Genomic Footprints of a Cryptic Plastid Endosymbiosis in Diatoms

Green for Diatoms Diatoms account for 20% of global carbon fixation and, together with other chromalveolates (e.g., dinoflagellates and coccolithophorids), represent many thousands of eukaryote taxa in the world's oceans and on the tree of life. Moustafa et al. (p. 1724; see the Perspective by Dagan and Martin) have discovered that the genomes of diatoms are highly chimeric, with about 10% of their nuclear genes being of foreign algal origin. Of this set of 1272 algal genes, 253 were, as expected, from a distant red algal secondary endosymbiont, but more than 1000 of the genes were derived from green algae and predated the red algal relationship. These protist taxa are important not only for genetic and genomic investigations but also for their potential in biofuel and nanotechnology applications and in global primary productivity in relation to climate change. The genomes of early plant representatives are composites, with a substantial number of foreign genes from red and green algae. Diatoms and other chromalveolates are among the dominant phytoplankters in the world’s oceans. Endosymbiosis was essential to the success of chromalveolates, and it appears that the ancestral plastid in this group had a red algal origin via an ancient secondary endosymbiosis. However, recent analyses have turned up a handful of nuclear genes in chromalveolates that are of green algal derivation. Using a genome-wide approach to estimate the “green” contribution to diatoms, we identified >1700 green gene transfers, constituting 16% of the diatom nuclear coding potential. These genes were probably introduced into diatoms and other chromalveolates from a cryptic endosymbiont related to prasinophyte-like green algae. Chromalveolates appear to have recruited genes from the two major existing algal groups to forge a highly successful, species-rich protist lineage.

[1]  W. Martin,et al.  Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[2]  A. Grossman,et al.  Ancient recruitment by chromists of green algal genes encoding enzymes for carotenoid biosynthesis. , 2008, Molecular biology and evolution.

[3]  T. Cavalier-smith Principles of Protein and Lipid Targeting in Secondary Symbiogenesis: Euglenoid, Dinoflagellate, and Sporozoan Plastid Origins and the Eukaryote Family Tree 1 , 2 , 1999, The Journal of eukaryotic microbiology.

[4]  David G. Mann,et al.  Diatoms: Biology and Morphology of the Genera , 1990 .

[5]  L. Katz,et al.  BMC Evolutionary Biology BioMed Central Research article Broadly sampled multigene trees of eukaryotes , 2008 .

[6]  D. Bhattacharya,et al.  Multiple Genes of Apparent Algal Origin Suggest Ciliates May Once Have Been Photosynthetic , 2008, Current Biology.

[7]  Paul G. Falkowski,et al.  Evolution of primary producers in the sea , 2007 .

[8]  Debashish Bhattacharya,et al.  Cyanobacterial Contribution to Algal Nuclear Genomes Is Primarily Limited to Plastid Functions , 2006, Current Biology.

[9]  C. Delwiche,et al.  Phylogenetic analyses indicate that the 19'Hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. , 2000, Molecular biology and evolution.

[10]  B. De Baets,et al.  Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Fabien Burki,et al.  Phylogenomics reveals a new ‘megagroup’ including most photosynthetic eukaryotes , 2008, Biology Letters.

[12]  U. Maier,et al.  How to Evolve a Complex Plastid? ‐ A Hypothesis , 1994 .

[13]  Debashish Bhattacharya,et al.  Phylogeny of Calvin cycle enzymes supports Plantae monophyly. , 2007, Molecular phylogenetics and evolution.

[14]  M. Melkonian,et al.  PRASINOPHYTES FORM INDEPENDENT LINEAGES WITHIN THE CHLOROPHYTA: EVIDENCE FROM RIBOSOMAL RNA SEQUENCE COMPARISONS 1 , 1994 .

[15]  Naiara Rodríguez-Ezpeleta,et al.  Monophyly of Primary Photosynthetic Eukaryotes: Green Plants, Red Algae, and Glaucophytes , 2005, Current Biology.

[16]  A. Falciatore,et al.  Evolutionary Origins and Functions of the Carotenoid Biosynthetic Pathway in Marine Diatoms , 2008, PloS one.

[17]  Nicole Poulsen,et al.  Diatoms-from cell wall biogenesis to nanotechnology. , 2008, Annual review of genetics.

[18]  J. Randerson,et al.  Primary production of the biosphere: integrating terrestrial and oceanic components , 1998, Science.

[19]  Sabine Cornelsen,et al.  Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Young,et al.  Coccolithophores : from molecular processes to global impact , 2004 .

[21]  B. Green,et al.  Second- and third-hand chloroplasts in dinoflagellates: Phylogeny of oxygen-evolving enhancer 1 (PsbO) protein reveals replacement of a nuclear-encoded plastid gene by that of a haptophyte tertiary endosymbiont , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[22]  H. Brinkmann,et al.  A “Green” Phosphoribulokinase in Complex Algae with Red Plastids: Evidence for a Single Secondary Endosymbiosis Leading to Haptophytes, Cryptophytes, Heterokonts, and Dinoflagellates , 2006, Journal of Molecular Evolution.

[23]  G Charles Dismukes,et al.  Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. , 2008, Current opinion in biotechnology.