S. M., and NORRIS, J. N. (1985) Deepest known plant life dis-covered on an uncharted seamount. Science 227, 57-59.CrossRefPubMedGoogle Scholar
  45. Littler, M. M., Littler, D. S., Blair, S. M., and NORRIS, J. N. (1986) Deep-water plant-communities from an uncharted seamount off San Salvador Island, Bahamas - distribution, abundance, and primary productivity. Deep-Sea Res. Part A-Oceanogr. Res. Pap. 33, 881-892.CrossRefGoogle Scholar
  46. Marquardt, J., Senger, H., Miyashita, H., Miyachi, S., and Morschel, E. (1997) Isolation and charac-terization of biliprotein aggregates from Acaryochloris marina, a Prochloron-like prokaryote con-taining mainly chlorophyll d. FEBS Lett. 410, 428-432.CrossRefPubMedGoogle Scholar
  47. Marris, E. (2005) The life aquatic. Nature 436, 908-909.CrossRefPubMedGoogle Scholar
  48. Morel, A., and Prieur, L. (1977) Analysis of variations in ocean color. Limnol. Oceanogr. 22, 709-722.Google Scholar
  49. Morel, A., Ahn, Y.-W., Partensky, F., Vaulot, D., and Claustre, H. (1993) Prochlorococcus and Synechococcus: a comparative study of their size, pigmentation and related optical properties. J. Mar. Res. 51, 617-649.CrossRefGoogle Scholar
  50. Murphy, A. M., and Cowles, T. J. (1997) Effects of darkness on multi-excitation in vivo fluorescence and survival in a marine diatom. Limnol. Oceanogr. 42, 1444-1453.Google Scholar
  51. Muscatine, L. (1990) The role of symbiotic algal in carbon and energy flux in reef corals, In: Z. Dubinsky, (ed.) Coral Reefs Elsevier, Amsterdam, pp. 75-87.Google Scholar
  52. Odum, H. T., and Odum, E. P. (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol. Monogr. 25, 291-320.CrossRefGoogle Scholar
  53. Olson, J. M. (1998) Chlorophyll organizationand function in green photosynthetic bacteria. Photochem. Photobiol. 67, 61-75.CrossRefGoogle Scholar
  54. Overmann, J., and Garcia-Pichel, F. (2005) The phototrophic way of life, In: M. Dworkin, (ed.) The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, Springer, New York.Google Scholar
  55. Overmann, J., Beatty, J. T., HALL, K. J., Pfennig, N., and Northcote, T. G. (1991) Characterization of a dense, purple sulfur bacterial layer in a meromictic salt lake. Limnol. Oceanogr. 36, 846-859.CrossRefGoogle Scholar
  56. Owrid, G., Socal, G., Civitarese, G., Luchetta, A., Wiktor, J., Nothig, E. M., Andreassen, I., Schauer, U., and Strass, V. (2000) Spatial variability of phytoplankton, nutrients and new production esti-mates in the waters around Svalbard. Polar Res. 19, 155-171.CrossRefGoogle Scholar
  57. Partensky, F., Hess, W. R., and Vaulot, D. (1999) Prochlorococcus, a marine photosynthetic prokary-ote of global significance. Microbiol Mol Biol Rev. 63, 106-127.PubMedGoogle Scholar
  58. Porter, J., Muscatine, L., Dubinsky, Z., and Falkowski, P. G. (1984) Reef coral energetics: primary pro-duction and photoadaptation. Proc. R. Soc. Lond. 222B, 161-180.CrossRefGoogle Scholar
  59. Reynolds, G. T., and Lutz, R. A. (2001) Sources of light in the deep ocean. Rev Geophys. 39, 123-136.CrossRefGoogle Scholar
  60. Rink, S., Kuhl, M., Bijma, J., and Spero, H. J. (1998) Microsensor studies of photosynthesis and res-piration in the symbiotic foraminifer Orbulina universa. Mar. Biol. 131, 583-595.CrossRefGoogle Scholar
  61. Roberts, R. D., Kuhl, M., Glud, R. N., and Rysgaard, S. (2002) Primary production of crustose coralline red algae in a high Arctic fjord. J. Phycol. 38, 273-283.CrossRefGoogle Scholar
  62. Samsonoff, W. A., and MacColl, R. (2001) Biliproteins and phycobilisomes from cyanobacteria and red algae at the extremes of habitat. Arch. Microbiol. 176, 400-405.CrossRefPubMedGoogle Scholar
  63. Schlichter, D., and Fricke, H. W. (1991) Mechanisms of amplification of photosynthetically active radiation in the symbiotic deep-water coral Leptoseris fragili. Hydrobiologia 216, 389-394.CrossRefGoogle Scholar
  64. Schonberg, C. H. L., de Beer, D., and Lawton, A. (2005) Oxygen microsensor studies on zooxanthel-late clionaid sponges from the Costa Brava, Mediterranean Sea. J. Phycol. 41, 774-779.CrossRefGoogle Scholar
  65. Schumacher, H., and Zibrowius, H. (1985) What is hermatypic? A redefinition of ecological groups in corals and other organisms. Coral Reefs 4, 1-9.CrossRefGoogle Scholar
  66. Schwarz, A. M., Hawes, I., Andrew, N., Mercer, S., Cummings, V., and Thrush, S. (2005) Primary pro-duction potential of non-geniculate coralline algae at Cape Evans, Ross Sea, Antarctica. Mar. Ecol. Prog. Ser. 294, 131-140.CrossRefGoogle Scholar
  67. Shashar, N., and Stambler, N. (1992) Endolithic algae within corals - life in an extreme environment. J. Exp. Mar. Biol. Ecol. 163, 277-286.CrossRefGoogle Scholar
  68. Shibata, K., and Haxo, F. T. (1969) Light transmission and spectral distribution through epi- and endozoic algal layers in the brain coral Favia. Biol. Bull. 136, 461-468.CrossRefGoogle Scholar
  69. Soohoo, J. B., Palmisano, A. C., Kottmeier, S. T., Lizotte, M. P., Soohoo, S. L., and Sullivan, C. W. (1987) Spectral light-absorption and quantum yield of photosynthesis in sea ice microalgae and a bloom of Phaeocystis pouchetii from Mcmurdo Sound, Antarctica. Mar. Ecol. Prog. Ser. 39, 175-189.CrossRefGoogle Scholar
  70. Stambler, N. (2006) Light and picophytoplankton in the Gulf of Eilat (Aqaba). Journal of Geophysical Research - Oceans, 111, C11009, doi:10.1029/2005JC003373.CrossRefGoogle Scholar
  71. Steglich, C., Frankenberg-Dinkel, N., Penno, S., and Hess, W. R. (2005) A green light-absorbing phy-coerythrin is present in the high-light-adapted marine cyanobacterium Prochlorococcus sp MED4. Environ. Microbiol. 7, 1611-1618.CrossRefPubMedGoogle Scholar
  72. Steglich, C., Mullineaux, C. W., Teuchner, K., Hess, W. R., and Lokstein, H. (2003) Photophysical properties of Prochlorococcus marinus SS120 divinyl chlorophylls and phycoerythrin in vitro and in vivo. FEBS Lett. 553, 79-84.CrossRefPubMedGoogle Scholar
  73. Steindler, L., Beer, S., and Ilan, M. (2002) Photosymbiosis in intertidal and subtidal tropical sponges. Symbiosis 33, 263-273.Google Scholar
  74. Tilzer, M. M., and Dubinsky, Z. (1987) Effects of temperature and day length on the mass balance of Antarctic phytoplankton. Polar Biol. 7, 35-42.CrossRefGoogle Scholar
  75. Van Dover, C. L. (2000) The Ecology of Deep-Sea Hydrothermal Vents, Princeton University Press, UK.Google Scholar
  76. VanDover, C. L., Reynolds, G. T., Chave, A. D., and Tyson, J. A. (1996) Light at deep-sea hydrother-mal vents. Geophys. Res. Lett. 23, 2049-2052.CrossRefGoogle Scholar
  77. White, S. N., Chave, A. D., Reynolds, G. T., and Van Dover, C. L. (2002) Ambient light emission from hydrothermal vents on the Mid-Atlantic Ridge. Geophys. Res. Lett. 29,Google Scholar
  78. Yurkov, V. V., and Beatty, J. T. (1998) Aerobic anoxygenic phototrophic bacteria. Microbiol. Mol. Biol. Rev. 62, 695-724.PubMedGoogle Scholar
  79. Zhang, Q., Gradinger, R., and Zhou, Q. S. (2003) Competition within the marine microalgae over the polar dark period in the Greenland Sea of high Arctic. Acta Oceanol. Sin. 22, 233-242.Google Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Noga Stambler
    • 1
  • Zvy Dubinsky
    • 1
  1. 1.The Mina & Everard Goodman Faculty of Life SciencesBar-Ilan UniversityIsrael

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