Evolutionary transfer of ORF-containing group I introns between different subcellular compartments (chloroplast and mitochondrion)

We describe here a case of homologous introns containing homologous openreading frames (ORFs) that are inserted at the same site in the largesubunit (LSU) rRNA gene of different organelles in distantly relatedorganisms. We show that the chloroplast LSU rRNA gene of the green algaChlamydomonas pallidostigmatica contains a group I intron (CpLSU.2)encoding a site-specific endonuclease (I-CpaI). This intron is inserted atthe identical site (corresponding to position 1931-1932 of the Escherichiacoli 23S rRNA sequence) as a group I intron (AcLSU.m1) in the mitochondrialLSU rRNA gene of the amoeboid protozoon Acanthamoeba castellanii. TheCpLSU.2 intron displays a remarkable degree of nucleotide similarity inboth primary sequence and secondary structure to the AcLSU.m1 intron;moreover, the Acanthamoeba intron contains an ORF in the same locationwithin its secondary structure as the CpLSU.2 ORF and shares with it astrikingly high level of amino acid similarity (65%; 42% identity). Acomprehensive survey of intron distribution at site 1931 of the chloroplastLSU rRNA gene reveals a rather restricted occurrence within thepolyphyletic genus Chlamydomonas, with no evidence of this intron among anumber of non- Chlamydomonad green algae surveyed, nor in land plants. Aparallel survey of homologues of a previously described and similarintron/ORF pair (C. reinhardtii chloroplast CrLSU/A. castellaniimitochondrial AcLSU.m3) also shows a restricted occurrence of this intron(site 2593) among chloroplasts, although the intron distribution issomewhat broader than that observed at site 1931, with site-2593 intronsappearing in several green algal branches outside of the Chlamydomonaslineage. The available data, while not definitive, are most consistent witha relatively recent horizontal transfer of both site-1931 and site- 2593introns (and their contained ORFs) between the chloroplast of aChlamydomonas-type organism and the mitochondrion of an Acanthamoeba- likeorganism, probably in the direction chloroplast to mitochondrion. The dataalso suggest that both introns could have been acquired in a single event.