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Cyanophora Paradoxa Genome Elucidates Origin of Photosynthesis

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Cyanophora Paradoxa Genome Elucidates Origin of Photosynthesis REPORTS sharing their kinematic models and GPS data for comparison geodetic and seismic data. The codes are available as a Figs. S1 and S2 with the dynamic models, L. Wen for help with using his zip file as part of the supporting online material. Table S1 code, and three anonymous reviewers for their comments References (29–37) that substantially improved the manuscript. We are grateful Supporting Online Material Computer Codes to UNAVCO, Incorporated Research Institutions for Seismology, www.sciencemag.org/cgi/content/full/335/6070/838/DC1 NSF-EarthScope, International GNSS Service, NASA, and Methods 20 September 2011; accepted 24 January 2012 countless researchers for facilitation and availability of SOM Text 10.1126/science.1214209 reinhardtii (20, 21). Phylogenomic analysis of Cyanophora paradoxa Genome the predicted C. paradoxa proteins showed 274 to be of cyanobacterial provenance (22). This Elucidates Origin of Photosynthesis constitutes ~6% of proteins in the glaucophyte that have significant BLASTp hits (i.e., 274 out of 4628), as found in other algae (20, 21). BLASTp in Algae and Plants analysis identified 2029 proteins that are puta- tively destined for the plastid, of which 293 con- 1 1 2,3 2 2 Dana C. Price, Cheong Xin Chan, * Hwan Su Yoon, Eun Chan Yang, Huan Qiu, tain the transit sequence for plastid import [identified 4 5 1 6 6 Andreas P. M. Weber, Rainer Schwacke, Jeferson Gross, Nicolas A. Blouin, Chris Lane, by the presence of phenylalanine (F) within the 7 8 8 9 Adrián Reyes-Prieto, Dion G. Durnford, Jonathan A. D. Neilson, B. Franz Lang, first four amino acids: MF, MAF, MNAF, MSAF, 9 10 11 12 Gertraud Burger, Jürgen M. Steiner, Wolfgang Löffelhardt, Jonathan E. Meuser, and MAAF] (23, 24) (fig. S4B). Of these 293 13 14 14 15 Matthew C. Posewitz, Steven Ball, Maria Cecilia Arias, Bernard Henrissat, proteins, 80% are derived from Cyanobacteria. 15 16,17,18 16,17 Pedro M. Coutinho, Stefan A. Rensing, Aikaterini Symeonidi, Another source of foreign genes in Plantae 19 20 1 Harshavardhan Doddapaneni, Beverley R. Green, Veeran D. Rajah, is horizontal gene transfer (HGT), which is not 21,22 1 Jeffrey Boore, Debashish Bhattacharya † associated with endosymbiosis. Using 35,126 bacterial sequences as a query, we found 444 The primary endosymbiotic origin of the plastid in eukaryotes more than 1 billion years ago led to the noncyanobacterial gene families with a common evolution of algae and plants. We analyzed draft genome and transcriptome data from the basally origin shared amongst Bacteria and Plantae. Among on February 21, 2012 diverging alga Cyanophora paradoxa and provide evidence for a single origin of the primary plastid in the them, 15 genes are present in all three Plantae eukaryote supergroup Plantae. C. paradoxa retains ancestral features of starch biosynthesis, fermentation, phyla. An example of a gene derived from Bacte- and plastid protein translocation common to plants and algae but lacks typical eukaryotic light-harvesting ria after an ancient HGT event that is shared by complex proteins. Traces of an ancient link to parasites such as Chlamydiae were found in the genomes C. paradoxa Chlamydia of and other Plantae. Apparently, -like bacteria donated genes that allow export 1Department of Ecology, Evolution, and Natural Resources and of photosynthate from the plastid and its polymerization into storage polysaccharide in the cytosol. Institute of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ 08901, USA. 2Bigelow Laboratory for Ocean 3 ukaryote evolution has largely been shaped test Plantae monophyly, we have generated a draft Sciences,WestBoothbayHarbor,ME04575,USA. Depart- ment of Biological Sciences, Sungkyunkwan University, Suwon by the process of primary endosymbiosis, assembly of the ≈70 Mbp nuclear genome from the 4 440-746, Korea. Institute for Plant Biochemistry, Heinrich- www.sciencemag.org Ewhereby bacterial cells were taken up and glaucophyte Cyanophora paradoxa CCMP329 Heine-University, D-40225 Duesseldorf, Germany. 5Botanical over time evolved into double membrane–bound (Pringsheim strain) (Fig. 1A). Institute, Biocenter Cologne, University of Cologne, Zülpicher organelles, the plastid and the mitochondrion A total of 27,921 C. paradoxa proteins were Strasse 47b, 50674 Cologne, Germany. 6Department of Bio- logical Sciences, University of Rhode Island, Kingston, RI 02881, [e.g., (1, 2)]. The cyanobacterium-derived plastid predicted from the genome data, and 4628 had 7 ≤ −10 USA. Canadian Institute for Advanced Research, Department is found in diverse photosynthetic organisms, significant BLASTp hits (e 10 ) to prokaryote of Biology, University of New Brunswick, Fredericton, New including Glaucophyta, Rhodophyta, and green and eukaryote genome data in our comprehensive Brunswick E3B 5A3, Canada. 8Department of Biology, Uni- algae and their land plant descendants (the local database (table S1). Using phylogenomics versity of New Brunswick, Fredericton, New Brunswick E3B 5A3, Canada. 9Centre Robert Cedergren, Départementde Biochimie, Viridiplantae). These three lineages are postu- (16), we generated 4445 maximum likelihood Downloaded from Université de Montréal, Montréal, Québec H3C 3J7, Canada. lated to form the monophyletic group Plantae (or trees from the C. paradoxa proteins and found 10Department of Biology/Plant Physiology, Martin-Luther-University Archaeplastida) (3–6), a hypothesis that suggests that >60% support a sister-group relationship Halle-Wittenberg, Germany. 11Max F. Perutz Laboratories, De- the primary cyanobacterial endosymbiosis oc- between glaucophytes and red and/or green algae partment of Biochemistry and Cell Biology, University of Vienna, 12 curred exclusively in their single common ances- with a bootstrap value ≥90% (Fig. 1B and fig. Vienna, Austria. Department of Civil and Environmental En- gineering, Colorado School of Mines, Golden, CO 80401, USA. tor. Plastid gene trees demonstrate a single origin S1). The Plantae clade in many of these trees is, 13Department of Chemistry and Geochemistry, Colorado School of the Plantae (5, 7); however, many nuclear, mul- however, interrupted by chlorophyll a + c contain- of Mines, Golden, CO 80401, USA. 14Unité de Glycobiologie tiprotein phylogenies provide little (8) or no support ing “chromalveolates.” An example of this type Structurale et Fonctionnelle, UMR 8576 CNRS-USTL, Université (9, 10) for their monophyly. These latter results of tree is fructose-1,6-bisphosphatase (Fig. 1C des Sciences et Technologies de Lille, 59655 Villeneuve d’Ascq Cedex, France. 15Universités Aix-Marseille I & II, Case 932, 163 may reflect a reticulate ancestry among genes and fig. S2), which has cytosolic and plastidic Avenue de Luminy, 13288 Marseille Cedex 9, France. 16Faculty that can mislead phylogenetic inference (11). isoforms. The gene for this enzyme, found in of Biology, University of Freiburg, Freiburg, Germany. 17FRISYS Furthermore, glaucophytes retain ancestral cya- stramenopiles (e.g., diatoms) and haptophytes, Freiburg Initiative in Systems Biology, University of Freiburg, Freiburg, Germany. 18BIOSS Centre for Biological Signalling nobacterial features not found in other Plantae originated from the red algal secondary endo- 19 (12)—such as the presence of peptidoglycan be- symbiont that gave rise to the plastid in these taxa Studies, University of Freiburg, Freiburg, Germany. Roy J. Carver Center for Genomics, Department of Biology, University of Iowa, tween the two bounding membranes of the plastid (2, 9). This sort of intracellular gene transfer asso- Iowa City, IA, 52242, USA. 20Department of Botany, University of (13)—that cast doubt on their evolutionary his- ciated with endosymbiosis (EGT) has greatly British Columbia, Vancouver, British Columbia V6T 1Z4, Canada. tory. It is therefore unclear whether the Plantae enriched algal and land plant genomes (17, 18). 21Genome Project Solutions, Hercules, CA 94547, USA. 22Depart- host and its plastid, with its associated complex We estimated the “footprint” of cyanobacterium- ment of Integrative Biology, University of California, Berkeley, CA 94720, USA. machinery (e.g., for plastid protein import and derived EGT in Plantae genomes. The proportion *Present address: Institute for Molecular Bioscience, Univer- solute transport) (14, 15), had a single origin or of cyanobacterium-derived nuclear genes varies sity of Queensland, Brisbane, QLD 4072, Australia. multiple origins. To elucidate the evolutionary from 18% in Arabidopsis thaliana (19)to~7%in †To whom correspondence should be addressed. E-mail: history of key algal and land plant traits and to mesophilic red algae and 6% in Chlamydomonas [email protected] www.sciencemag.org SCIENCE VOL 335 17 FEBRUARY 2012 843 REPORTS Plantae is that encoding a thiamine pyrophosphate– erated a near-complete plastid genome sequence of the plastid data shows the expected monophyly dependent pyruvate decarboxylase family protein from G. nostochinearum that was added to the of Plantae plastids (2, 5, 6) and places glauco- involved in alcohol fermentation (Fig. 1D). An- existing plastid genome data from C. paradoxa phytes very close to the divergence point of red other 60 genes were present in only two of the tree (GenBank NC_001675). The mitochondrial DNAs and green algae (fig. S5A). phyla (i.e., 24, 10, and 26 genes in Glaucophyta- (mtDNAs) of C. paradoxa and G. nostochinearum Building on the support for Plantae mono- Viridiplantae, Glaucophyta-Rhodophyta, and share similar characteristics, including a large gene
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