MBE Advance Access published online on March 20, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn064
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Research Article |
A Cryptic Algal Group Unveiled: A Plastid Biosynthesis Pathway in the Oyster Parasite Perkinsus marinus
* Department of Biological Sciences, Graduate School of Science, University of Tokyo, Japan
Department of Life Science, College of Science, and Research Information Center for Extremophile, Rikkyo University, Japan; and
Department of Biomedical Chemistry, Graduate School of Medicine, University of Tokyo, Japan
Corresponding author: Motomichi Matsuzaki, Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan, TEL/FAX: +81-3-5841-4046, e-mail: mzaki{at}biol.s.u-tokyo.ac.jp
Received for publication November 22, 2007. Revision received March 4, 2008. Accepted for publication March 14, 2008.
Plastids are widespread in plant and algal lineages. They are also exploited by some non-photosynthetic protists, including malarial parasites, to support their diverse modes of life. However, cryptic plastids may exist in other non-photosynthetic protists, which could be important in studies on the diversity and evolution of plastids. The parasite Perkinsus marinus, which causes mass mortality in oyster farms, is a non-photosynthetic protist that is phylogenetically related to plastid-bearing dinoflagellates and apicomplexans. In this study, we searched for P. marinus methylerythritol phosphate (MEP) pathway genes, responsible for de novo isoprenoid synthesis in plastids, and determined the full-length gene sequences for 6 of 7 of these genes. Phylogenetic analyses revealed that each P. marinus gene clusters with orthologs from plastid-bearing eukaryotes (PBEs), which have MEP pathway genes with essentially the same mosaic pattern of evolutionary origin. A new analytical method called Sliding-Window Iteration of TargetP was developed to examine the distribution of targeting preferences. This analysis revealed that the sequenced genes encode bipartite targeting peptides that are characteristic of proteins targeted to secondary plastids originating from endosymbiosis of eukaryotic algae. These results support our idea that Perkinsus is a cryptic algal group containing non-photosynthetic secondary plastids. In fact, immunofluorescent microscopy indicated that one of the MEP pathway enzymes, 1-deoxy-D-xylulose 5-phosphate reductoisomerase, was localized to small compartments near mitochondrion, which are possibly plastids. This tiny organelle seems to contain very low quantities of DNA, or may even lack DNA entirely. The MEP pathway genes are a useful tool for investigating plastid evolution in both of the photosynthetic and non-photosynthetic eukaryotes, and led us to propose the hypothesis that ancestral "chromalveolates" harbored plastids before a secondary endosymbiotic event.
Key Words: secondary endosymbiosis • protein-sorting signal • chromalveolates • methylerythritol phosphate pathway • Perkinsus marinus