Skip to main content
Log in

Photosynthetic characteristics of Prochloron sp./ascidian symbioses

I. Light and temperature responses of the algal symbiont of Lissoclinum patella

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The prokaryotic green alga Prochloron sp. (Prochlorophyta) is found in symbiotic association with colonial didemnid ascidians that inhabit warm tropical waters in a broad range of light environments. We sought to determine the light-adaptation features of this alga in relation to the natural light environments in which the symbioses are found, and to characterize the temperature sensitivity of photosynthesis and respiration of Prochloron sp. in order to assess its physiological role in the productivity and distribution of the symbiosis. Colonies of the host ascidian Lissoclinum patella were collected from exposed and shaded habitats in a shallow lagoon in Palau, West Caroline Islands, during February and March, 1983. Some colonies from the two light habitats were maintained under conditions of high light (2 200 μE m−2 s−1) and low light (400 μE m−2 s−1) in running seawater tanks. The environments were characterized in terms of daily light quantum fluxes, daily periods of light-saturated photosynthesis (Hsat), and photon flux density levels. Prochloron sp. cells were isolated from the hosts and examined for their photosynthesis vs irradiance relationships, respiration, pigment content and photosynthetic unit features. In addition, daily P:R ratios, photosynthetic quotients, carbon balances and photosynthetic carbon release were also characterized. It was found that Prochloron sp. cells from low-light colonies possessed lower chlorophyll a/b ratios, larger photosynthetic units sizes based on both reaction I and reaction II, similar numbers of reaction center I and reaction center II per cell, lower respiration levels, and lower Pmax values than cells from high-light colonies. Cells isolated from low-light colonies showed photoinhibition of Pmax at photon flux densities above 800 μE m−2 s−1. However, because the host tissue attenuates about 60 to 80% of the incident irradiance, it is unlikely that these cells are normally photoinhibited in hospite. Collectively, the light-adaptation features of Prochloron sp. were more similar to those of eukaryotic algae and vascular plant chloroplasts than to those of cyanobacteria, and the responses were more sensitive to the daily flux of photosynthetic quantum than to photon flux density per se. Calculation of daily minimum carbon balances indicated that, though high-light cells had daily P:R ratios of 1.0 compared to 4.6 for low-light cells, the cells from the two different light environments showed nearly identical daily carbon gains. Cells isolated from high-light colonies released between 15 and 20% of their photosynthetically-fixed carbon, levels sufficient to be important in the nutrition of the host. Q10 responses of photosynthesis and respiration in Prochloron sp. cells exposed briefly (15–45 min) to temperatures between 15° and 45°C revealed a discontinuity in the photosynthetic response at the ambient growth temperatures. The photosynthetic rates were found to be more than twice as sensitive to temperatures below ambient (Q10=3.47) than to temperatures above ambient (Q10=1.47). The Q10 for respiration was constant (Q10=1.66) over the temperature range examined. It appears that the photosynthetic temperature sensitivity of Prochloron sp. may restrict its distribution to warmer tropical waters. The ecological implications of these findings are discussed in relation to published data on other symbiotic systems and free-living algae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature cited

  • Akazawa, T., E. H. Newcomb and C. B. Osmond: Pathway and products of CO2-fixation by green prokaryotic algae in the cloacal cavity of Diplosoma virens. Mar. Biol. 47, 325–330 (1978)

    Google Scholar 

  • Alberte, R. S., P. R. McClure and J. P. Thornber: Photosynthesis in trees: organization of chlorophyll and phytosynthetic unit sizes in isolated gymnosperm chloroplasts. Plant Physiol. 59, 351–353 (1976)

    Google Scholar 

  • Alberte, R. S., A. M. Wood, T. A. Kursar and R. R. L. Guillard: Novel phycoerythrins in marine Synechococcus spp.: characterization, and evolutionary and ecological implications. Plant Physiol. 75, 732–739 (1984)

    Google Scholar 

  • Arnon, D. I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24, 1–15 (1949)

    Google Scholar 

  • Barlow, R. G. and R. S. Alberte: Photosynthetic characteristics of phycoerythrin-containing marine Synechococcus spp. I. Response to growth photon flux density. Mar. Biol. 86, 63–74 (1985)

    Google Scholar 

  • Brown, J. A., R. S. Alberte and J. P. Thornber: Comparative studies on the occurrence and spectral composition of chlorophyll-protein complexes in a wide variety of plant material, pp 1951–1962. Ed. by M. Avron. In: 3rd Int. Congr. Photosyn. Rehovot: Elsevier 1974

    Google Scholar 

  • Bunce, J. A., D. T. Patterson, M. M. Peet and R. S. Alberte: Light acclimation during and after leaf expansion in soybean. Plant Physiol. 60, 255–258 (1977)

    Google Scholar 

  • Chang, S. S., B. B. Prezelin and R. K. Trench: Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar. Biol. 76, 219–229 (1983)

    Article  Google Scholar 

  • Critchley, C. and T. J. Andrews: Photosynthesis and plasmamembrane permeability properties of Prochloron. Arch. Microbiol. 138, 247–250 (1984)

    Google Scholar 

  • Dennison, W. C. and R. S. Alberte: Photosynthetic responses of Zostera marina L. (eelgras) to in situ manipulations of light intensity. Oecologia, Berl. 55, 137–144 (1982)

    Google Scholar 

  • Dennison, W. C. and R. S. Alberte: Role of daily light period in the depth distribution of Zostera marina (eelgrass). Mar. Ecol. Prog. Ser. 25, 51–61 (1985)

    Google Scholar 

  • Dustan, P.: Depth-dependent photoadaptation by zooxanthellae of the reef coral Montastrea annularis. Mar. Biol. 68, 253–264 (1982)

    Google Scholar 

  • Falkowski, P. G. and Z. Dubinsky: Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature, Lond. 289, 172–174 (1981)

    Google Scholar 

  • Falkowski, P. G. and T. G. Owens: Light-shade adaptation: two strategies in marine phytoplankton. Plant Physiol. 66, 632–635 (1981)

    Google Scholar 

  • Falkowski, P. G., T. G. Owens, A. C. Ley and D. C. Mauzerall: Effects of growth irradiance levels on the ratio of reaction centers in two species of marine phytoplankton. Plant Physiol. 68, 969–973 (1981)

    Google Scholar 

  • Fisher, C. R. and R. K. Trench: In vitro carbon fixation by Prochloron sp. isolated from Diplosoma virens. Biol. Bull. mar. biol. Lab., Woods Hole 159, 636–648 (1980)

    Google Scholar 

  • Gallagher, J. C. and R. S. Alberte: Photosynthetic and cellular photoadaptive characteristics of three ecotypes of the marine diatom, Skeletonema costatum. J. exp. Mar. Biol. Ecol. (In press)

  • Gallagher, J. C., A. M. Wood and R. S. Alberte: Ecotypic differentiation in the marine diatom Skeletonema costatum: influence of light intensity on the photosynthetic apparatus. Mar. Biol. 82, 121–134 (1984)

    Google Scholar 

  • Griffiths, D. J. and L. Thinh: Transfer of photosynthetically fixed carbon between the prokaryotic green alga Prochloron and its ascidian host. Aust. J. mar. freshwat. Res. 34, 431–440 (1983)

    Google Scholar 

  • Kawamura, M., M. Murata and Y. Fujita: Quantitative relationships of the two reaction centers in the photosystem of blue-green algae. Plant Cell Physiol. 20, 697–705 (1979)

    Google Scholar 

  • Kirchman, D. L., L. Mazzella, R. S. Alberte and R. Mitchell: Bacterial epiphyte production on Zostera marina L. Mar. Ecol. Prog. Ser. 15, 207–211 (1984)

    Google Scholar 

  • Kott, P.: Algal supporting didemnid ascidians of the Great Barrier Reef, pp 616–622. In: 3rd Int. Coral Reef Symp. 1977

  • Kott, P.: Algal-bearing didemnid ascidians in the Indo-West-Pacific. Mem. Queensl. Mus. 20, 1–47 (1980)

    Google Scholar 

  • Kremer, B. P., R. Pardy and R. A. Lewin: Carbon fixation and photosynthates of Prochloron, a green alga symbiotic with an ascidian, Lissoclinum patella. Phycologia 21, 258–263 (1982)

    Google Scholar 

  • Kursar, T. A. and R. S. Alberte: Photosynthetic unit organisation in a red alga. Relationships between light harvesting pigments and reaction centers. Plant Physiol. 72, 409–414 (1983)

    Google Scholar 

  • Lee, M. J., R. Ellis and J. J. Lee: A comparative study of photoadaptation in four diatoms isolated as endosymbionts from larger foraminifera. Mar. Biol. 68, 193–197 (1982)

    Google Scholar 

  • Lewin, R. A.: A marine Synechocystis (Cyanophyta, Chlorococcales) epizoic on ascidians. Phycologia 14, 153–160 (1975)

    Google Scholar 

  • Lewin, R. A.: Prochloron, type genus of the Prochlorophyta. Phycologia 16, 217 (1977)

    Google Scholar 

  • Lewin, R. A.: The prochlorophytes, Ch. 13, pp 257–266. In: The prokaryotes. Ed. by M. P. Starr et al. Berlin: Springer-Verlag 1981

    Google Scholar 

  • Lewin, R. A.: Prochloron — a status report. Phycologia 23, 203–208 (1984)

    PubMed  Google Scholar 

  • Lewin, R. A. and L. Cheng: Associations of microscopic algae with didemnid ascidians. Phycologia 14, 149–152 (1975)

    Google Scholar 

  • Lewin, R. A., L. Cheng and R. S. Alberte: Prochloron-ascidian symbioses: photosynthetic potential and productivity. Micronesica 19, 165–170 (1983)

    Google Scholar 

  • Mazzella, L., D. Mauzerall, H. Lyman and R. S. Alberte: Protoplast isolation and photosynthetic characteristics of Zostera marina L. (eelgrass). Bot. mar. 24, 285–290 (1981)

    Google Scholar 

  • McCourt, R. M., A. F. Michaels and R. W. Hoshaw: Seasonality of symbiotic Prochloron (Prochlorophyta) and its didemnid host in the northern Gulf of California. Phycologia 23, 95–101 (1984)

    Google Scholar 

  • Muller-Parker, G.: Photosynthesis-irradiance responses and photosynthetic periodicity in the sea anemone Aiptasia pulchella and its zooxanthellae. Mar. Biol. 82, 225–232 (1984)

    Google Scholar 

  • Muscatine, L.: Productivity of zooxanthellae, pp 403–410. In: Primary productivity in the sea. Ed. by P. G. Falkowski. New York: Plenum Press 1980

    Google Scholar 

  • Myers, J., J.-R. Graham and R. T. Wang: Light harvesting in Anacystis nidulans studied in pigment mutants. Plant Physiol. 66, 1144–1149 (1980)

    Google Scholar 

  • Newcomb, E. H. and T. D. Pugh: Blue-green algae associated with ascidians of the Great Barrier Reef. Nature, Lond. 253, 533–534 (1975)

    Google Scholar 

  • Nolan, W. G. and R. M. Smilie: Multi-temperature effects on Hill reaction activity of barley chloroplasts. Biochim. biophys. Acta 440, 461–475 (1976)

    PubMed  Google Scholar 

  • Paerl, H.: N2 fixation (nitrogenase activity) attributable to a specific Prochloron (prochlorophyta)-ascidian association in Palau, W. Micronesia. Mar. Biol. 84, 251–254 (1984)

    Google Scholar 

  • Paerl, H., R. A. Lewin and L. Cheng: Chlorophyll and carotenoid pigments of Prochloron (Prochlorophyta). Bot. mar. 27, 257–264 (1984)

    Google Scholar 

  • Parsons, T. R., M. Takahashi and B. Hargrave: Biological oceanographic processes, 330 pp. 3rd ed. New York: Pergamon Press 1984

    Google Scholar 

  • Patterson, D. T.: Light and temperature adaptation, pp 205–235. In: Predicting photosynthesis for ecosystems models. Ed. by J. D. Hesketh and J. W. Jones. Boca Raton, Fl: CRC Press 1980

    Google Scholar 

  • Perry, M. J., M. C. Talbot and R. S. Alberte: Photoadaptation in marine phytoplankton: response of the photosynthetic unit. Mar. Biol. 62, 91–101 (1981)

    Google Scholar 

  • Rasion, J. K.: A biochemical explanation of low-temperature stress in tropical and subtropical plants. In: Mechanisms of regulation of plant growth. Ed. by R. L. Bieleski, A. R. Gerguson and M. N. Cresswell, R. Soc. N. Zeal. Bull. 12, 487–497 (1974)

  • Rasion, J. K. and J. A. Berry: Responses of macrophytes to temperature. Encycl. Plant Physiol., new series 12A, 277–338 (1979)

    Google Scholar 

  • Richardson, K., J. Beardall and J. A. Raven: Adaptation of unicellular algae to irradiance; an analysis of strategies. New Phytol. 93, 157–191 (1983)

    Google Scholar 

  • Ryland, J. S., R. A. Wigley and A. Muirhead: Ecology and colonial dynamics of some Pacific reef Didemnidae (Ascidiacea). Zool. J. Linn. Soc 80, 261–282 (1984)

    Google Scholar 

  • Stackebrandt, E., E. Seewaldt, V. J. Fowler and K.-H. Scheifer: The relatedness of Prochloron sp. isolated from different didemnid ascidian hosts. Arch. Microbiol. 132, 216–217 (1982)

    Google Scholar 

  • Schuster, G., G. C. Owens, Y. Cohen and I. Ohad: Thylakoid polypeptide composition and light-dependent phosphorylation of the chlorophyll a,b-protein in Prochloron, a prokaryote exhibiting oxygenic photosynthesis. Biochim. biophys. Acta 767, 596–605 (1984)

    Google Scholar 

  • Terri, J. A., D. T. Patterson, R. S. Alberte and R. M. Castelberry: Changes in the photosynthetic apparatus of maize in response to simulated natural temperature fluctuations. Plant Physiol. 60, 255–258 (1977)

    Google Scholar 

  • Thinh, L.-V. and D. J. Griffiths: Studies on the relationships between the ascidian Diplosoma virens and its associated microscopic algae. I. Photosynthetic characteristics of the algae. Aust. J. mar. freshwat. Res. 28, 673–681 (1977)

    Google Scholar 

  • Trench, R. K.: The cell biology of plant-animal symbiosis. Ann. Rev. Plant Physiol. 30, 485–532 (1979)

    Article  Google Scholar 

  • Van Valen, L.: Phylogenies in molecular evolution: Prochloron. Nature, Lond. 298, 493–494 (1980)

    Google Scholar 

  • Vierling, E. and R. S. Alberte: Functional organization and plasticity of the photosynthetic unit of the cyanobacterium Anacystis nidulans. Physiologia Plant. 50, 93–98 (1980)

    Google Scholar 

  • Withers, N. W., R. S. Alberte, R. A. Lewin, J. P. Thornber, G. Britton and T. W. Goodwin: Carotenoids, chlorophyll-protein composition, and photosynthetic unit size of Prochloron sp., a prokaryotic green alga. Proc. natl Acad. Sci. USA 75, 2301–2305 (1978)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by R. W. Doyle, Halifax

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alberte, R.S., Cheng, L. & Lewin, R.A. Photosynthetic characteristics of Prochloron sp./ascidian symbioses. Mar. Biol. 90, 575–587 (1986). https://doi.org/10.1007/BF00409278

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00409278

Keywords

Navigation