The Phylogenetic Position of Red Algae Revealed by Multiple Nuclear Genes from Mitochondria-Containing Eukaryotes and an Alternative Hypothesis on the Origin of Plastids

Abstract

Red algae are one of the main photosynthetic eukaryotic lineages and are characterized by primitive features, such as a lack of flagella and the presence of phycobiliproteins in the chloroplast. Recent molecular phylogenetic studies using nuclear gene sequences suggest two conflicting hypotheses (monophyly versus non-monophyly) regarding the relationships between red algae and green plants. Although kingdom-level phylogenetic analyses using multiple nuclear genes from a wide-range of eukaryotic lineages were very recently carried out, they used highly divergent gene sequences of the cryptomonad nucleomorph (as the red algal taxon) or incomplete red algal gene sequences. In addition, previous eukaryotic phylogenies based on nuclear genes generally included very distant archaebacterial sequences (designated as the outgroup) and/or amitochondrial organisms, which may carry unusual gene substitutions due to parasitism or the absence of mitochondria. Here, we carried out phylogenetic analyses of various lineages of mitochondria-containing eukaryotic organisms using nuclear multigene sequences, including the complete sequences from the primitive red alga Cyanidioschyzon merolae. Amino acid sequence data for two concatenated paralogous genes (alpha- and beta-tubulin) from mitochondria-containing organisms robustly resolved the basal position of the cellular slime molds, which were designated as the outgroup in our phylogenetic analyses. Phylogenetic analyses of 53 operational taxonomic units (OTUs) based on a 1525-amino-acid sequence of four concatenated nuclear genes (actin, elongation factor-1alpha, alpha-tubulin, and beta-tubulin) reliably resolved the phylogeny only in the maximum parsimonious (MP) analysis, which indicated the presence of two large robust monophyletic groups (Groups A and B) and the basal eukaryotic lineages (red algae, true slime molds, and amoebae). Group A corresponded to the Opisthokonta (Metazoa and Fungi), whereas Group B included various primary and secondary plastid-containing lineages (green plants, glaucophytes, euglenoids, heterokonts, and apicomplexans), Ciliophora, Kinetoplastida, and Heterolobosea. The red algae represented the sister lineage to Group B. Using 34 OTUs for which essentially the entire amino acid sequences of the four genes are known, MP, distance, quartet puzzling, and two types of maximum likelihood (ML) calculations all robustly resolved the monophyly of Group B, as well as the basal position of red algae within eukaryotic organisms. In addition, phylogenetic analyses of a concatenated 4639-amino-acid sequence for 12 nuclear genes (excluding the EF-2 gene) of 12 mitochondria-containing OTUs (including C. merolae) resolved a robust non-sister relationship between green plants and red algae within a robust monophyletic group composed of red algae and the eukaryotic organisms belonging to Group B. A new scenario for the origin and evolution of plastids is suggested, based on the basal phylogenetic position of the red algae within the large clade (Group B plus red algae)...

Monophyly of Archaeplastida supergroup and relationships among its lineages in the light of phylogenetic and phylogenomic studies. Are we close to a consensus?

“…In addition, other representatives of the main eukaryotic supergroups, such as Excavata and SAR, grouped with the Archaeplastida with high support in other phylogenetic analyses [29,31,64,68,74,76,82,83]. Such relationships were also inferred from many other data sets but with weaker or no support (Tab.…”

“…Three scenarios have been proposed (Fig. 1) that are compatible with the unquestionable monophyly of plastid genes, and explain both similar and different plastid features of Archaeplastida members (for wide discussion see [27][28][29][30][31][32][33]41,83,121,122]). One of them assumes that multiple independent primary endosymbioses occurred involving closely related cyanobacteria and separate Archaeplastida lineages.…”

Phototaxis in the Unicellular Red Algae Cyanidioschyzon merolae and Cyanidium caldarium

“…It is possible therefore that C. merolae might use a non-conventional system for movement. Elucidating the molecular mechanism of phototaxis and gravitaxis in C. merolae using genomic information (Ohta et al 1998, Matsuzaki et al 2004, Nozaki et al 2007) and genetic techniques , Ohnuma et al 2008, 2009, Imamura et al 2009 would inform future studies of the phototaxic and gravitaxtic mechanism in primitive algae.…”

Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D

“…merolae has noteworthy properties, which are relevant for examining the origin of eukaryotes, and primary and secondary plastid endosymbiosis 20 . Only 30 transfer RNAs (tRNAs) were detected in the nuclear genome using the program tRNAscan-SE with relaxed parameter settings (Fig.…”