The making of a photosynthetic animal

Journal of Experimental Biology

Volumn 214, Issue 2, 2011, Pages 303-311

  Rumpho, Mary E ^a   Pelletreau, Karen N ^a   Moustafa, Ahmed ^b   Bhattacharya, Debashish ^c  

^a UNIVERSITY OF MAINE   (United States)

^b The American University in Cairo   (Egypt)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

Elysia chlorotica; Horizontal gene transfer; Mollusc; Photosynthesis; Plastid; Sea slug; Symbiosis; Vaucheria litorea

Indexed keywords

ANIMAL; ARTICLE; EVOLUTION; GENE EXPRESSION PROFILING; GENETICS; GREEN ALGA; HORIZONTAL GENE TRANSFER; METABOLISM; MOLLUSC; PHOTOSYNTHESIS; PLASTID; SYMBIOSIS;

ANIMALS; BIOLOGICAL EVOLUTION; CHLOROPHYTA; GENE EXPRESSION PROFILING; GENE TRANSFER, HORIZONTAL; MOLLUSCA; PHOTOSYNTHESIS; PLASTIDS; SYMBIOSIS;

ALGAE; ANIMALIA; ELYSIA CHLOROTICA; MOLLUSCA; OPISTHOBRANCHIA; VAUCHERIA LITOREA;

EID: 78651315893     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.046540     Document Type: Article

References (113)

1. Adam, Z. and Clarke, A. K. (2002). Cutting edge of chloroplast proteolysis. Trends Plant Sci. 7, 451-456.
2. Adl, S. M., Simpson, A. G. B., Farmer, M. A., Andersen, R. A., Anderson, O. R., Barta, J. R., Bowser, S. S., Brugerolle, G., Fensome, R. A., Fredericq, S. et al. (2005). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52, 399-451.
3. Akiba, T., Koyama, K., Ishiki, Y., Kimura, S. and Fukushima, T. (1960). On the mechanism of the development of multiple-drug-resistant clones of Shigella. Jpn. J. Microbiol. 4, 219-227.
4. Andersen, R. A. (2004). Biology and systematics of heterokont and haptophyte algae. Am. J. Bot 91, 1508-1522.
5. Andersson, J. O. (2005). Lateral gene transfer in eukaryotes. Cell. Mol. Life Sci. 62, 1182-1197.
6. Archibald, J. M., Rogers, M. B., Toop, M., Ishida, K. and Keeling, P. J. (2003). Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc. Natl. Acad. Sci. USA 100, 7678-7683.
7. Armbrust, E. V., Berges, J. A., Bowler, C., Green, B. R., Martinez, D., Putnam, N. H., Zhou, S. G., Allen, A. E., Apt, K. E., Bechner, M. et al. (2004). The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306, 79-86.
8. Aro, E., Virgin, I. and Andersson, B. (1993). Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143, 113-134.
9. Aro, E. M., Suorsa, M., Rokka, A., Allahverdiyeva, Y., Paakkarinen, V., Saleem, A., Battchikova, N. and Rintamaki, E. (2005). Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J. Exp. Bot. 56, 347-356.
10. Beagley, C. T., Okada, N. A. and Wolstenholme, D. R. (1996). Two mitochondrial group I introns in a metazoan, the sea anemone Metridium senile: one intron contains genes for subunits 1 and 3 of NADH dehydrogenase. Proc. Natl. Acad. Sci. USA 93, 5619-5623.
11. Bhattacharya, D. and Medlin, L. (1995). The phylogeny of plastids: A review based on comparisons of small subunit ribosomal RNA coding regions. J. Phycol. 31, 489-498.
12. Bhattacharya, D. and Nosenko, T. (2008). Endosymbiotic and horizontal gene transfer in chromalveolates. J. Phycol. 44, 7-10.
13. Bhattacharya, D., Yoon, H. W. and Hackett, J. D. (2004). Photosynthetic eukaryotes unite: endosymbiosis connects the dots. BioEssays 26, 50-60.
14. Biehl, A., Richly, E., Noutsos, C., Salamini, F. and Leister, D. (2005). Analysis of 101 nuclear transcriptomes reveals 23 distinct regulons and their relationship to metabolism, chromosomal gene distribution and co-ordination of nuclear and plastid gene expression. Gene 344, 33-41.
15. Bock, R. (2010). The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci. 15, 11-22.
16. Bock, R. and Timmis, J. N. (2008). Reconstructing evolution: gene transfer from plastids to the nucleus. BioEssays 30, 556-566.
17. Bowler, C., Allen, A. E., Badger, J. H., Grimwood, J., Jabbari, K., Kuo, A., Maheswari, U., Martens, C., Maumus, F., Otillar, R. P. et al. (2008). The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239-244.
18. Brandt, K. (1883). Über die morphologische und physiologische bedeutung des chlorophylls bei tieren. Mit. Zool. Stn. Neapel. 4, 191-302.
19. Carlsson, J., Lagercrantz, U., Sundstrorm, J., Teixeira, R., Wellmer, F., Meyerowitz, E. M. and Glimelius, K. (2007). Microarray analysis reveals altered expression of a large number of nuclear genes in developing cytoplasmic male sterile Brassica napus flowers. Plant J. 49, 452-462.
20. Clark, K. B. and Busacca, M. (1978). Feeding specificity and chloroplast retention in 4 tropical ascoglossa, with a discussion of the extent of chloroplast symbiosis and the evolution of the order. J. Moll. Stud. 44, 272-282.
21. Clark, K. B., Jensen, K. R. and Stirts, H. M. (1990). Survey for functional kleptoplasty among West Atlantic Ascoglossa (=Sacoglossa) (Mollusca, Opisthobranchia). Veliger 33, 339-345.
22. De La Cruz, F. and Davies, J. (2000). Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol. 8, 128-133.
23. De Negri, A. and De Negri, G. (1876). Farbstoff aus Elysia viridis. Ber. Deut. Chem. Gesellsch. 9, 84.
24. Erwin, P. M. and Thacker, R. W. (2008). Phototrophic nutrition and symbiont diversity of two Caribbean sponge-cyanobacteria symbioses. Mar. Ecol. Prog. Ser. 362, 139-147.
25. Falkowski, P. G., Katz, M. E., Knoll, A. H., Quigg, A., Raven, J. A., Schofield, O. and Taylor, F. J. R. (2004). The evolution of modern eukaryotic phytoplankton. Science 305, 354-360.
26. Friesen, T. L., Stukenbrock, E. H., Liu, Z. H., Meinhardt, S., Ling, H., Faris, J. D., Rasmussen, J. B., Solomon, P. S., McDonald, B. A. and Oliver, R. P. (2006). Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38, 953-956.
27. Gelvin, S. B. (2009). Agrobacterium in the genomics age. Plant Physiol. 150, 1665-1676.
28. Gibbs, S. P. (1993). The evolution of algal chloroplasts. In Origins of Plastids (ed. R. A. Lewin), pp. 107-121. New York: Chapman and Hall.
29. Gibson, G. D., Toews, D. P. and Bleakney, J. S. (1986). Oxygen production and consumption in the sacoglossan (=ascoglossan) Elysia chlorotica Gould. Veliger 28, 397-400.
30. Gladyshev, E. and Meselson, M. (2008). Extreme resistance of bdelloid rotifers to ionizing radiation. Proc. Natl. Acad. Sci. USA 105, 5139-5144.
31. Graves, D. A., Gibson, M. A. and Bleakney, J. S. (1979). Digestive diverticula of Alderia modesta and Elysia chlorotica (Opisthobranchia, Sacoglossa). Veliger 21, 415-422.
32. Gray, M., Burger, G. and Lang, B. F. (2001). The origin and early evolution of mitochondria. Genome Biol. Rev. 2, 1018.1-1018.5.
33. Green, B. J., Li, W.-Y., Manhart, J. R., Fox, T. C., Summer, E. J., Kennedy, R. A., Pierce, S. K. and Rumpho, M. E. (2000). Mollusc-algal chloroplast endosymbiosis: photosynthesis, thylakoid protein maintenance, and chloroplast gene expression continue for many months in the absence of the algal nucleus. Plant Physiol. 124, 331-342.
34. Green, B. J., Fox, T. C., Manhart, J. R. and Rumpho, M. E. (2005). Stability of isolated chromophytic algal chloroplasts that participate in a unique molluscan/algal endosymbiosis. Symbiosis 40, 31-40.
35. Greene, R. W. and Muscatine, L. (1972). Symbiosis in sacoglossan opisthobranchs - photosynthetic products of animal-chloroplast associations. Mar. Biol. 14, 253-259.
36. Händeler, K., Grzymbowski, Y. P., Krug, P. K. and Wagele, H. (2009). Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life. Front. Zool. 6, 1-18.
37. Heinemann, J. A. and Kurenbach, B. (2009). Horizontal transfer of genes between microorganisms. In Encyclopedia of Microbiology, 3rd edn (ed. M. Schaechter). New York: Academic Press.
38. Hinde, R. (1980). Chloroplasts "symbiosis" in sacoglossan molluscs. In Endocytobiology: Endosymbiosis and Cell Biology, a Synthesis of Recent Research (ed. W. Schwemmler and H. E. A. Schenk), pp. 729-736. Berlin: Walter de Gruyter.
39. Hinde, R. and Smith, D. C. (1972). Persistence of functional chloroplast in Elysia viridis (Opisthobranchia, Sacoglossa). Nat. New Biol. 239, 30-31.
40. Hinde, R. and Smith, D. C. (1974). "Chloroplast symbiosis" and extent to which it occurs in Sacoglossa (Gastropoda, Mollusca). Biol. J. Linn. Soc. 6, 349-356.
41. Hooge, M. D. and Tyler, S. (2008). Acoela (Acoelomorpha) from Bocas del Toro, Panama. Zootaxa 1719, 1-40.
42. Jensen, K. R. (1986). Observations on copulation in two species of Elysia from Florida (Opisthobranchi, Ascoglossa). Ophelia 25, 25-32.
43. Kawaguti, S. and Yamasu, T. (1965). Electron microscopy on the symbiosis between an elysioid gastropod and chloroplasts from a green alga. Biol. J. Okayama Univ. II, 57-64.
44. Keeling, P. J. (2004). Diversity and evolutionary history of plastids and their hosts. Am. J. Bot. 91, 1481-1493.
45. Keeling, P. J. (2009). Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr. Opin. Genet. Dev. 19, 613-619.
46. Klasson, L., Kambris, Z., Cook, P. E., Walker, T. and Sinkins, S. P. (2009). Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti. BMC Genomics 10, 33.
47. Kondo, N., Nikoh, N., Ijichi, N., Shimada, M. and Fukatsu, T. (2002). Genome fragment of Wolbachiaendosymbiont transferred to X chromosome of host insect. Proc. Natl. Acad. Sci. USA 99, 14280-14285.
48. Koonin, E. V., Makarova, K. S. and Aravind, L. (2001). Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol. 55, 709-742.
49. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., et al. (2001). Initial sequencing and analysis of the human genome. Nature 409, 860-921.
50. Lane, C. E. and Archibald, J. M. (2008). The eukaryotic tree of life: endosymbiosis takes its TOL. Trends Ecol. Evol. 23, 268-275.
51. Lavrov, D. V. (2007). Key transitions in animal evolution: a mitochondrial DNA perspective. Integr. Comp. Biol. 47, 734-743.
52. Lee, R. E. (2008). Heterokontophyta, Xanthophyceae. In Phycology (ed. R. E. Lee), pp. 413-423. Cambridge: Cambridge University Press.
53. Loftus, B., Anderson, I., Davies, R., Alsmark, U. C. M., Samuelson, J., Amedeo, P., Roncaglia, P., Berriman, M., Hirt, R. P., Mann, B. J. et al. (2005). The genome of the protist parasite Entamoeba histolytica. Nature 433, 865-868.
54. Mann, N. H., Cook, A., Millard, A., Bailey, S. and Clokie, M. (2003). Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424, 741.
55. Marchetti, A., Parker, M. S., Moccia, L. P., Lin, E. O., Arrieta, A. L., Ribalet, F., Murphy, M. E., Maldonado, M. T. and Armbrust, E. V. (2009). Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 457, 467-470.
56. Martin, W., Rujan, T., Richly, E., Hansen, A., Cornelsen, S., Lins, T., Leister, D., Stoebe, B., Hasegawa, M. and Penny, D. (2002). Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl. Acad. Sci. USA 99, 12246-12251.
57. McFadden, G. I. (2001). Primary and secondary endosymbiosis and the origin of plastids. J. Phycol. 37, 951-959.
58. Meeks, J. C., Elhai, J., Thiel, T., Potts, M., Larimer, F., Lamerdin, J., Predki, P. and Atlas, R. (2001). An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosyn. Res. 70, 85-106.
59. Moran, N. A. and Jarvik, T. (2010). Lateral transfer of genes from fungi underlies carotenoids production in aphids. Science 328, 624-627.
60. Moustafa, A. and Bhattacharya, D. (2008). PhyloSort: a user-friendly phylogenetic sorting tool and its application to estimating the cyanobacterial contribution to the nuclear genome of Chlamydomonas. BMC Evol. Biol. 8, 6.
61. Moustafa, A., Chan, C., Danforth, M., Zear, D., Ahmed, H., Jadhav, N., Savage, T. and Bhattacharya, D. (2008a). A phylogenomic approach for studying plastid endosymbiosis. Gen. Inform. Intern. Conf. Genome Inform. 21, 165-176.
62. Moustafa, A., Reyes-Prieto, A. and Bhattacharya, D. (2008b). Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions. PLoS ONE 3, e2205.
63. Moustafa, A., Beszteri, B., Maier, U. G., Bowler, C., Valentin, K. and Bhattacharya, D. (2009). Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324, 1724-1726.
64. Muscatine, L., Pool, R. R. and Trech, R. K. (1975). Symbiosis of algae and invertebrates - aspects of symbiont surface and host-symbiont interface. Trans. Am. Microsc. Soc. 94, 450-469.
65. Nelson, N. and Yocum, C. F. (2006). Structure and function of photosystems I and II. Annu. Rev. Plant Biol. 57, 521-565.
66. Nikoh, N., Tanaka, K., Shibata, F., Kondo, N., Hizume, M., Shimada, M. and Fukatsu, T. (2008). Wolbachia genome integrated in an insect chromosome: Evolution and fate of laterally transferred endosymbiont genes. Gen. Res. 18, 272-280.
67. Norton, J. H., Shepherd, M. A., Long, H. M. and Fitt, W. K. (1992). Zooxanthellal tubular system in the giant clam. Biol. Bull. 183, 503-506.
68. Nosenko, T. and Bhattacharya, D. (2007). Horizontal gene transfer in chromalveolates. BMC Evol. Biol. 7, 173.
69. Pierce, S. K., Biron, R. W. and Rumpho, M. E. (1996). Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J. Exp. Biol. 199, 2323-2330.
70. Pierce, S. K., Curtis, N. E., Hanten, J. J., Boerner, S. L. and Schwartz, J. A. (2007). Transfer, integration and expression of functional nuclear genes between multicellular species. Symbiosis 43, 57-64.
71. Pierce, S. K., Curtis, N. E. and Schwartz, J. A. (2009). Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis 49, 121-131.
72. Raghavendra, A. S. (1998). Photosynthesis. A Comprehensive Treatise. Cambridge: Cambridge University Press.
73. Raven, J. A., Beardall, J., Flynn, K. and Maberly, S. (2009). Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: relation to Darwin's insectivorous plants. J. Exp. Bot. 60, 3975-3987.
74. Reyes-Prieto, A., Weber, A. P. M. and Bhattacharya, D. (2007). The origin and establishment of the plastid in algae and plants. Annu. Rev. Genet. 41, 147-168.
75. Richards, T. A., Soanes, D. M., Foster, P. G., Leonard, G., Thornton, C. R. and Talbot, N. J. (2009). Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell 21, 1897-1911.
76. Richardson, A. O. and Palmer, J. D. (2007). Horizontal gene transfer in plants. J. Exp. Bot. 58, 1-9.
77. Richly, E. and Leister, D. (2004). An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329, 11-16.
78. Rocap, G., Larimer, F. W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N. A., Arellano, A., Coleman, M., Hauser, L. and Hess, W. R. (2003). Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424, 1042-1047.
79. Roelofs, J. and Van Haastert, P. J. M. (2001). Genomics: genes lost during evolution. Nature 411, 1013-1014.
80. Rot, C., Goldfarb, I., Ilan, M. and Huchon, D. (2006). Putative cross-kingdom horizontal gene transfer in sponge (Porifera) mitochondria. BMC Evol. Biol. 6, 71.
81. Rumpho, M. E., Summer, E. J. and Manhart, J. R. (2000). Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol. 123, 29-38.
82. Rumpho, M. E., Summer, E. J., Green, B. J., Fox, T. C. and Manhart, J. R. (2001). Mollusc/algal chloroplast symbiosis: how can isolated chloroplasts continue to function for months in the cytosol of a sea slug in the absence of an algal nucleus? Zoology 104, 303-312.
83. Rumpho, M. E., Dastoor, F. P., Manhart, J. R. and Lee, J. (2006). The Kleptoplast. In Advances in Photosynthesis and Respiration - the Structure and Function of Plastids, Vol. 23 (ed. R. R. Wise and J. K. Hoober), pp. 451-473. New York: Springer.
84. Rumpho, M. E., Worful, J. M., Lee, J., Kannan, K., Tyler, M. S., Bhattacharya, D., Moustafa, A. and Manhart, J. R. (2008). Horizontal gene transfer of the algal nuclear gene psbOto the photosynthetic sea slug Elysia chlorotica. Proc. Natl. Acad. Sci. USA 105, 17867-17871.
85. Rumpho, M. E., Pochareddy, S., Worful, J. M., Summer, E. J., Bhattacharya, D., Pelletreau, K. N., Tyler, M. S., Lee, J., Manhart, J. R. and Soule, K. M. (2009). Molecular characterization of the Calvin cycle enzyme phosphoribulokinase in the stramenopile alga Vaucheria litorea and the plastid hosting mollusc Elysia chlorotica. Mol. Plant 2, 1384-1396.
86. Sakamoto, W. (2006). Protein degradation machineries in plastids. Annu. Rev. Plant Biol. 57, 599-621.
87. Salzberg, S. L., White, O., Peterson, J. and Eisen, J. A. (2001). Microbial genes in the human genome: lateral transfer or gene loss? Science 292, 1903-1906.
88. Sánchez-Puerta, M. V. and Delwiche, C. F. (2008). A hypothesis for plastid evolution in chromalveolates. J. Phycol. 44, 1097-1107.
89. Sanders, I. R. (2006). Rapid disease emergence through horizontal gene transfer between eukaryotes. Trends Ecol. Evol. 21, 656-658.
90. Schwartz, J. A., Curtis, N. E. and Pierce, S. K. (2010). Using algal transcriptome sequences to identify transferred genes in the sea slug, Elysia chlorotica. Evol. Biol. 37, 29-37.
91. Soule, K. M. (2009). Light-regulated photosynthetic gene expression and enzyme activity in the heterokont alga Vaucheria litoreaand its symbiotic partner the sacoglossan mollusc Elysia chlorotica. MSc thesis. University of Maine.
92. Starcevic, A., Akthar, S., Dunlap, W. C., Shick, J. M., Hranueli, D., Cullum, J. and Long, P. F. (2008). Enzymes of the shikimic acid pathway encoded in the genome of a basal metazoan, Nematostella vectensis, have microbial origins. Proc. Natl. Acad. Sci. USA 105, 2533-2537.
93. Stegemann, S. and Bock, R. (2009). Exchange of genetic material between cells in plant tissue grafts. Science 324, 649-651.
94. Sullivan, M. B., Coleman, M. L., Weigele, P., Rohwer, F. and Chisholm, S. W. (2005). Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol. 3, e144.
95. Trench, R. K. (1969). Chloroplasts as functional endosymbionts in the mollusc Tridachnia crispata (Bërgh), (Opisthobranchia, Sacoglossa). Nature 222, 1071-1072.
96. Trench, R. K. (1975). Of 'leaves that crawl': functional chloroplasts in animal cells. In Symposia of the Society for Experimental Biology (ed. D. H. Jennings), pp. 229-265. London: Cambridge University Press.
97. Trench, R. K. (1993). Microalgal-invertebrate symbiosis: a review. Endocyt. Cell Res. 9, 135-175.
98. Trench, R. K., Greene, R. W. and Bystrom, B. G. (1969). Chloroplasts as functional organelles in animal tissues. J. Cell Biol. 42, 404-417.
99. Trench, R. K., Trench, M. E. and Muscatine, L. (1972). Symbiotic chloroplasts - their photosynthetic products and contribution to mucus synthesis in two marine slugs. Biol. Bull. 142, 335-349.
100. Trench, R. K., Boyle, E. J. and Smith, D. C. (1973a). The association between chloroplasts of Codium fragileand the mollusc Elysia viridis. I. Characteristics of isolated Codium chloroplasts. Proc. R. Soc. Lond. B Biol. Sci. 184, 51-61.
101. Trench, R. K., Boyle, E. J. and Smith, D. C. (1973b). Association between chloroplasts of Codium fragileand the mollusc Elysia viridis. II. Chloroplast ultrastructure and photosynthetic carbon fixation in Elysia viridis. Proc. R. Soc. Lond. 184, 63-81.
102. van Oppen, M. J. H., Catmull, J., McDonald, B. J., Hislop, N. R., Hagerman, P. J. and Miller, D. J. (2002). The mitochondrial genome of Acropora tenuis (Cnidaria: Scleractinia) contains a large group I intron and a candidate control region. J. Mol. Evol. 55, 1-13.
103. Venn, A. A., Loram, J. E. and Dougalas, A. E. (2008). Photosynthetic symbiosis in animals. J. Exp. Bot. 59, 1069-1080.
104. Voolstra, C. R., Schwarz, J. A., Schnetzer, J., Sunagawa, S., Desalvo, M. K., Szmant, A. M., Coffroth, M. A. and Medina, M. (2009). The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Mol. Ecol. 1, 1823-1833.
105. Wägele, H., Deusch, O., Händeler, K., Martin, R., Schmitt, V., Christa, G., Pinzger, B., Gould, S. B., Dagan, T., Klussmann-Kolb, A. and Martin, W. (2010). Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timidaand Plakobrachus ocellatusdoes not entail lateral transfer of algal nuclear genes. Mol. Biol. Evol. doo: 10.1093/molbev/msq239.
106. Wasmuth, J., Schmid, R., Hedley, A. and Blaxter, M. (2008). On the extent and origins of genetic novelty in the phylum nematoda. PLoS Negl. Trop. Dis. 2, e258.
107. West, H. H. (1979). Chloroplast symbiosis and development of the ascoglossan opistobranch Elysia chlorotica. PhD thesis, Northeastern University, Boston, MA.
108. West, H. H., Harrigan, J. and Pierce, S. K. (1984). Hybridization of two populations of a marine opistobranch with different development patterns. Veliger 26, 199-206.
109. Willerslev, E., Mourier, T., Hansen, A. J., Christensen, B., Barnes, I. and Salzberg, S. L. (2002). Contamination in the draft of the human genome masquerades as lateral gene transfer. DNA Seq. 13, 75-76.
110. Williamson, S. J., Rusch, D. B., Yooseph, S., Halpern, A. L., Heidelberg, K. B., Glass, J. I., Andrews-Pfannkoch, C., Fadrosh, D., Miller, C. S., Sutton, G. et al. (2008). The sorcerer II global ocean sampling expedition: metagenomic characterization of viruses within aquatic microbial samples. PLoS ONE 3, e1456.
111. Woolfit, M., Iturbe-Ormaetxe, I., McGraw, E. A. and O'Neill, S. L. (2009). An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis. Mol. Biol. Evol. 26, 367-374.
112. Yellowlees, D., Rees, T. and Leggat, W. (2008). Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ. 31, 679-694.
113. Yoon, H. S., Hackett, J. D., Van Dolah, F. M., Nosenko, T., Lidie, K. L. and Bhattacharya, D. (2005). Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol. Biol. Evol. 22, 1299-1308.