MBE Advance Access originally published online on August 10, 2005
Molecular Biology and Evolution 2005 22(12):2343-2353; doi:10.1093/molbev/msi230
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Research Article |
Mosaic Origin of the Heme Biosynthesis Pathway in Photosynthetic Eukaryotes
,
* Department of Botany, University of British Columbia, Vancouver BC, Canada; Institute of Parasitology, Academy of Sciences of Czech Republic, Brani
ovská, 
eské Bud
jovice, Czech Republic; and Faculty of Biological Sciences, University of South Bohemia, Braniovská, eské Budjovice, Czech Republic
E-mail: brgreen{at}interchange.ubc.ca.
Heme biosynthesis represents one of the most essential metabolic pathways in living organisms, providing the precursors for cytochrome prosthetic groups, photosynthetic pigments, and vitamin B12. Using genomic data, we have compared the heme pathway in the diatom Thalassiosira pseudonana and the red alga Cyanidioschyzon merolae to those of green algae and higher plants, as well as to those of heterotrophic eukaryotes (fungi, apicomplexans, and animals). Phylogenetic analyses showed the mosaic character of this pathway in photosynthetic eukaryotes. Although most of the algal and plant enzymes showed the expected plastid (cyanobacterial) origin, at least one of them (porphobilinogen deaminase) appears to have a mitochondrial (
-proteobacterial) origin. Another enzyme, glutamyl-tRNA synthase, obviously originated in the eukaryotic nucleus. Because all the plastid-targeted sequences consistently form a well-supported cluster, this suggests that genes were either transferred from the primary endosymbiont (cyanobacteria) to the primary host nucleus shortly after the primary endosymbiotic event or replaced with genes from other sources at an equally early time, i.e., before the formation of three primary plastid lineages. The one striking exception to this pattern is ferrochelatase, the enzyme catalyzing the first committed step to heme and bilin pigments. In this case, two red algal sequences do not cluster either with the other plastid sequences or with cyanobacterial sequences and appear to have a proteobacterial origin like that of the apicomplexan parasites Plasmodium and Toxoplasma. Although the heterokonts also acquired their plastid via secondary endosymbiosis from a red alga, the diatom has a typical plastid-cyanobacterial ferrochelatase. We have not found any remnants of the plastidlike heme pathway in the nonphotosynthetic heterokonts Phytophthora ramorum and Phytophthora sojae.
Key Words: heme biosynthetic pathway • algae • chloroplasts • evogenomics
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