The Nostoc-Gunnera magellanica symbiosis: Phycobiliproteins, carboxysomes and Rubisco in the cyanobiont

Abstract

1992. The Nostoc-Gunnera magellanica symbiosis: Phycobiliproteins, carboxysomes and Rubisco in the cyanobiont. -Physioi. Plant. 84: 425-432.In the nitrogen fixing symbiosis between Nostoc and ttie angiosperm Gunnera. the eyanobiont is found in stem glands and is thought to have a heterotropbic mode of nutrition. To investigate whether the pbotosynthetic machinery in the cyanobiont is down-regulated in the symbiosis, the presence of the pbycobiliproteins, phycoerythrin and phyeocyanin, and ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco. EC 4.1.1.39) in cyanobionts of Gunnera magellanica Lam. and in a free-hving (cultured) isolate of tbe cyaoobacterium was studied by immunoelectron microscopy. Carboxysomes were numerous in all vegetative cells (ca 3.5 per ceil section), and on an area basis they showed a iiigh Rubisco label compared to tlie cytoplasm: bot recalculation on a volume basis demonstrated tbat the carboxysomal fraction of Rubisco decreased in the cyanobiont along the plant stem. Along the whole Gunnera stem both types of pbycobiliproteins were present in the symbiotic Nostoc and in amounts equivalent to or above those detected in the free-living isolate. As the symbiotic Nostoc is located intracellularly, out of reach of light in the plant stem, the findings indicate a lack of regulation of the pholosyntbetic protein synthesis in the symbiotic state.

The Nostoc–Gunnera symbiosis

“…This is evidenced by the fact that cyanophycin granules and phycobiliproteins are present in the vegetative cells (Soderback & Bergman, 1992). The situation is similar in other symbiotic cyanobacteria (BraunHowland et al, 1988;Rai et al, 1989).…”

“…As neither of the light-harvesting pigments, phycocyanin (PC) and phycoerythrin (PE), were detected, though chlorophyll was present, it was concluded that the cyanobiont had lost the ability to synthesize photosynthetic proteins and to carry out photosynthesis (Silvester, 1976). Later this hypothesis was tested in the cyanobiont of G. magellanica (Soderback & Bergman, 1992). It was found that the cyanobiont contained both the primary COg-fixing enzyme, ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco), as well as the PC and PE proteins, and at levels comparable to those of free-living isolates (Soderback & Bergman, 1992).…”

“…Later this hypothesis was tested in the cyanobiont of G. magellanica (Soderback & Bergman, 1992). It was found that the cyanobiont contained both the primary COg-fixing enzyme, ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco), as well as the PC and PE proteins, and at levels comparable to those of free-living isolates (Soderback & Bergman, 1992). The proteins were absent from heterocysts but present in vegetative cells, from young to old glands, and were distributed in the same fashion as in free-living cyanobacteria.…”

“…The proportion of heterocysts increases gradually, and influences the function of Nostoc drastically (Silvester, 1976;Soderback et al, 1990). The volume of the Nostoc cells also increases several fold (Soderback & Bergman, 1992) while the growth rate is retarded (Soderback et al, 1990). Another impact is the formation of peculiarly shaped, probably degenerate, Nostoc cells in older Gunnera glands (Silvester, 1976;Soderback et al, 1990).…”

Regulation of Cellular Differentiation in Filamentous Cyanobacteria in Free-Living and Plant-Associated Symbiotic Growth States

“…Nostoc cultures freshly separated from Anthoceros have only 12% of the in vitro Rubisco activity of corresponding free-living cultures, similar to the in vivo rate of symbiotic light-dependent CO 2 assimilation (176). In contrast, the in vitro Rubisco activities in Nostoc from both the cycad (107) and Gunnera (173) associations are equivalent to those in free-living cultures. It may be that the low rate of in vivo CO 2 fixation by Nostoc in association with cycads or Gunnera is attributable to a reversible inhibitor of Rubisco, which is lost by dilution in the in vitro assay.…”