Physiological studies of phototrophy and heterotrophy in two algae with contrasting nutritional characteristics, Pyrenomonas salina (Cryptophyceae) and Poterioochromonas malhamensis (Chrysophyceae)

Abstract

The ability of algae to take up dissolved organic compounds is well documented for cultured and field populations yet the physiological mechanisms controlling this behavior are largely unknown. The effects of dissolved organic compound additions on the growth and photosynthetic apparatus were examined in two nanophytoplankton with contrasting nutritional characteristics, Pyrenomonas salina (Cryptophyceae) and Poterioochromonas malhamensis (Chrysophyceae). Although both species are capable of chemoheterotrophic nutrition, great differences were found in the relative contribution of heterotrophy to their overall nutrition and the physiological response of their photosynthetic systems to changes in nutritional mode. These differences indicate that the physiological mechanisms involved in integrating autotrophic and heterotrophic nutrition and the environmental control of this integration are distinct in these species. In comparison to other facultatively heterotrophic algae, P. malhamensis is exceptional in the dominant contribution of heterotrophy to its overall nutrition. Growth could be significantly enhanced by organic substrate additions to P. malhamensis at all light intensities and the growth rate on glucose in the dark was equal to the maximum growth rate on glucose in the light. In addition, when organic substrates were available to the alga, chlorophyll a cell-1 was reduced and the extent of this reduction varied with the type of organic substrate. These results support the hypothesis that chloroplast development in P. malhamensis is catabolite-sensitive. The inhibitory effect of organic substrates on chlorophyll production by P. malhamensis was only transitory; i.e., after the initial decline in chlorophyll a cell-1, chlorophyll production increased and the organic substrate uptake rate cell-1 decreased despite the persistence of a relatively high substrate concentration in the culture medium. These results suggest that the accumulation of substance(s) excreted by P. malhamensis conditioned the culture medium and led to a relief of the inhibitory effect of organic substrates on chlorophyll production by the alga. P. salina is typical of most facultatively heterotrophic algae in culture in that phototrophic growth can be enhanced by organic enrichment only at light intensities limiting for photoautotrophic growth. Contrary to P. malhamensis, the effect of organic compounds on the growth rate of P. salina was critically light intensity-dependent under all organic substrate concentrations used in this study. In addition, whereas in P. malhamensis the addition of organic substrates repressed chloroplast development, only selected elements of the photosynthetic system were inhibited by organic substrate additions to P. salina, and the uptake rate of inorganic carbon was not affected. These results indicate that these algae have contrasting metabolic strategies for integrating autotrophic and heterotrophic nutrition for growth. When organic substrates are available to P. malhamensis, the synthesis of the photosynthetic apparatus is repressed and growth and maintenance requirements are met by the catabolism of organic substrates. In contrast, given a sufficient light supply, maximal growth rates can be obtained photoautotrophically by P. salina, but organic substrates can be used to augment the carbon, energy, and/or reductant supply when photosynthetic rates are light-limited. The physiological response of P. salina's photosynthetic system to changes in environmental conditions was further examined by testing two hypotheses. The first hypothesis was that P. salina responds to nitrogen deprivation by mobilizing phycoerythrin in order to help sustain cellular nitrogen requirements. In response to nitrogen depletion from the culture medium, the phycoerythrin content of P. salina cells decreased prior to any changes in growth rate, cell volume, or cellular concentrations of chlorophyll a, carbon, or nitrogen. These results support the hypothesis and suggest that, in addition to its light-harvesting role, phycoerythrin may serve as an important endogenous nitrogen source for this cryptophyte. The second hypothesis was that glycerol uptake selectively inhibits the synthesis of photosynthetic components involved in light-harvesting. Glycerol addition to P. salina cultures grown at a limiting light intensity reduced the cell phycoerythrin content, phycoerythrin to chlorophyll a ratio, thylakoid width, degree of thylakoid packing, number of thylakoids cell-1, and size of photosystem II complexes. These properties were reduced to a similar extent by increasing the light intensity for growth. These results strongly support the hypothesis and indicate that enhancement of heterotrophic potential occurs at the expense of light-harvesting ability in glycerol-grown P. salina.