Primary endosymbiosis and the evolution of light and oxygen sensing in photosynthetic eukaryotes

Frontiers in Ecology and Evolution

Volumn 2, Issue OCT, 2014, Pages

  Rockwell, Nathan C ^a   Lagarias, J C ^a   Bhattacharya, Debashish ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Algal evolution; Archaeplastida; Ferredoxin depending bilin reductase; Phagotrophy; Phytochrome; Primary endosymbiosis

Indexed keywords

EID: 84920389561     PISSN: None     EISSN: 2296701X     Source Type: Journal    
DOI: 10.3389/fevo.2014.00066     Document Type: Article

References (125)

1. Adl, S. M., Simpson, A. G., Lane, C. E., Lukeš, J., Bass, D., Bowser, S. S., et al. (2012). The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59, 429-493. doi: 10.1111/j.1550-7408.2012.00644.x
2. Adolf, J. E., Stoecker, D. K., and Harding, L. W. Jr. (2006). The balance of autotrophy and heterotrophy during mixotrophic growth of Karlodinium micrum (Dinophyceae). J. Plankton Res. 28, 737-751. doi: 10.1093/plankt/fbl007
3. Alvey, R. M., Biswas, A., Schluchter, W. M., and Bryant, D. A. (2011). Effects of modified Phycobilin biosynthesis in the Cyanobacterium Synechococcus sp. Strain PCC 7002. J. Bact. 193, 1663-1671. doi: 10.1128/JB.01392-10
4. Apple, J. K., Strom, S. L., Palenik, B., and Brahamsha, B. (2011). Variability in protist grazing and growth on different marine Synechococcus isolates. Appl. Environ. Microbiol. 77, 3074-3084. doi: 10.1128/AEM.02241-10
5. Auldridge, M. E., and Forest, K. T. (2011). Bacterial phytochromes: more than meets the light. Crit. Rev. Biochem. Mol. Biol. 46, 67-88. doi: 10.3109/10409238.2010.546389
6. Ball, S. G., Subtil, A., Bhattacharya, D., Moustafa, A., Weber, A. P., Gehre, L., et al. (2013). Metabolic effectors secreted by bacterial pathogens: essential facilitators of plastid endosymbiosis? Plant Cell 25, 7-21. doi: 10.1105/tpc.112.101329
7. Becker, B., Hoef-Emden, K., and Melkonian, M. (2008). Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes. BMC Evol. Biol. 8:203. doi: 10.1186/1471-2148-8-203
8. 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. doi: 10.1038/ncomms2931
9. Bhattacharya, D., Yoon, H. S., and Hackett, J. D. (2004). Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 26, 50-60. doi: 10.1002/bies.10376
10. Bhoo, S. H., Davis, S. J., Walker, J., Karniol, B., and Vierstra, R. D. (2001). Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 414, 776-779. doi: 10.1038/414776a
11. Bibby, T. S., Nield, J., and Barber, J. (2001). Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412, 743-745. doi: 10.1038/35089098
12. Boekema, E. J., Hifney, A., Yakushevska, A. E., Piotrowski, M., Keegstra, W., Berry, S., et al. (2001). A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature 412, 745-748. doi: 10.1038/35089104
13. Brandt, S., von Stetten, D., Günther, M., Hildebrandt, P., and Frankenberg-Dinkel, N. (2008). The fungal phytochrome FphA from Aspergillus nidulans. J. Biol. Chem. 283, 34605-34614. doi: 10.1074/jbc. M805506200
14. Burkholder, J. M., Gilbert, P. M., and Skelton, H. M. (2008). Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8, 77-93. doi: 10.1016/j.hal.2008.08.010
15. Burki, F., Shalchian-Tabrizi, K., and Pawlowski, J. (2007). Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE 2:e790. doi: 10.1371/journal.pone.0000790
16. Casal, J. J. (2013). Photoreceptor signaling networks in plant responses to shade. Ann. Rev. Plant Biol. 64, 403-427. doi: 10.1146/annurev-arplant-050312-120221
17. Cavalier-Smith, T. (1982). The origin of plastids. Biol. J. Linn. Soc. 17, 289-306. doi: 10.1111/j.1095-8312.1982.tb02023.x
18. Chan, C. X., Bhattacharya, D., and Reyes-Prieto, A. (2012). Endosymbiotic and horizontal gene transfer in microbial eukaryotes: Impacts on cell evolution and the tree of life. Mob. Genet. Elements 2, 101-105. doi: 10.4161/mge.20110
19. Chan, C. X., Reyes-Prieto, A., and Bhattacharya, D. (2011). Red and green algal origin of diatom membrane transporters: insights into environmental adaptation and cell evolution. PLoS ONE 6:e29138. doi: 10.1371/journal.pone.0029138
20. Chen, Y. R., Su, Y.-S., and Tu, S.-L. (2012). Distinct phytochrome actions in nonvascular plants revealed by targeted inactivation of phytobilin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 109, 8310-8315. doi: 10.1073/pnas.1201744109
21. Collén, J., Porcel, B., Carré, W., Ball, S. G., Chaparro, C., Tonon, 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. U.S.A. 110, 5247-5252. doi: 10.1073/pnas.1221259110
22. Colleoni, C., Linka, M., Deschamps, P., Handford, M. G., Dupree, P., Weber, A. P., et al. (2010). Phylogenetic and biochemical evidence supports the recruitment of an ADP-glucose translocator for the export of photosynthate during plastid endosymbiosis. Mol. Biol. Evol. 27, 2691-2701. doi: 10.1093/molbev/msq158
23. Curtis, B. A., Tanifuji, G., Burki, F., Gruber, A., Irimia, M., Maruyama, S., et al. (2012). Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492, 59-65. doi: 10.1038/nature11681
24. Dammeyer, T., Bagby, S. C., Sullivan, M. B., Chisholm, S. W., and Frankenberg-Dinkel, N. (2008). Efficient phage-mediated pigment biosynthesis in oceanic cyanobacteria. Curr. Biol. 18, 442-448. doi: 10.1016/j.cub.2008.02.067
25. Dammeyer, T., and Frankenberg-Dinkel, N. (2006). Insights into phycoerythrobilin biosynthesis point toward metabolic channeling. J. Biol. Chem. 281, 27081-27089. doi: 10.1074/jbc. M605154200
26. Dammeyer, T., and Frankenberg-Dinkel, N. (2008). Function and distribution of bilin biosynthesis enzymes in photosynthetic organisms. Photochem. Photobio. Sci. 7, 1121-1130. doi: 10.1039/b807209b
27. Davis, S. J., Vener, A. V., and Vierstra, R. D. (1999). Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria. Science 286, 2517-2520. doi: 10.1126/science.286.5449.2517
28. Derelle, E., Ferraz, C., Rombauts, S., Rouzé, P., Worden, A. Z., Robbens, S., et al. (2006). Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc. Natl. Acad. Sci. U.S.A. 103, 11647-11652. doi: 10.1073/pnas.0604795103
29. Duanmu, D., Bachy, C., Sudek, S., Wong, C.-H., Jimenez, V., Rockwell, N. C., et al. (2014). Marine algae and land plants share conserved phytochrome signaling systems. Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.1416751111. [Epub ahead of print]
30. Duanmu, D., Casero, D., Dent, R. M., Gallaher, S., Yang, W., Rockwell, N. C., et al. (2013). Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival. Proc. Natl. Acad. Sci. U.S.A. 110, 3621-3626. doi: 10.1073/pnas.1222375110
31. Facchinelli, F., Pribil, M., Oster, U., Ebert, N. J., Bhattacharya, D., Leister, D., et al. (2013). Proteomic analysis of the Cyanophora paradoxa muroplast provides clues on early events in plastid endosymbiosis. Planta 237, 637-651. doi: 10.1007/s00425-012-1819-3
32. Falkowski, P. G., Katz, M. E., Knoll, A. H., Quigg, A., Raven, J. A., Schofield, O., et al. (2004). The evolution of modern eukaryotic phytoplankton. Science 305, 354-360. doi: 10.1126/science.1095964
33. Frankenberg, N., Mukougawa, K., Kohchi, T., and Lagarias, J. C. (2001). Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 13, 965-978. doi: 10.1105/tpc.13.4.965
34. Franklin, K. A., and Quail, P. H. (2010). Phytochrome functions in Arabidopsis development. J. Exp. Bot. 61, 11-24. doi: 10.1093/jxb/erp304
35. Froehlich, A. C., Noh, B., Vierstra, R. D., Loros, J., and Dunlap, J. C. (2005). Genetic and molecular analysis of phytochromes from the filamentous fungus Neurospora crassa. Eukaryot. Cell 4, 2140-2152. doi: 10.1128/EC.4.12.2140-2152.2005
36. Gast, R. J., McKie-Krisberg, Z. M., Fay, S. A., Rose, J. M., and Sanders, R. W. (2014). Antarctic mixotrophic protist abundances by microscopy and molecular methods. FEMS Microbiol. Ecol. 89, 388-401. doi: 10.1111/1574-6941.12334
37. Giovagnetti, V., Flori, S., Tramontano, F., Lavaud, J., and Brunet, C. (2014). The velocity of light intensity increase modulates the photoprotective response in coastal diatoms. PLoS ONE 9:e103782. doi: 10.1371/journal.pone.0103782
38. Giraud, E., Fardoux, J., Fourrier, N., Hannibal, L., Genty, B., Bouyer, P., et al. (2002). Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 417, 202-205. doi: 10.1038/417202a
39. Glazer, A. N. (1988). Phycobiliproteins. Meth. Enz. 167, 291-303. doi: 10.1016/0076-6879(88)67034-0
40. Goss, R., and Lepetit, B. (2014). Biodiversity of NPQ. J. Plant Physiol. doi: 10.1016/j.jplph.2014.03.004. [Epub ahead of print]
41. Grant, J. R., and Katz, L. A. (2014). Building a phylogenomic pipeline for the eukaryotic tree of life-addressing deep phylogenies with genome-scale data. PLoS Curr. 2:6. doi: 10.1371/currents.tol.c24b6054aebf3602748ac042ccc8f2e9
42. Gross, J., and Bhattacharya, D. (2008). Revaluating the evolution of the Toc/Tic protein translocons. Trends Plant Sci. 14, 13-20. doi: 10.1016/j.tplants.2008.10.003
43. Gross, J., and Bhattacharya, D. (2009). Mitochondrial and plastid evolution in eukaryotes: an outsider's perspective. Nat. Rev. Genet. 10, 495-505. doi: 10.1038/nrg2610
44. Guillou, L., Chrétiennot-Dinet, M. J., Boulben, S., Moon-van der Staay, S. Y., and Vaulot, D. (1999). Symbiomonas scintillans gen. et sp. nov. and Picophagus flagellatus gen. et sp. nov. (Heterokonta): two new heterotrophic flagellates of picoplanktonic size. Protist. 150, 383-398. doi: 10.1016/S1434-4610(99)70040-4
45. Guillou, L., Jacquet, S., Chrétiennot-Dinet, M. J., and Vaulot, D. (2001). Grazing impact of two small heterotrophic flagellates on Prochlorococcus and Synechococcus. Aquat. Microb. Ecol. 26, 201-207. doi: 10.3354/ame026201
46. Hackett, J. D., Yoon, H. S., Li, S., Reyes-Prieto, A., Rümmele, S. E., and Bhattacharya, D. (2007). Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Mol. Biol. Evol. 24, 1702-1713. doi: 10.1093/molbev/msm089
47. Halliwell, B. (2006). Reactive species and antioxidants: Redox biology is a fundamental theme of aerobic life. Plant Physiol. 141, 312-322. doi: 10.1104/pp.106.077073
48. Hori, K., Maruyama, F., Fujisawa, T., Togashi, T., Yamamoto, N., Seo, M., et al. (2014). Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 5:3978. doi: 10.1038/ncomms4978
49. Hörtensteiner, S., and Kräutler, B. (2011). Chlorophyll breakdown in higher plants. Biochim. Biophys. Acta 1807, 977-988. doi: 10.1016/j.bbabio.2010.12.007
50. Hu, W., Su, Y.-S., and Lagarias, J. C. (2009). A light-independent allele of phytochrome B faithfully recapitulates photomorphogenic transcriptional networks. Mol. Plant 2, 166-182. doi: 10.1093/mp/ssn086
51. Huang, J., and Gogarten, J. P. (2007). Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol. 8:R99. doi: 10.1186/gb-2007-8-6-r99
52. Ikeuchi, M., and Ishizuka, T. (2008). Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem. Photobiol. Sci. 7, 1159-1167. doi: 10.1039/b802660m
53. Jarvis, P., and Soll, J. (2002). Toc, tic, and chloroplast protein import. Biochim. Biophys. Acta 1590, 177-189. doi: 10.1016/S0167-4889(02)00176-3
54. Jeong, H. J. (2011). Mixotrophy in red tide algae raphidophytes. J. Eukaryot. Microbiol. 58, 215-222. doi: 10.1111/j.1550-7408.2011.00550.x
55. Jeong, H. J., Yoo, Y. D., Kang, N. S., Lim, A. S., Seong, K. A., Lee, S. Y., et al. (2012). Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc. Natl. Acad. Sci. U.S.A. 109, 12604-12609. doi: 10.1073/pnas.1204302109
56. Jeong, H. J., Yoo, Y. D., Kim, J. S., Seong, K. A., Kang, N. S., and Kim, T. H. (2010). Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 45, 65-91. doi: 10.1007/s12601-010-0007-2
57. Jorissen, H., Braslavsky, S. E., Wagner, G., and Gärtner, W. (2002). Heterologous expression and characterization of recombinant phytochrome from the green alga Mougeotia scalaris. Photochem. Photobiol. 76, 457-461. doi: 10.1562/0031-8655(2002)076<0457:HEACOR>2.0.CO;2
58. Kalanon, M., and McFadden, G. I. (2008). The chloroplast protein translocation complexes of Chlamydomonas reinhardtii: a bioinformatic comparison of Toc and Tic components in plants, green algae and red algae. Genetics 179, 95-112. doi: 10.1534/genetics.107.085704
59. Keeling, P. J., Burki, F., Wilcox, H. M., Allam, B., Allen, E. E., Amaral-Zettler, L. A., et al. (2014). The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the Functional Diversity of Eukaryotic Life in the Oceans through Transcriptome Sequencing. PLoS Biol. 12:e1001889. doi: 10.1371/journal.pbio.1001889
60. Kidd, D. G., and Lagarias, J. C. (1990). Phytochrome from the green alga Mesotaenium caldariorum. Purification and preliminary characterization. J. Biol. Chem. 265, 7029-7035
61. Kim, K. M., Park, J. H., Bhattacharya, D., and Yoon, H. S. (2014). Applications of next-generation sequencing to unravelling the evolutionary history of algae. Int. J. Syst. Evol. Microbiol. 64, 333-345. doi: 10.1099/ijs.0.054221-0
62. Knoefler, D., Thamsen, M., Koniczek, M., Niemuth, N. J., Diederich, A. K., and Jakob, U. (2012). Quantitative in vivo redox sensors uncover oxidative stress as an early event in life. Mol. Cell. 47, 767-776. doi: 10.1016/j.molcel.2012.06.016
63. Kohchi, T., Mukougawa, K., Frankenberg, N., Masuda, M., Yokota, A., and Lagarias, J. C. (2001). The Arabidopsis HY2 gene encodes phytochromobilin synthase, a ferredoxin-dependent biliverdin reductase. Plant Cell 13, 425-436. doi: 10.1105/tpc.13.2.425
64. Lamparter, T., Carrascal, M., Michael, N., Martinez, E., Rottwinkel, G., and Abian, J. (2004). The biliverdin chromophore binds covalently to a conserved cysteine residue in the N-terminus of Agrobacterium phytochrome Agp1. Biochemistry 43, 3659-3669. doi: 10.1021/bi035693l
65. Lamparter, T., Michael, N., Caspani, O., Miyata, T., Shirai, K., and Inomata, K. (2003). Biliverdin binds covalently to Agrobacterium phytochrome Agp1 via its ring A vinyl side chain. J. Biol. Chem. 278, 33786-33792. doi: 10.1074/jbc. M305563200
66. Lemaux, P. G., and Grossman, A. R. (1985). Major light-harvesting polypeptides encoded in polycistronic transcripts in a eukaryotic alga. EMBO J. 4, 1911-1919
67. Li, L., and Lagarias, J. C. (1992). Phytochrome assembly-Defining chromophore structural requirements for covalent attachment and photoreversibility. J. Biol. Chem. 267, 19204-19210
68. Martin, W., and Herrmann, R. G. (1998). Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol. 118, 9-17. doi: 10.1104/pp.118.1.9
69. Martin, W., Rujan, T., Richly, E., Hansen, A., Cornelsen, S., Lins, T., et al. (2002). Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl. Acad. Sci. U.S.A. 99, 12246-12251. doi: 10.1073/pnas.182432999
70. Maruyama, S., and Kim, E. (2013). A modern descendant of early green algal phagotrophs. Curr. Biol. 23, 1081-1084. doi: 10.1016/j.cub.2013.04.063
71. McFadden, G. I., and van Dooren, G. G. (2004). Evolution: red algal genome affirms a common origin of all plastids. Curr. Biol. 14, R514-R516. doi: 10.1016/j.cub.2004.06.041
72. McKie-Krisberg, Z. M., and Sanders, R. W. (2014). Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans. ISME J. 8, 1953-1961. doi: 10.1038/ismej.2014.16
73. Moestrup, O., and Sengco, M. (2001). Ultrastructural Studies On Bigelowiella natans, Gen. et Sp. Nov., a Chlorarachniophyte Flagellate. J. Phycol. 37, 624-646. doi: 10.1046/j.1529-8817.2001.037004624.x
74. Moreau, H., Verhelst, B., Couloux, A., Derelle, E., Rombauts, S., Grimsley, N., et al. (2012). Gene functionalities and genome structure in Bathycoccus prasinos reflect cellular specializations at the base of the green lineage. Genome Biol. 13:R74. doi: 10.1186/gb-2012-13-8-r74
75. Moustafa, A., Reyes-Prieto, A., and Bhattacharya, D. (2008). Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions. PLoS ONE 3:e2205. doi: 10.1371/journal.pone.0002205
76. Nakamura, Y., Sasaki, N., Kobayashi, M., Ojima, N., Yasuike, M., Shigenobu, Y., et al. (2013). The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLoS ONE 8:e57122. doi: 10.1371/journal.pone.0057122
77. Niyogi, K. K., and Truong, T. B. (2013). Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr. Opin. Plant Biol. 16, 307-314. doi: 10.1016/j.pbi.2013.03.011
78. Nowack, E. C., Melkonian, M., and Glockner, G. (2008). Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr. Biol. 18, 410-418. doi: 10.1016/j.cub.2008.02.051
79. Nozaki, H., Takano, H., Misumi, O., Terasawa, K., Matsuzaki, M., Maruyama, S., et al. (2007). A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol. 5:28. doi: 10.1186/1741-7007-5-28
80. Okamoto, N., and Inouye, I. (2006). Hatena arenicola gen. et sp. nov., a katablepharid undergoing probable plastid acquisition. Protist 157, 401-419. doi: 10.1016/j.protis.2006.05.011
81. Palenik, B., Grimwood, J., Aerts, A., Rouzé, P., Salamov, A., Putnam, N., et al. (2007). The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc. Natl. Acad. Sci. U.S.A. 104, 7705-7710. doi: 10.1073/pnas.0611046104
82. Palmer, J. D. (2002). The symbiotic birth and spread of plastids: how many times and whodunit? J. Phycol. 39, 4-11. doi: 10.1046/j.1529-8817.2003.02185.x
83. Parfrey, L. W., Grant, J., Tekle, Y. I., Lasek-Nesselquist, E., Morrison, H. G., Sogin, M. L., et al. (2010). Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of life. Syst. Biol. 59, 518-533. doi: 10.1093/sysbio/syq037
84. Patron, N. J., Inagaki, Y., and Keeling, P. J. (2007). Multiple gene phylogenies support the monophyly of cryptomonad and haptophyte host lineages. Curr. Biol. 17, 887-891. doi: 10.1016/j.cub.2007.03.069
85. Pinevich, A., Velichko, N., and Ivanikova, N. (2012). Cyanobacteria of the genus Prochlorothrix. Front. Microbiol. 3:173. doi: 10.3389/fmicb.2012.00173
86. Pirone, C., Johnson, J. V., Quirke, J. M., Priestap, H. A., and Lee, D. (2010). Bilirubin present in diverse angiosperms. AoB Plants. 2010:plq020. doi: 10.1093/aobpla/plq020
87. Pirone, C., Quirke, J. M., Priestap, H. A., and Lee, D. W. (2009). Animal pigment bilirubin discovered in plants. J. Am. Chem. Soc. 131:2830. doi: 10.1021/ja809065g
88. Price, D. C., Chan, C. X., Yoon, H. S., Yang, E. C., Qiu, H., Weber, A. P., et al. (2012). Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335, 843-847. doi: 10.1126/science.1213561
89. Qiu, H., Price, D. C., Weber, A. P., Facchinelli, F., Yoon, H. S., and Bhattacharya, D. (2013a). Assessing the bacterial contribution to the plastid proteome. Trends Plant Sci. 18, 680-687. doi: 10.1016/j.tplants.2013.09.007
90. Qiu, H., Price, D. C., Weber, A. P., Reeb, V., Yang, E. C., Lee, J. M., et al. (2013c). Adaptation through horizontal gene transfer in the cryptoendolithic red alga Galdieria phlegrea. Curr. Biol. 23, R865-R866. doi: 10.1016/j.cub.2013.08.046
91. Qiu, H., Yoon, H. S., and Bhattacharya, D. (2013b). Algal endosymbionts as vectors of horizontal gene transfer in photosynthetic eukaryotes. Front. Plant Sci. 4:366. doi: 10.3389/fpls.2013.00366
92. Reumann, S., Inoue, K., and Keegstra, K. (2005). Evolution of the general protein import pathway of plastids (review). Mol. Membr. Biol. 22, 73-86. doi: 10.1080/09687860500041916
93. Reyes-Prieto, A., and Bhattacharya, D. (2007). Phylogeny of Calvin cycle enzymes supports Plantae monophyly. Mol. Phylogenet. Evol. 45, 384-391. doi: 10.1016/j.ympev.2007.02.026
94. Reyes-Prieto, A., Moustafa, A., and Bhattacharya, D. (2008). Multiple genes of apparent algal origin suggest ciliates may once have been photosynthetic. Curr. Biol. 18, 956-962. doi: 10.1016/j.cub.2008.05.042
95. Roberts, E.-C., and Laybourn-Parry, J. (1999). Mixotrophic cryptophytes and their predators in the Dry Valley lakes of Antarctica. Freshwater Biol. 41, 737-746. doi: 10.1046/j.1365-2427.1999.00401.x
96. Rockwell, N. C., Duanmu, D., Martin, S. S., Bachy, C., Price, D. C., Bhattacharya, D., et al. (2014). Eukaryotic algal phytochromes span the visible spectrum. Proc. Natl. Acad. Sci. U. S. A. 111, 3871-3876. doi: 10.1073/pnas.1401871111
97. Rockwell, N. C., and Lagarias, J. C. (2010). A brief history of phytochromes. ChemPhysChem. 11, 1172-1180. doi: 10.1002/cphc.200900894
98. Rockwell, N. C., Martin, S. S., Feoktistova, K., and Lagarias, J. C. (2011). Diverse two-cysteine photocycles in phytochromes and cyanobacteriochromes. Proc. Natl. Acad. Sci. U.S.A. 108, 11854-11859. doi: 10.1073/pnas.1107844108
99. Rockwell, N. C., Su, Y. S., and Lagarias, J. C. (2006). Phytochrome structure and signaling mechanisms. Annu. Rev. Plant Biol. 57, 837-858. doi: 10.1146/annurev.arplant.56.032604.144208
100. Rodríguez-Ezpeleta, N., Brinkmann, H., Burey, S. C., Roure, B., Burger, G., Löffelhardt, W., et al. (2005). Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr. Biol. 15, 1325-1330. doi: 10.1016/j.cub.2005.06.040
101. Röhrig, J., Kastner, C., and Fischer, R. (2013). Light inhibits spore germination through phytochrome in Aspergillus nidulans. Curr. Genet. 59, 55-62. doi: 10.1007/s00294-013-0387-9
102. Schluchter, W. M., and Glazer, A. N. (1997). Characterization of cyanobacterial biliverdin reductase. Conversion of biliverdin to bilirubin is important for normal phycobiliprotein biosynthesis. J. Biol. Chem. 272, 13562-13569. doi: 10.1074/jbc.272.21.13562
103. Schmitz-Esser, S., Toenshoff, E. R., Haider, S., Heinz, E., Hoenninger, V. M., Wagner, M., et al. (2008). Diversity of bacterial endosymbionts of environmental acanthamoeba isolates. Appl. Environ. Microbiol. 74, 5822-5831 doi: 10.1128/AEM.01093-08
104. Schönknecht, G., Chen, W. H., Ternes, C. M., Barbier, G. G., Shrestha, R. P., Stanke, M., et al. (2013). Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339, 1207-1210. doi: 10.1126/science.1231707
105. Shi, L. X., and Theg, S. M. (2013). The chloroplast protein import system: from algae to trees. Biochim. Biophys. Acta 1833, 314-331. doi: 10.1016/j.bbamcr.2012.10.002
106. Song, C., Psakis, G., Kopycki, J., Lang, C., Matysik, J., and Hughes, J. (2014). The D-ring, not the A-ring, rotates in Synechococcus OS-B' phytochrome. J. Biol. Chem. 289, 2552-2562. doi: 10.1074/jbc. M113.520031
107. Song, C., Psakis, G., Lang, C., Mailliet, J., Gärtner, W., Hughes, J., et al. (2011). Two ground state isoforms and a chromophore D-ring photoflip triggering extensive intramolecular changes in a canonical phytochrome. Proc. Natl. Acad. Sci. U.S.A. 108, 3842-3847. doi: 10.1073/pnas.1013377108
108. Stegemann, S., Hartmann, S., Ruf, S., and Bock, R. (2003). High-frequency gene transfer from the chloroplast genome to the nucleus. Proc. Natl. Acad. Sci. U.S.A. 100, 8828-8833. doi: 10.1073/pnas.1430924100
109. Stiller, J. W. (2007). Plastid endosymbiosis, genome evolution and the origin of green plants. Trends Plant Sci. 12, 391-396. doi: 10.1016/j.tplants.2007.08.002
110. Stocker, R. (2004). Antioxidant activities of bile pigments. Antioxid. Redox Signal. 6, 841-849. doi: 10.1089/ars.2004.6.841
111. Stoecker, D. K., Li, A., Coats, D. W., Gustafson, D. E., and Nannen, M. K. (1997). Mixotrophy in the dinoflagellate Prorocentrum minimum. Mar. Ecol. Prog. Ser. 152, 1-12. doi: 10.3354/meps152001
112. Süssenbacher, I., Christ, B., Hörtensteiner, S., and Kräutler, B. (2014). Hydroxymethylated phyllobilins: a puzzling new feature of the dioxobilin branch of chlorophyll breakdown. Chemistry 20, 87-92. doi: 10.1002/chem.201303398
113. Timme, R. E., Bachvaroff, T. R., and Delwiche, C. F. (2012). Broad phylogenomic sampling and the sister lineage of land plants. PLoS ONE 7:e29696. doi: 10.1371/journal.pone.0029696
114. Timmis, J. N., Ayliffe, M. A., Huang, C. Y., and Martin, W. (2004). Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5, 123-135. doi: 10.1038/nrg1271
115. Unrein, F., Gasol, J. M., Not, F., Forn, I., and Massana, R. (2014). Mixotrophic haptophytes are key bacterial grazers in oligotrophic coastal waters. ISME J. 8, 164-176. doi: 10.1038/ismej.2013.132
116. Van Donk, E., Cerbin, S., Wilken, S., Helmsing, N. R., Ptacnik, R., and Verschoor, A. M. (2009). The effect of a mixotrophic chrysophyte on toxic and colony-forming cyanobacteria. Freshwater Biol. 54, 1843-1855. doi: 10.1111/j.1365-2427.2009.02227.x
117. Weber, A. P., Linka, M., and Bhattacharya, D. (2006). Single, ancient origin of a plastid metabolite translocator family in Plantae from an endomembrane-derived ancestor. Eukaryot. Cell 5, 609-612. doi: 10.1128/EC.5.3.609-612.2006
118. Wegele, R., Tasler, R., Zeng, Y., Rivera, M., and Frankenberg-Dinkel, N. (2004). The heme oxygenase(s)-phytochrome system of Pseudomonas aeruginosa. J. Biol. Chem. 279, 45791-45802. doi: 10.1074/jbc. M408303200
119. Worden, A. Z., Lee, J. H., Mock, T., Rouzé, P., Simmons, M. P., Aerts, A. L., et al. (2009). Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324, 268-272. doi: 10.1126/science.1167222
120. Wu, S. H., McDowell, M. T., and Lagarias, J. C. (1997). Phycocyanobilin is the natural precursor of the phytochrome chromophore in the green alga Mesotaenium caldariorum. J. Biol. Chem. 272, 25700-25705. doi: 10.1074/jbc.272.41.25700
121. Yamaguchi, A., Yubuki, N., and Leander, B. S. (2012). Morphostasis in a novel eukaryote illuminates the evolutionary transition from phagotrophy to phototrophy: description of Rapaza viridis n. gen. et sp. (Euglenozoa, Euglenida). BMC Evol. Biol. 12:29. doi: 10.1186/1471-2148-12-29
122. Yamaguchi, H., Nakayama, T., Hongoh, Y., Kawachi, M., and Inouye, I. (2014). Molecular diversity of endosymbiotic Nephroselmis (Nephroselmidophyceae) in Hatena arenicola (Katablepharidophycota). J. Plant Res. 127, 241-247. doi: 10.1007/s10265-013-0591-1
123. Yang, X., Ren, Z., Kuk, J., and Moffat, K. (2011). Temperature-scan cryocrystallography reveals reaction intermediates in bacteriophytochrome. Nature 479, 428-432. doi: 10.1038/nature10506
124. Yeh, K.-C., Wu, S.-H., Murphy, J. T., and Lagarias, J. C. (1997). A cyanobacterial phytochrome two-component light sensory system. Science 277, 1505-1508. doi: 10.1126/science.277.5331.1505
125. Yoon, H. S., Yang, E. C., Qiu, H., and Bhattacharya, D. (2014). "Photosynthetic Paulinella: recapitulation of primary plastid establishment". in Endosymbiosis, ed W. Löffelhardt (Vienna: Springer), 151-166