The evolution of photosynthesis in chromist algae through serial endosymbioses

Abstract

Chromist algae include diverse photosynthetic organisms of great ecological and social importance. Despite vigorous research efforts, a clear understanding of how various chromists acquired photosynthetic organelles has been complicated by conflicting phylogenetic results, along with an undetermined number and pattern of endosymbioses, and the horizontal movement of genes that accompany them. We apply novel statistical approaches to assess impacts of endosymbiotic gene transfer on three principal chromist groups at the heart of long-standing controversies. Our results provide robust support for acquisitions of photosynthesis through serial endosymbioses, beginning with the adoption of a red alga by cryptophytes, then a cryptophyte by the ancestor of ochrophytes, and finally an ochrophyte by the ancestor of haptophytes. Resolution of how chromist algae are related through endosymbioses provides a framework for unravelling the further reticulate history of red algal-derived plastids, and for clarifying evolutionary processes that gave rise to eukaryotic photosynthetic diversity.

Figure 1. Evidence of EGT from regression analyses with significant outliers.

Linear regressions on relationships between the number of most similar sequences (measured as top BLAST matches) from 13 other eukaryotic lineages to all inferred protein-encoding genes in haptophyte (solid line, black triangles) and cryptophyte (dashed line, grey circles) genomes. The largest outliers are highlighted with studentized residuals (residual divided by its standard deviation; ‘s.d.’ on figure) and images of the taxa that share more genes than expected based on the model, heterokonts in both cases. For comparison, the data points that indicate measures of similarity between cryptophytes and haptophytes genome also are highlighted. No studentized residual is provided for the data point indicating the number of top BLAST hits to haptophytes using the cryptophyte genome as query, because it falls at the predicted value from the regression line. Arrows indicate the proposed direction of EGT based on our overall model, except for the double-pointed arrow (the X indicating no evidence of EGT in either direction), which shows the reciprocal results between haptophytes and cryptophytes. A query’s matches to its own group (for example, haptophyte to haptophyte) are not counted, meaning these reciprocal data points are both unpaired on the figure.

Figure 2. Model of serial plastid endosymbioses and a test using genes from plastid genomes.

(a) Model of serial plastid endosymbioses suggested by regression analyses. The relationships depicted agree with general inferences from eukaryotic phylogenomics that heterokonts are not closely related to cryptophytes or haptophytes, and that each of the three groups emerge from mutually exclusive clades containing heterotrophic relatives. With respect to our proposed model of serial endosymbioses, the specific topology of the tree is not important, only that the three chromist algal groups do not form an exclusively monophyletic grouping that excludes aplastidial heterokonts. (b) Tree of plastid relationships based on an alignment of 5,818 amino-acid positions from genes inherited directly through the plastid genome, an independent data set for testing the model of plastid transfer inferred from EGT. The tree shown was recovered using both Bayesian and maximum-likelihood (ML) approaches. Bayesian posterior probabilities and ML bootstrap support values are provided for each node, with a star indicating 1.0 and 100% support, respectively. A second bootstrap value on nodes in the red plastid clade is from ML analyses performed in the absence of the green plastid lineage as outgroup. Bayesian probabilities are based on 5,000 sampled trees and bootstrap support values are from 1,000 replicates in each case.