Diversification of a chimaeric algal group, the chlorarachniophytes: Phylogeny of nuclear and nucleomorph small-subunit rRNA genes

Abstract

Chlorarachniophytes are a group of algae that acquired their chloroplasts by a eukaryote-eukaryote endosymbiosis (secondary endosymbiosis) between a protozoan and a green alga. The green algal endosymbiont still keeps its own nucleus as a reduced form, called a nucleomorph, that contains the smallest eukaryotic genome. We sequenced both nuclear and nucleomorph small-subunit ribosomal RNA (SSU rRNA) genes from seven chlorarachniophyte strains. In order to examine the origins of this algal group in more detail and clarify their phylogenetic relationship and morphological diversification, we performed molecular phylogenetic analyses of their nuclear and nucleomorph SSU rRNA genes with maximum-likelihood, maximum- parsimony, and neighbor-joining methods. The results show that chlorarachniophytes evolved from a single secondary endosymbiosis and suggest that the endosymbiont was an ulvophycean green alga. They also confirm that the host was related to monadofilosans (sarcomonad flagellates and euglyphid amoebae). Nuclear and nucleomorph trees are largely congruent, and both show the same five major chlorarachniophyte lineages. However, nucleotide substitution rates of nucleomorph rRNA genes were much higher than those of the nuclear genes. The four known types of pyrenoid ultrastructure map onto the molecular tree in such a way that each had only a single origin, indicating that these ultrastructural differences among the endosymbionts are reliable indicators of their phylogenetic relationship. Mapping overall cell morphology onto the tree suggests that at least four losses of the amoeboid stage of the life cycle, two losses of cell walls, and two losses of phagotrophy may have occurred independently in the evolution of the chlorarachniophytes.