Abstract
In marine tropical or subtropical plankton the filamentous, heterocyst-forming cyanobacterium Richelia intracellularis forms a symbiosis with the diatom Rhizosolenia clevei. An ultrastructural analysis of the apex of Rhizosolenia clevei showed that the cytoplasm in that particular part of the cell was present only where the cyanobiont was located. The cyanobiont was, however, always outside the host cytoplasm. Vegetative cells as well as the heterocysts of the cyanobiont were devoid of gas vesicles and cyanophycin granules, while carboxysomes and large glycogen granules were common. The cyanobacterial cell wall apparently remained intact in both vegetative and heterocyst cells. In green excitation light the heterocysts and vegetative cells emitted a bright yellow fluorescence, indicating that both cell types possessed high concentrations of the pigment phycoerythrin (PE) commonly associated with photosystem (PS) II. The presence of this pigment in both cell types was verified by immunogold localisation. Using the same technique, the nitrogenase (dinitrogenase reductase) enzyme was shown to be exclusively present in the heterocysts, while Rubisco was localised primarily to the carboxy-somes, which were only detected in vegetative cells. Using an antiserum against the ammonia assimilating enzyme glutamine synthetase (GS), we could demonstrate very low levels of this enzyme, indicating repression of GS in the cyanobiont.
Similar content being viewed by others
References
Bergman B, Carpenter EJ (1991) Nitrogenase confined to randomly distributed trichomes in the marine cyanobacterium Trichodesmium thiebautii. J Phycol 27: 158–165
Bergman B, Lindblad P, Pettersson A, Renström E, Tiberg E (1985) Immunogold localization of glutamine synthetase in a nitrogenfixing cyanobacterium (Anabaena cylindrica). Planta 166: 329–334
Bergman B, Lindblad P, Rai AN (1986) Nitrogenase in free-living and symbiotic cyanobacteria: immunoelectron microscopic localization. Fedn eur microbiol Soc (FEMS) Lett 35: 75–78
Bergman B, Rai AN (1989) The Nostoc-Nephroma symbiosis: localization, distribution pattern and levels of key proteins involved in nitrogen and carbon metabolism of the cyanobiont. Physiologia P1 77: 216–224
Bergman B, Rai AN, Johansson C, Söderbäck E (1992) Cyanobacterial-plant symbioses. Symbioses 14: 61–81
Braun-Howland E, Nierzwicki-Bauer S (1990) Azolla-Anabaena symbiosis: biochemistry, physiology, ultrastructure and molecular biology. In: Rai AN (ed) CRC handbook of symbiotic cyanobacteria. CRC Press Inc., Boca Raton, Florida, pp 65–117
Carpenter EJ, Romans KM (1991) Major role of the cyanobacterium Trichodesmium in nutrient cycling in the north Atlantic Ocean. Science, NY 254: 1356–1358
Cossar JD, Rowell P, Darling AJ, Murray S, Codd GA, Stewart WDP (1985) Localization of ribulose 1,5-bisphosphate carboxylase/oxygenase in the N2-fixing cyanobacterium Anabaena cylindrica. Fedn eur microbiol Soc (FEMS) Lett 28: 65–68
Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56: 340–373
Fogg GE (1982) Marine plankton. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell Science Publications, Oxford, pp 491–513
Geitler L (1932) Cyanophyceae. In: Kolkwitz R (ed) Rabenhorst's Kryptogamenflora von Deutschland, Österreich und der Schweiz, Vol. 14. Akademische Verlagsgesellschaft, Leipzig, Germany
Janson S, Carpenter EJ, Bergman B (1994a) Fine structure and localisation of proteins in Aphanizomenon sp. from the Baltic Sea. Eur Phycol 29: 203–211
Janson S, Carpenter EJ, Bergman B (1994b) Compartmentalisation of nitrogenase in a non-heterocystous cyanobacterium: Trichodesmium contortum. Fedn eur microbiol Soc (FeMS) Lett 118: 9–14
Janson S, Rai AN, Bergman B (1993) The marine lichen Lichina confinis (O.F.Müll.) C.Ag.: ultrastructure and localization of nitrogenase, glutamine synthetase, phycoerythrin and ribulose 1,5-bisphosphate carboxylase/oxygenase in the cyanobiont. New Phytol 124: 149–160
Mague TH, Mague FC, Holm-Hansen O (1977) Physiology and chemical composition of nitrogen-fixing phytoplankton in the central North Pacific Ocean. Mar Biol 41: 213–227
Martinez L, Silver MW, King JM, Alldredge AL (1983) Nitrogen fixation by floating diatom mats: a source of new nitrogen to oligotrophic ocean waters. Science, NY 221: 152–154
Meeks JC (1990) Cyanobacterial-bryophyte associations. In: Rai AN (ed) CRC handbook of symbiotic cyanobacteria. CRC Press Inc., Boca Raton, Florida, pp 43–63
Orr J, Haselkorn R (1982) Regulation of glutamine synthetase activity and synthesis in free-living and symbiotic Anabaena spp. J Bact 152: 626–635
Peterson RB, Dolan E, Calvert HE, Ke B (1981) Energy transfer from phycobiliproteins to photosystem I in vegetative cells and heterocysts of Anabaena variabilis. Biochim biophys Acta 634: 237–248
Peveling E (1973) Vesicles in the phycobiont sheath as possible transfer structures between the symbionts in the lichen Lichina pygmaea New Phytol 72: 343–347
Rai AN (1990a) Cyanobacteria in symbioses. In: Rai AN (ed) CRC handbook of symbiotic cyanobacteria. CRC Press Inc, Boca Raton, Florida, pp 1–7
Rai AN (1990b) Cyanobacterial-fungal symbiosis. In: Rai AN (ed) CRC handbook of symbiotic cyanobacteria. CRC Press Inc., Boca Raton, Florida, pp 9–41
Rai AN, Borthakur M, Singh S, Bergman B (1989) Anthoceros-Nostoc symbiosis: immuno electronmicroscopic localization of nitrogenase, glutamine synthetase, phycoerythrin and ribulose-1,5-bisphosphate carboxylase/oxygenase in the cyanobiont and the cultured (free-living) isolate Nostoc 7801. J gen Microbiol 135: 385–395
Söderbäck E, Bergman B (1991) The Nostoc-Gunnera magellanica symbiosis: phycobiliproteins, carboxysomes and Rubisco in the cyanobiont. Physiologia P 84: 425–432
Söderbäck E, Lindblad P, Bergman B (1990) Developmental patterns related to nitrogen fixation in the Nostoc-Gunnera magellanica Lam. symbiosis. Planta 182: 355–362
Stewart WDP (1980) Some aspects of structure and function in N2-fixing cyanobacteria. A Rev Microbiol 34: 497–536
Sundström BG (1984) Observations on Rhizosolenia clevei Ostenfeld (Bacillariophyceae) and Richelia intracellularis Schmidt (Cyanophyceae). Botanica mar 27: 345–355
Sundström BG (1986) The marine diatom genus Rhizosolenia. A new approach to the taxonomy. Ph D. Thesis, University of Lund, Lund
Taylor FJR (1982) Symbioses in marine microplankton. Annls Inst océanogr, Paris 58 (Suppl): 61–90
Venrick EL (1974) The distribution and significance of Richelia intracellularis Schmidt in the North Pacific Central Gyre. Limnol Oceanogr 19: 437–445
Villareal TA (1990) Laboratory culture and preliminary characterization of the nitrogen-fixing Rhizosolenia-Richelia symbiosis. Mar Ecol, Naples 11: 117–132
Weare NM, Azam F, Mague TH, Holm-Hansen O (1974) Microautoradiographic studies of the marine phycobionts Rhizosolenia and Richelia. J Phycol 10: 369–371
Whitton BA (1987) The biology of Rivulaiaceae. In: Fay P, van Baalen C (eds) The cyanobacteria. Elsevier Science Publishers, Amsterdam, pp 513–534
Yamanaka G, Glazer AN (1983) Phycobiliproteins in Anabaena 7119 heterocysts. In: Papageorgiou GC, Packer L (eds) Photosynthetic prokaryotes: cell differentiation and function Elsevier Science Publishers, Amsterdam, pp 69–90
Author information
Authors and Affiliations
Additional information
Communicated by T.M. Fenchel, Helsingør
Rights and permissions
About this article
Cite this article
Jahson, S., Rai, A.N. & Bergman, B. Intracellular cyanobiont Richelia intracellularis: ultrastructure and immuno-localisation of phycoerythrin, nitrogenase, Rubisco and glutamine synthetase. Marine Biology 124, 1–8 (1995). https://doi.org/10.1007/BF00349140
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00349140