The origin of photoactivated adenylyl cyclase (PAC), the Euglena blue-light receptor: phylogenetic analysis of orthologues of PAC subunits from several euglenoids and trypanosome-type adenylyl cyclases from Euglena gracilis

Abstract

Photoactivated adenylyl cyclase (PAC) is the blue-light receptor flavoprotein recently identified as a photoreceptor for photoavoidance of the unicellular flagellate, Euglena gracilis. To gain an insight into the evolution of this unique protein, similar sequences were searched for in several euglenoids by reverse transcriptase-polymerase chain reation (RT-PCR) using degenerate primers. Two similar transcripts were detected in each of the four phototrophic euglenoids, Euglena stellata, Colacium sideropus, Eutreptia viridis, Eutreptiella gymnastica, and in an osmotrophic (i.e., obtaining nutrients by absorption) one, Khawkinea quartana, but not in a phagotrophic euglenoid, Petalomonas cantuscygni. Each of them seemed to be orthologous to PACα and PACβ, respectively, and had the same domain structure as PAC subunits each of which is composed of two flavin binding domains, F1 and F2, each followed by an adenylyl cyclase catalytic domain, C1 and C2, respectively. This fact implies that they constitute a functional photoactivated adenylyl cyclase like PAC. Phylogenetic analysis of the adenylyl cyclase catalytic domains revealed that they belong to a bacterial cluster, not to a trypanosomal one. In addition, two trypanosome-type adenylyl cyclases were discovered in E. gracilis. In contrast to PAC, deduced amino acid sequences of the trypanosome-type adenylyl cyclases indicated that they are integral membrane proteins with a membrane spanning region at the midpoint of them, followed by an adenylyl cyclase catalytic domain which seems cytoplasmic. Overall, we propose that PAC might have been transferred to euglenoids on the occasion of secondary endosymbiosis.