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MBE Advance Access published online on April 18, 2007
Molecular Biology and Evolution, doi:10.1093/molbev/msm075
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© The Author 2007. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

Evolution of the Glucose-6-phosphate Isomerase: The Plasticity of Primary Metabolism in Photosynthetic Eukaryotes

Carina Grauvogel1,2, Henner Brinkmann3 and Jörn Petersen1,*

1 Institut für Genetik, Technische Universität Braunschweig, D-38106 Braunschweig, Germany
2 Georg-Speyer-Haus, Paul-Ehrlich-Straße 42-44, D-60596 Frankfurt am Main, Germany
3 Département de Biochimie, Université de Montréal C.P. 6128, Canada

* Address for Correspondence: Jörn Petersen; e-mail: j.petersen{at}tu-bs.de; phone: (+49) 531-391-5785; fax: (+49) 531-391-5765; address: Technische Universität Braunschweig, Institut für Genetik, Spielmannstraße 7; D-38106 Braunschweig, Germany.

Received for publication January 31, 2007. Revision received March 29, 2007. Accepted for publication April 2, 2007.

Glucose-6-phosphate isomerase (GPI) has an essential function in both catabolic glycolysis and anabolic gluconeogenesis and is universally distributed among eukaryotes, Bacteria and some Archaea. In addition to the cytosolic GPI, land plant chloroplasts harbor a nuclear encoded isoenzyme of cyanobacterial origin that is indispensable for the oxidative pentose phosphate pathway (OPPP) and plastid starch accumulation. We established twelve new GPI sequences from rhodophytes, the glaucophyte Cyanophora paradoxa, a ciliate and all orders of complex algae with red plastids (haptophytes, diatoms, cryptophytes, dinoflagellates). Our comprehensive phylogenies do not support previous GPI based speculations about a eukaryote-to-prokaryote horizontal gene transfer from metazoa to {gamma}-proteobacteria. The evolution of cytosolic GPI is largely in agreement with SSU analyses, which indicates that it is a specific marker of the host cell. A distinct subtree comprising alveolates (ciliates, apicomplexa, Perkinsus, dinoflagellates), stramenopiles (diatoms, Phytophthora [oomycete]) and Plantae (green plants, rhodophytes, Cyanophora) might suggest a common origin of these superensembles. Finally, in contrast to land plants where the plastid GPI is of cyanobacterial origin, chlorophytes and rhodophytes independently recruited a duplicate of the cytosolic GPI that subsequently acquired a transit peptide for plastid import. A secondary loss of the cytosolic isoenzyme and the plastid localization of the single GPI in chlorophycean green algae is compatible with physiological studies. Our findings reveal the fundamental importance of the plastid OPPP for Plantae and document the plasticity of primary metabolism.

Key Words: algal evolution • endosymbioses • gene transfer • glycolysis • oxidative pentose phosphate pathway • plastid metabolism


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