Diversification of light capture ability was accompanied by the evolution of phycobiliproteins in cryptophyte algae

Abstract

Evolutionary biologists have long sought to identify phenotypic traits whose evolution enhances an organism's performance in its environment. Diversification of traits related to resource acquisition can occur owing to spatial or temporal resource heterogeneity. We examined the ability to capture light in the Cryptophyta, a phylum of single-celled eukaryotic algae with diverse photosynthetic pigments, to better understand how acquisition of an abiotic resource may be associated with diversification. Cryptophytes originated through secondary endosymbiosis between an unknown eukaryotic host and a red algal symbiont. This merger resulted in distinctive pigment-protein complexes, the cryptophyte phycobiliproteins, which are the products of genes from both ancestors. These novel complexes may have facilitated diversification across environments where the spectrum of light available for photosynthesis varies widely. We measured light capture and pigments under controlled conditions in a phenotypically and phylogenetically diverse collection of cryptophytes. Using phylogenetic comparative methods, we found that phycobiliprotein characteristics were evolutionarily associated with diversification of light capture in cryptophytes, while non-phycobiliprotein pigments were not. Furthermore, phycobiliproteins were evolutionarily labile with repeated transitions and reversals. Thus, the endosymbiotic origin of cryptophyte phycobiliproteins provided an evolutionary spark that drove diversification of light capture, the resource that is the foundation of photosynthesis.

Keywords: photosynthesis; photosynthetically usable radiation; phycobilin; resource acquisition.

Figure 1.

Discrete character ancestral state estimates of phycobiliprotein maximum absorption peak wavelength mapped onto the rbcL phylogeny. Node labels indicate the posterior probability (PP) of each ancestral state. The size of the pie graphs are for better visualization towards the root of the phylogeny and are not indicative of PP values. Tip labels denote each species' state. Phylogenetic clade designations are derived from the rbcL maximum-likelihood bootstrap support values (see the electronic supplementary material, figure S1). Colours do not indicate the actual qualitative colours of the cultures. Wavelengths for each class are in nanometres (nm). Cr, cryptophytes; PE, phycoerythrin; PC, phycocyanin.

Figure 2.

Log₁₀-transformed data are plotted with a trend line indicating the relationships between photosynthetically usable radiant energy (PUR) and phycobiliprotein concentration per cell (a), PUR and phycobiliprotein maximum absorption peak wavelength (b), and PUR and the additive value of the concentrations per cell of the non-phycobiliprotein pigments (c; alloxanthin, α-carotene, chlorophyll a and chlorophyll c₂). (Online version in colour.)