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Published online on May 30, 2003, 10.1073/pnas.1230951100

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Evolution
Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans

( molecular evolution | chlorarachniophytes | chloroplast | phylogeny | secondary endosymbiosis )

John M. Archibald, Matthew B. Rogers, Michael Toop, Ken-ichiro Ishida *, and Patrick J. Keeling {dagger}

Canadian Institute for Advanced Research, Program in Evolutionary Biology, Department of Botany, University of British Columbia, 3529-6270 University Boulevard, Vancouver, BC, Canada V6T 1Z4

Edited by Jeffrey Donald Palmer, Indiana University, Bloomington, IN, and approved April 18, 2003 (received for review February 18, 2003)

Chlorarachniophytes are amoeboflagellate algae that acquired photosynthesis secondarily by engulfing a green alga and retaining its plastid (chloroplast). An important consequence of secondary endosymbiosis in chlorarachniophytes is that most of the nuclear genes encoding plastid-targeted proteins have moved from the nucleus of the endosymbiont to the host nucleus. We have sequenced and analyzed 83 cDNAs encoding 78 plastid-targeted proteins from the model chlorarachniophyte Bigelowiella natans (formerly Chlorarachnion sp. CCMP621). Phylogenies inferred from the majority of these genes are consistent with a chlorophyte green algal origin. However, a significant number of genes ({approx}21%) show signs of having been acquired by lateral gene transfer from numerous other sources: streptophyte algae, red algae (or algae with red algal endosymbionts), as well as bacteria. The chlorarachniophyte plastid proteome may therefore be regarded as a mosaic derived from various organisms in addition to the ancestral chlorophyte plastid. In contrast, the homologous genes from the chlorophyte Chlamydomonas reinhardtii do not show any indications of lateral gene transfer. This difference is likely a reflection of the mixotrophic nature of Bigelowiella (i.e., it is photosynthetic and phagotrophic), whereas Chlamydomonas is strictly autotrophic. These results underscore the importance of lateral gene transfer in contributing foreign proteins to eukaryotic cells and their organelles, and also suggest that its impact can vary from lineage to lineage.

*Present address: Department of Biology, Faculty of Science, Kanazawa University, Kakuma, Kanazawa 920-1192, Japan.

{dagger}To whom correspondence should be addressed.

E-mail: pkeeling{at}interchange.ubc.ca.

www.pnas.org/cgi/doi/10.1073/pnas.1230951100
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