Of Pyrenomonas Salina (Cryptophyceae)
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MARINE ECOLOGY PROGRESS SERIES Vol. 61: 171-181, 1990 Published March 8 Mar. Ecol. Prog. Ser. Relative effects of nitrogen or phosphorus depletion and light intensity on the pigmentation, chemical composition, and volume of Pyrenomonas salina (Cryptophyceae) Alan J. Lewitus, David A. Caron Biology Department, Woods Hole Oceanographic Institution. Woods Hole, Massachusetts 02543, USA ABSTRACT: The nitrogen-rich phycobiliproteins are efficient light-harvesting pigments of crypto- phytes, cyanobacteria, and rhodophytes. Whereas it is well established that certain cyanobacteria mobilize their phycobiliproteins in response to nitrogen deprivation, the effect of nitrogen stress on cryptophyte physiology has been studied only rarely. We compared the effects of nitrogen and phosphorus depletion on the biovolume, chemical composition, and pigment composition of the marine cryptophyte Pyrenomonas salina, grown in batch cultures under light-limiting and light-saturating conditions. Cellular phycoerythrin content declined during the late exponential growth phase in nitrogen-depleted cultures, and the cells were nearly devoid of phycoerythrin (< 3 % of the phyco- erythrin content of nitrogen-replete cells) at the beginning of stationary growth. Phycoerythrin content also decreased during late exponential phase in phosphorus-depleted cultures, but these latter cells contained more than 10 times the phycoerythrin concentration of nitrogen-depleted cells at the same growth stage. Chlorophyll a content declined in nitrogen-depleted cultures, but at a slower rate than the decrease in phycoerythrin, such that the phycoerythrin to chlorophyll a ratio decreased by more than 95 O/O from the early exponential to early stationary growth phase. In nitrogen-depleted cultures grown at a low light intensity, the decline in phycoerythrin content preceded the decline in chlorophyll a content, and resulted in only slight changes in cellular nitrogen content and biovolume. These data indicate that phycoerythrin is preferentially lost from P. salina during nitrogen deficiency, and support the hypothesis that, similar to certain cyanobacteria, P. salina responds to nitrogen deprivation by mobilizing phycoerythrin in order to help sustain cellular nitrogen requirements. INTRODUCTION phycobiliproteins within the thylakoid lumen. Cryp- tophytes also differ from cyanobacteria and rhodo- Phycobiliproteins are the major light-harvesting pig- phytes in containing 2 light-harvesting pigment com- ments in cyanobacteria, rhodophytes, and crypto- plexes, the phycobiliprotein-associated protein com- phytes. Cryptophyte phycobiliproteins are immuno- plex and a chlorophyll a/c protein complex. The latter chemically related to cyanobacteria and rhodophyte is integrally bound to the thylakoid membrane, and phycobiliproteins (MacColl et al. 1976, Guard-Friar et transfers energy to either photosystem (Lichtle et al. al. 1986), suggesting a common evolutionary ancestry 1980). to the 3 pigment groups. However, the phylogenetic Cryptophytes resemble cyanobacteria and rhodo- status of cryptophyte phycobiliproteins is complicated phytes, however, in that Photosystem I1 receives excita- by their distinct physical properties and molecular tion energy primarily through the phycobiliprotein structures (Glazer 1981), and especially by the unique light-harvesting protein complex (reviewed in Larkum way in which they are organized within the chloroplast & Barrett 1983, MacColl & Guard-Friar 1987), and this (Gantt 1979). Whereas the phycobiliproteins of cyano- energy transfer is highly efficient (Haxo & Fork 1959, bacteria and rhodophytes are organized within discrete Holzwarth et al. 1983, Hanzlik et al. 1985, Bruce et al. phycobilisomes located on the outer thylakoid mem- 1986). Efficient energy transfer in cyanobacteria and brane, cryptophytes lack phycobilisomes, and contain rhodophytes can be partly explained by the highly O Inter-Research/Printed in F R. Germany 172 Mar Ecol. Prog. Ser. 61: 171-181, 1990 ordered juxtapositioning of antenna pigments within Analogous information on the effects of nitrogen the phycobilisome and the close spectral overlap availability on the pigment concentration of crypto- between phycoerythrin, phycocyanin, al.lophycocya- phytes is rare, and the relative importance of light nin, and chlorophyll a (reviewed in Scheer 1981). Effi- intensity and nutrient status to cryptophyte pigment cient energy transfer to Photosystem I1 is not as production is unclear. Results from 2 studies indicate thoroughly understood in cryptophytes, where phy- that phycobiliproteins may be selectively lost during cobiliprotein complexes are seemingly less efficiently nitrogen-deficient conditions in cryptophytes. Lichtl6 organized, allophycocyanin is absent, and phycoery- (1979) compared the pigment content and chloroplast thrin and phycocyanin have never been demonstrated ultrastructure of nitrogen-replete Cryptomonas rufes- in the same organism (reviewed in Gantt 1979). How- cens cultures grown at a relatively high light intensity, ever, the presence of multiple forms of phycoerythrin or nitrogen-replete cultures grown at a relatively low light phycocyanin within a species (Hiller & Martin 1987 and intensity, and nitrogen-deficient cultures grown at a references therein), and the organization of phycobili- relatively low light intensity. Cells from the nitrogen- proteins into discrete units closely associated with the replete cultures grown at the low light intensity and thylakoid membrane (Lichtle et al. 1987, Ludwig & sampled during the exponential growth phase con- Gibbs 1989) may partly account for efficient energy tained higher concentrations of all photosynthetic pig- conversion in cryptophytes. Clearly, cryptophytes have ments and a greater proportion of phycoerythrin to total evolved a unique system for harvesting light, com- chlorophyll than cells from the nitrogen-deficient bining strategies of other phycobiliprotein-containing cultures grown at the low light ~ntensity.This result is organisms and chromophytes. consistent with the selective degradation of phycoery- One issue that has been extensively studied in thnn and/or inhibition of phycoerythrin production by cyanobacteria, but not cryptophytes, is the response of C. rufescens in response to nitrogen stress. Pigment the photosynthetic system to changes in nutrient status. determinations from the nitrogen-replete cultures In general, cyanobacteria react to nitrogen depletion grown at the high light intensity were made at, or just by decreasing the rate of phycobiliprotein production prior to, the stationary growth phase. Because these (reviewed in Grossman et al. 1986). Constant rates of cultures were grown in media with a dissolved nitrogen growth and chlorophyll a production were maintained to phosphorus ratio of ca 8, it is possible that the cells while phycobiliprotein content declined during the were nitrogen-deficient during this growth stage. initial stages of nitrogen depletion in cultures of Therefore, the effects of light intensity and nitrogen Cyanophora paradoxa (Schenk et al. 1987), Spirulina availability on the pigment content of C. rufescens platensis (Boussiba & Richmond 1980), Anacystis nidu- cannot be adequately distinguished based on these lans (Bayer & Schenk 1986), and Agmenellum quadru- results. plicatum (Stevens et al. 1981a). De novo synthesis of Similarly, Rhiel et al. (1985, 1986) found that nitro- phycocyanin was shown to be selectively depressed by gen-deficient Cryptomonas maculafa cells, grown nitrogen-deficient Anacystis nidulans (Lau et al. 1977). under a relatively high light intensity, contained a This is not surprising given that the light-harvesting much lower concentration of phycoerythrin, a lower machinery associated with phycobiliproteins requires proportion of phycoerythrin to chlorophyll, and fewer substantial amounts of nitrogen relative to the Photosystem I1 particles than nitrogen-sufficient cells chlorophyll/protein complexes (Raven 1984), and that grown at a lower light level. Resupplying the nitrogen- photosynthesis can function in the absence of phy- deficient cells with nitrate caused a restoration of the cobiliproteins (Lemasson et al. 1973, Arnon et al. 1974). red color characteristic of cultures growing exponen- In addition to reducing the rate of phycobiliprotein tially, but the pigment content was not quantified. production, cyanobacteria also appear to be able to Therefore, the relative importance of light intensity and degrade phycobiliproteins already present in the cell nitrogen availability on the cryptophyte photosynthetic when organisms become nitrogen-stressed (Allen & apparatus is difficult to differenhate from these results. Smith 1969, Foulds & Carr 1977. Lau et al. 1977, The effects of nutrient status (nitrogen depletion, Yamanaka & Glazer 1980). Phycobiliproteins can, phosphorus depletion) and light intensity on photo- under certain conditions, account for a significant por- synthetic pigment production in the marine cryp- tion of the cellular nitrogen content (Myers & Kratz tophyte Pyrenomonas salina were examined in this 1955, Bennett & Bogorad 1973, Kana & Glibert 1987a). study. The physiological response of P. salina to nitro- Phycobiliprotein degradation is believed to be a gen depletion resembled that of certain cyanobacteria mechanism for mobilizing nitrogen for processes in that, independent of light intensity, cellular phy- required to sustain cellular growth or metabolism du- cobiliprotein content declin.ed before cell division