Evidence of ancient genome reduction in red algae (Rhodophyta)

Journal of Phycology

Volumn 51, Issue 4, 2015, Pages 624-636

  Qiu, Huan ^a   Price, Dana C ^a   Yang, Eun Chan ^b   Yoon, Hwan Su ^c   Bhattacharya, Debashish ^a  

^a The State University of New Jersey   (United States)

^b Korea Research Institute of Ships and Ocean Engineering   (South Korea)

^c Sungkyunkwan University   (South Korea)

Author keywords

Flagella loss; Genome reduction; GPI biosynthesis; Horizontal gene transfer; Rhodophyta

Indexed keywords

ALGAE; BACTERIA (MICROORGANISMS); CYANIDIOPHYCEAE; EUKARYOTA; RHODOPHYTA;

EID: 84938986149     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/jpy.12294     Document Type: Article

References (70)

1. Bhattacharya, D., Price, D., Chan, C. X., Qiu, H., Rose, N., Ball, S. et al. 2013. Genome of the red alga Porphyridium purpureum. Nat. Commun. 4:1941.
2. Bhattacharya, D., Yoon, H. S. & Hackett, J. D. 2004. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. BioEssays 26:50-60.
3. Blanc, G., Agarkova, I., Grimwood, J., Kuo, A., Brueggeman, A., Dunigan, D. D., Gurnon, J. et al. 2012. The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol. 13:R39.
4. Boutet, E., Lieberherr, D., Tognolli, M., Schneider, M. & Bairoch, A. 2007. UniProtKB/Swiss-Prot. Methods Mol. Biol. 406:89-112.
5. Capella-Gutierrez, S., Silla-Martinez, J. M. & Gabaldon, T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972-3.
6. Cavalier-Smith, T. 1999. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Eukaryot. Microbiol. 46:347-66.
7. Chan, C. X., Blouin, N. A., Zhuang, Y. Y., Zäuner, S., Prochnik, S. E., Lindquist, E., Lin, S. et al. 2012a. Porphyra (Bangiophyceae) transcriptomes provide insights into red algal development and metabolism. J. Phycol. 48:1328-42.
8. Chan, C. X., Soares, M. B., Bonaldo, M. F., Wisecaver, J. H., Hackett, J. D., Anderson, D. M., Erdner, D. L. & Bhattacharya, D. 2012b. Analysis of Alexandrium tamarense (Dinophyceae) genes reveals the complex evolutionary history of a microbial eukaryote. J. Phycol. 48:1130-42.
9. Chan, C. X., Yang, E. C., Banerjee, T., Yoon, H. S., Martone, P. T., Estevez, J. M. & Bhattacharya, D. 2011. Red and green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Curr. Biol. 21:328-33.
10. Clarke, M., Lohan, A. J., Liu, B., Lagkouvardos, I., Roy, S., Zafar, N., Bertelli, C. et al. 2013. Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling. Genome Biol. 14:R11.
11. Cohen, O., Ashkenazy, H., Belinky, F., Huchon, D. & Pupko, T. 2010. GLOOME: gain loss mapping engine. Bioinformatics 26:2914-5.
12. Cohen, O. & Pupko, T. 2010. Inference and characterization of horizontally transferred gene families using stochastic mapping. Mol. Biol. Evol. 27:703-13.
13. Collen, J., Porcel, B., Carre, W., Ball, S. G., Chaparro, C., Tonon, T., Barbeyron, T. et al. 2013. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc. Natl. Acad. Sci. USA 110:5247-52.
14. Das, G. & Varshney, U. 2006. Peptidyl-tRNA hydrolase and its critical role in protein biosynthesis. Microbiology 152:2191-5.
15. Delwiche, C. F. & Palmer, J. D. 1996. Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol. Biol. Evol. 13:873-82.
16. Deusch, O., Landan, G., Roettger, M., Gruenheit, N., Kowallik, K. V., Allen, J. F., Martin, W. & Dagan, T. 2008. Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol. Biol. Evol. 25:748-61.
17. Edgar, R. C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113.
18. Farris, J. 1977. Phylogenetic analysis under Dollo's law. Syst. Zool. 26:77-88.
19. Felsenstein, J. 1996. Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. Methods Enzymol. 266:418-27.
20. Finet, C., Timme, R. E., Delwiche, C. F. & Marletaz, F. 2010. Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr. Biol. 20:2217-22.
21. Fumi, Y. Y., Keiji, N., Haruko, K., Toshiyuki, N. & Tsuneyoshi, K. 2005. Identification of lysosome-like structures in a unicellular red alga Cyanidioschyzon merolae. Cytologia 70:351-4.
22. Giovannoni, S. J., Tripp, H. J., Givan, S., Podar, M., Vergin, K. L., Baptista, D., Bibbs, L. et al. 2005. Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:1242-5.
23. Harada, F. & Nishimura, S. 1972. Possible anticodon sequences of tRNA His, tRNA Asm, and tRNA Asp from Escherichia coli B. Universal presence of nucleoside Q in the first postion of the anticondons of these transfer ribonucleic acids. Biochemistry 11:301-8.
24. Howe, C. J., Barbrook, A. C., Nisbet, R. E., Lockhart, P. J. & Larkum, A. W. 2008. The origin of plastids. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363:2675-85.
25. Huang, J. & Yue, J. 2013. Horizontal gene transfer in the evolution of photosynthetic eukaryotes. J. Syst. Evol. 51:13-29.
26. Iwata-Reuyl, D. 2003. Biosynthesis of the 7-deazaguanosine hypermodified nucleosides of transfer RNA. Bioorg. Chem. 31:24-43.
27. Jurka, J., Kapitonov, V. V., Pavlicek, A., Klonowski, P., Kohany, O. & Walichiewicz, J. 2005. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110:462-7.
28. Kanehisa, M. & Goto, S. 2000. KEGG: Kyoto encyclopedia of genes and genomes. Nuc. Acids Res. 28:27-30.
29. Kawagoe, K., Kitamura, D., Okabe, M., Taniuchi, I., Ikawa, M., Watanabe, T., Kinoshita, T. & Takeda, J. 1996. Glycosylphosphatidylinositol-anchor-deficient mice: implications for clonal dominance of mutant cells in paroxysmal nocturnal hemoglobinuria. Blood 87:3600-6.
30. Keeling, P. J. 2009. Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr. Opin. Genet. Dev. 19:613-9.
31. Keeling, P. J. & Palmer, J. D. 2008. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9:605-18.
32. Kettler, G. C., Martiny, A. C., Huang, K., Zucker, J., Coleman, M. L., Rodrigue, S., Chen, F. et al. 2007. Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet. 3:e231.
33. Kroemer, G., Marino, G. & Levine, B. 2010. Autophagy and the integrated stress response. Mol. Cell 40:280-93.
34. Larkum, A. W., Lockhart, P. J. & Howe, C. J. 2007. Shopping for plastids. Trends Plant Sci. 12:189-95.
35. Leliaert, F., Smith, D. R., Moreau, H., Herron, M. D., Verbruggen, H., Delwiche, C. F. & De Clerck, O. 2012. Phylogeny and molecular evolution of the green algae. Crit. Rev. Plant Sci. 31:1-46.
36. Levine, B., Mizushima, N. & Virgin, H. W. 2011. Autophagy in immunity and inflammation. Nature 469:323-35.
37. Li, L., Stoeckert, C. J. Jr & Roos, D. S. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178-89.
38. Lillico, S., Field, M. C., Blundell, P., Coombs, G. H. & Mottram, J. C. 2003. Essential roles for GPI-anchored proteins in African trypanosomes revealed using mutants deficient in GPI8. Mol. Biol. Cell 14:1182-94.
39. Matsuzaki, M., Misumi, O., Shin, I. T., Maruyama, S., Takahara, M., Miyagishima, S. Y., Mori, T. et al. 2004. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653-7.
40. McCutcheon, J. P. & Moran, N. A. 2012. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10:13-26.
41. Minh, B. Q., Nguyen, M. A. & von Haeseler, A. 2013. Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol. 30:1188-95.
42. Moran, N. A. 2002. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583-6.
43. Morgat, A., Coissac, E., Coudert, E., Axelsen, K. B., Keller, G., Bairoch, A., Bridge, A., Bougueleret, L., Xenarios, I. & Viari, A. 2012. UniPathway: a resource for the exploration and annotation of metabolic pathways. Nuc. Acids Res. 40:D761-9.
44. Moriya, Y., Itoh, M., Okuda, S., Yoshizawa, A. C. & Kanehisa, M. 2007. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 35:W182-5.
45. Morrison, H. G., McArthur, A. G., Gillin, F. D., Aley, S. B., Adam, R. D., Olsen, G. J., Best, A. A. et al. 2007. Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317:1921-6.
46. Nakamura, Y., Sasaki, N., Kobayashi, M., Ojima, N., Yasuike, M., Shigenobu, Y., Satomi, M. et al. 2013. The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLoS ONE 8:e57122.
47. Niersbach, M., Kreuzaler, F., Geerse, R. H., Postma, P. W. & Hirsch, H. J. 1992. Cloning and nucleotide sequence of the Escherichia coli K-12 ppsA gene, encoding PEP synthase. Mol. Gen. Genet. 231:332-6.
48. Nikaido, I., Asamizu, E., Nakajima, M., Nakamura, Y., Saga, N. & Tabata, S. 2000. Generation of 10, 154 expressed sequence tags from a leafy gametophyte of a marine red alga, Porphyra yezoensis. DNA Res. 7:223-7.
49. Obornik, M. & Green, B. R. 2005. Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol. Biol. Evol. 22:2343-53.
50. Palenik, B., Grimwood, J., Aerts, A., Rouze, P., Salamov, A., Putnam, N., Dupont, C. et al. 2007. The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc. Natl. Acad. Sci. USA 104:7705-10.
51. Parra, G., Bradnam, K. & Korf, I. 2007. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23:1061-7.
52. Pazour, G. J., Agrin, N., Leszyk, J. & Witman, G. B. 2005. Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170:103-13.
53. Price, D. C., Chan, C. X., Yoon, H. S., Yang, E. C., Qiu, H., Weber, A. P., Schwacke, R. et al. 2012. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335:843-7.
54. Prochnik, S. E., Umen, J., Nedelcu, A. M., Hallmann, A., Miller, S. M., Nishii, I., Ferris, P. et al. 2010. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329:223-6.
55. Qiu, H., Price, D., Webber, A. P., Reeb, V., Yang, E. C., Lee, J. M., Kim, S. Y., Yoon, H. S. & Bhattacharya, D. 2013a. Adaptation through horizontal gene transfer in the cryptoendolithic red alga Galdieria phlegrea. Curr. Biol. 23:R865-6.
56. Qiu, H., Yoon, H. S. & Bhattacharya, D. 2013b. Algal endosymbionts as vectors of horizontal gene transfer in photosynthetic eukaryotes. Front. Plant Sci. 4:366.
57. Reeb, V. & Bhattacharya, D. 2010. The thermo-acidophilic Cyanidiophyceae (Cyanidiales). In Seckbach, J. & Chapman, D. [Eds.] Red Algae in the Genomic Age, Vol 13, Cellular Origin, Life in Extreme Habitats and Astrobiology. Springer, New York, pp. 409-26.
58. Rockwell, N. C., Duanmu, D., Martin, S. S., Bachy, C., Price, D. C., Bhattacharya, D., Worden, A. Z. & Lagarias, J. C. 2014. Eukaryotic algal phytochromes span the visible spectrum. Proc. Natl. Acad. Sci. USA 111:3871-6.
59. Schoenknecht, G., Chen, W. H., Ternes, C. M., Barbier, G. G., Shrestha, R. P., Stanke, M., Brautigam, A. et al. 2013. Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339:1207-10.
60. Searles, R. B. 1980. The strategy of the red algal life history. Am. Nat. 116:113-20.
61. Sherrier, D. J., Prime, T. A. & Dupree, P. 1999. Glycosylphosphatidylinositol-anchored cell-surface proteins from Arabidopsis. Electrophoresis 20:2027-35.
62. Sinden, R. E., Talman, A., Marques, S. R., Wass, M. N. & Sternberg, M. J. 2010. The flagellum in malarial parasites. Curr. Opin. Microbiol. 13:491-500.
63. Spiegel, F. W. 2012. Contemplating the first Plantae. Science 335:809-10.
64. Takeda, J. & Kinoshita, T. 1995. GPI-anchor biosynthesis. Trends Biochem. Sci. 20:367-71.
65. Timmis, J. N., Ayliffe, M. A., Huang, C. Y. & Martin, W. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5:123-35.
66. Toft, C. & Fares, M. A. 2008. The evolution of the flagellar assembly pathway in endosymbiotic bacterial genomes. Mol. Biol. Evol. 25:2069-76.
67. Wolf, Y. I. & Koonin, E. V. 2013. Genome reduction as the dominant mode of evolution. BioEssays 35:829-37.
68. Worden, A. Z., Lee, J. H., Mock, T., Rouze, P., Simmons, M. P., Aerts, A. L., Allen, A. E. et al. 2009. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268-72.
69. Yoon, H. S., Müller, K. M., Sheath, R. G., Ott, F. D. & Bhattacharya, D. 2006. Defining the major lineages of red algae (Rhodophyta). J. Phycol. 42:482-92.
70. Yue, J., Sun, G., Hu, X. & Huang, J. 2013. The scale and evolutionary significance of horizontal gene transfer in the choanoflagellate Monosiga brevicollis. BMC Genom. 14:729.