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Evolutionary origin of cryptomonad microalgae: Two novel chloroplast/cytosol-specific GAPDH genes as potential markers of ancestral endosymbiont and host cell components

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Abstract

Cryptomonads are complex microalgae which share characteristics of chromophytes (chlorophyll c, extra pair of membranes surrounding the plastids) and rhodophytes (phycobiliproteins). Unlike chromophytes, however, they contain a small nucleus-like organelle, the nucleomorph, in the periplastidial space between the inner and outer plastid membrane pairs. These cellular characteristics led to the suggestion that cryptomonads may have originated via a eukaryoteeukaryote endosymbiosis between a phagotrophic host cell and a unicellular red alga, a hypothesis supported by rRNA phylogenies. Here we characterized cDNAs of the nuclear genes encoding chloroplast and cytosolic glyceraldehyde-3-phosphate dehydrogenases (GAPDH) from the two cryptomonads Pyrenomonas salina and Guillardia theta. Our results suggest that in cryptomonads the classic Calvin cycle GAPDH enzyme of cyanobacterial origin, GapAB, is absent and functionally replaced by a photosynthetic GapC enzyme of proteobacterial descent, GapCl. The derived GapCl precursor contains a typical signal/transit peptide of complex structure and sequence signatures diagnostic for dual cosubstrate specificity with NADP and NAD. In addition to this novel GapCl gene a cytosol-specific GapC2 gene of glycolytic function has been found in both cryptomonads showing conspicuous sequence similarities to animal GAPDH. The present findings support the hypothesis that the host cell component of cryptomonads may be derived from a phototrophic rather than a organotrophic cell which lost its primary plastid after receiving a secondary one. Hence, cellular compartments of endosymbiotic origin may have been lost or replaced several times in eukaryote cell evolution, while the corresponding endosymbiotic genes (e.g., GapC1) were retained, thereby increasing the chimeric potential of the nuclear genome.

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Authors and Affiliations

  1. Institut für Genetik, Universität Braunschweig, D-38106, Braunschweig, Germany

    Marie-Françoise Liaud, Ulrike Brandt & Rüdiger Cerff

  2. Institut für Biologie II, Universität Freiburg, D-79104, Freiburg, Germany

    Margitta Scherzinger

  3. Lehrstuhl Pflanzenökologie und Systematik, Universität Bayreuth, D-95440, Bayreuth, Germany

    Margitta Scherzinger

Authors
  1. Marie-Françoise Liaud
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  2. Ulrike Brandt
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  3. Margitta Scherzinger
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  4. Rüdiger Cerff
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Additional information

The nucleotide sequence data (cDNAs) reported will appear in the DDBJ/EMBL/GenBank International Nucleotide Sequence Database under the accession numbers U40032 (GapCl, Guillardia theta), U40033 (CapC1, Pyrenomonas salina), U39873 (GapC2, Guillardia theta), and U39897 (GapC2, Pyrenomonas salina). Until recently Guillardia theta (original name Cryptomonas theta) has been erroneously called Cryptomonas phi due to a confusion of the two different organisms prior to the distribution of cultures to the international cryptomonad community (G. McFadden, publication in preparation)

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Liaud, MF., Brandt, U., Scherzinger, M. et al. Evolutionary origin of cryptomonad microalgae: Two novel chloroplast/cytosol-specific GAPDH genes as potential markers of ancestral endosymbiont and host cell components. J Mol Evol 44 (Suppl 1), S28–S37 (1997). https://doi.org/10.1007/PL00000050

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  • DOI: https://doi.org/10.1007/PL00000050

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