Microenvironmental ecology of the chlorophyll b-containing symbiotic cyanobacterium Prochloron in the didemnid ascidian Lissoclinum patella

Frontiers in Microbiology

Volumn 3, Issue NOV, 2012, Pages

  Kühl, Michael ^a,b,c   Behrendt, Lars ^a   Trampe, Erik ^a   Qvortrup, Klaus ^a   Schreiber, Ulrich ^d   Borisov, Sergey M ^e   Klimant, Ingo ^e   Larkum, Anthony W D ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Bioimaging; Didemnid ascidian; Lissoclinum patella; Microenvironment; Microsensor; Photobiology; Prochloron; Symbiosis

Indexed keywords

EID: 84875905851     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00402     Document Type: Article

References (114)

1. Adams, D. G. (2000). "Symbiotic interactions," in The Ecology of Cyanobacteria, eds B. A. Whitton and M. Potts (Dordrecht: Kluwer Academic publishers), 563-561.
2. Alberte, R. S., Cheng, L., and Lewin, R. A. (1987). Characteristics of Prochloron/ascidian symbioses. II.Photosynthesis-irradiance relationships and carbon balance of associations from Palau, Micronesia. Symbiosis 4, 147-170.
3. Badger, M. R., Hanson, D., and Price, G. D. (2002). Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Funct. Plant Biol. 29, 161-173.
4. Behrendt, L., Larkum, A. W. D., Trampe, E., Norman, A., Sørensen, S. J., and Kühl, M. (2012a). Microbial diversity of biofilm communities in microniches associated with the didemnid ascidian Lissoclinum patella. ISME J. 6, 1222-1237.
5. Behrendt, L., Schrameyer, V., Qvortrup, K., Lundin, L., Sørensen, S. J., Larkum, A. W. D., et al. (2012b). Biofilm growth and near infrared radiation-driven photosynthesis of the chlorophyll d-containing cyanobacteriumAcaryochloris marina. Appl. Environ. Microbiol. 78, 3896-3904.
6. Behrendt, L., Trampe, E., Larkum, A. W. D., Qvortrup, K., Norman, A., Chen, M., et al. (2011). Endolithic chlorophyll d-containing cyanobacteria. ISMEJ. 5,1072-1076.
7. Bibby, T., Nield, J., Chen, M., Larkum, A. W. D., and Barber, J. (2003). Structure of a photosystem II super-complex isolated from Prochloron, retaining its chlorophyll a/b light-harvesting system. Proc. Natl. Acad. Sci. U.S.A. 100, 9050-9054.
8. Borisov, S. M., Nuss, G., Haas, W., Saf, R., Schmuck, M., and Klimant, I. (2009a). Photophysical properties of the new phosphorescent platinum(II) and palladium(II) complexes of benzoporphyrins and chlorines. J. Photochem. Photobiol A Chem.201, 128-135.
9. Borisov, S. M., Herrod, D. L., and Klimant, I. (2009b). Fluorescent poly(styrene-block-vinylpyrrolidone)nanobeads for optical sensing of pH. Sens. Actuators B Chem. 139, 52-58.
10. Borisov, S. M., Nuss, G., and Klimant, I. (2008). Red light-excitable oxygen sensing materials based on platinum(II) and palladium(II) benzoporphyrins. Anal. Chem. 80, 9435-9442.
11. Bothe, H., Tripp, H. J., and Zehr, J. P. (2010). Unicellular cyanobacteria with a new mode of life: the lack of photosynthetic oxygen evolution allows nitrogen fixation to proceed. Arch. Microbiol. 192, 783-790.
12. Brümmer, F., Pfannkuchen, M., Baltz, A., Hauser, T., and Thiel, V. (2008). Light inside sponges. J. Exp. Mar. Biol.Ecol. 367,61-64.
13. Burns, B. P., Goh, F., Allen, M., and Neilan,B. A. (2004). Microbial diversity of extant stromatolites in the hypersaline marine environment of Shark Bay, Australia. Environ. Microbiol. 6, 1096-1101.
14. Chen, M., Hiller, R. G., Howe, C. J., and Larkum, A. W. D. (2005). Unique origin and lateral transfer of prokaryotic chlorophyll b and chlorophyll d light-harvesting systems. Mol. Biol. Evol. 22, 21-28.
15. Chen, M., Schliep, M., Willows, R. D., Cai, Z.-L., Neilan, B. A., and Scheer, H. (2010). A red-shifted chlorophyll. Science 329, 1318-1319.
16. Cheng, L., and Lewin, R. A. (1984). Prochloron on Synaptula. Bull. Mar. Sci. 35, 95-98.
17. Cox, G. C. (1986). Comparison of Prochloron from different hosts. New Phytol. 104,429-445.
18. Cox, G. C., Hiller, R. G., and Larkum, A. W. D. (1985). An usual cyanophyte, containing phycourobilin and symbiotic with ascidians and sponges. Mar. Biol. 89, 149-163.
19. Critchley, C., and Andrews, T. J. (1984). Photosynthesis and plasmamembrane permeability properties of Prochloron. Arch. Microbiol. 138, 247-250.
20. Dionisio-Sese, M. L., Ishikura, M., Maruyama, T., and Miyachi, S. (1997). UV-absorbing substances in the tunic of a colonial ascidian protect its symbiont, Prochloron sp., from damage by UV-B radiation. Mar. Biol. 128,455-461.
21. Dionisio-Sese, M. L., Maruyama, T., and Miyachi, S. (2001). Photosynthesis of Prochloron as affected by environmental factors. Mar. Biotechnol. 3, 74-79.
22. Donia, M. S., Fricke, W. F., Ravel, J., and Schmidt, E. W. (2011a). Variation in tropical reef symbiont metagenomes defined by secondary metabolism. PLoS ONE 6, e17897. doi:10.1371/journal.pone.00 17897
23. Donia, M. S., Fricke, W. F., Partensky, F., Cox, J., Elshahawi, S. I., White, J. R., et al. (2011b). Complex microbiome underlying secondary and primary metabolism in the tunicate-Prochloron symbiosis. Proc. Natl. Acad. Sci. U.S.A. 108, E1423-E1432.
24. Enriquez, S., Mendez, E. R., and Iglesias-Prieto, R. (2005). Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol. Oceanogr. 50, 1025-1032.
25. Fabricius-Dyg, J., Mistlberger, G., Staal, M., Borisov, S. M., Klimant, I., and Kühl, M. (2012). Imaging of surface O2 dynamics in corals with magnetic micro optode particles. Mar. Biol. 159, 1621-1631.
26. Giordano, M., Beardall, J., and Raven, J. A. (2005). CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 56, 99-131.
27. Goodbody, I. (1974). The physiology of ascidians. Adv. Mar. Biol. 12, 121-149.
28. Gorton, H. L., Brodersen, C. R., Williams, W. E., and Vogelmann, T. C. (2010). Measurement of the optical properties of leaves under diffuse light. Photochem. Photobiol. 86, 1076-1083.
29. Griffiths, D. J. (2006). Chlorophyll b-containing oxygenic photosynthetic prokaryotes: oxychlorobacteria (Prochlorophytes). Bot. Rev. 72, 330-366.
30. Griffiths, D. J., and Thinh, L. V. (1983). Transfer of photosynthetically fixed carbon between the prokaryotic green alga Prochloron and its ascidian host. Aust. J. Mar. Freshwater Res. 34,431-440.
31. Grunwald, B., and Kühl, M. (2004). A system for imaging variable chlorophyll fluorescence of aquatic phototrophs. Ophelia 58, 79-89.
32. He, Q. F., Dolganov, N., Björkman, O., and Grossman, A. R. (2001). The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J. Biol. Chem. 276, 306-314.
33. Hirose, E. (2009). Ascidian tunic cells: morphology and functional diversity of free cells outside the epidermis. Invertebr. Biol. 128, 83-96.
34. Hirose, E., Hirabayashi, S., Hori, K., Kasai, F., and Watanabe, M. M. (2006). UV protection in the photo-symbiotic ascidian Didemnum molle inhabiting different depths. Zool Sci. 23, 57-63.
35. Hirose, E., and Maruyama, T. (2004). What are the benefits in the ascidian-Prochloron symbiosis? Endocytobiosis Cell Res. 15,51-62.
36. Hirose, E., Neilan, B. A., Schmidt, E. W., and Murakami, A. (2009a). "Enigmatic life and evolution of Prochloron and related cyanobacteria inhabiting colonial ascidians," in Handbook on Cyanobacteria, eds. P. M. Gault and H. J. Marler (NewYork: Nova), 161-189.
37. Hirose, E., Uchida, H., and Murakami, A. (2009b). Ultrastructural and microspectrophotometric characterization of multiple species of cyanobacterial photosymbionts coexisting in the colonial ascidian Trididemnum clinides (Tunicata, Ascidiacea, Didemnidae). Eur. J. Phycol. 44, 365-375.
38. Hirose, E., Ohtsuka, K., Ishikura, M., and Maruyama, T. (2004). Ultraviolet absorption in ascidian tunic and ascidian-Prochloron symbiosis. J. Mar. Biolog. Assoc. U.K. 84, 789-794.
39. Holst, G., Kohls, O., Klimant, I., König, B., Richter, T., and Kühl, M. (1998). A modular luminescence lifetime imaging system for mapping oxygen distribution in biological samples. Sens. Act. B 51,163-170.
40. Jensen, S. I., Stenou, A.-S., Bhaya, D., Kühl, M., and Grossman, A. R. (2011). In situ dynamics of O2, pH and cyanobacterial transcripts associated with CCM, photosynthesis and detoxification of ROS. ISME J. 5,317-328.
41. Kline, T. C., and Lewin, R. A. (1999). Natural 15N/14N abundance as evidence for N2 fixation by Prochloron (Prochloro-phyta) endosymbiotic with didemnidascidians. Symbiosis26,193-198.
42. Koike, I., Yamamuro, M., and Pollard, P. C. (1993). Carbon and nitrogen budgets of two ascidians and their symbiont, Prochloron, in a tropical seagrass meadow. Aust. J. Mar. Freshwater Res. 44,173-182.
43. Kott, P. (1984). Related species of Trididemnum in symbiosis with Cyanophyta. Proc. Linn. Soc. N. S. W. 107,515-520.
44. Kremer, B. P., Pardy, R., and Lewin, R. A. (1982). Carbon fixation and photosynthates of Prochloron, a green alga symbiotic with an ascidian, Lissoclinum patella. Phycologia 21, 258-263.
45. Kühl, M. (2005). Optical microsensors for analysis of microbial communities. Meth. Enzymol. 397, 166-199.
46. Kühl, M., Chen, M., and Larkum, A. W. D. (2007a). "Biology of the chlorophyll d-containing cyanobacterium Acaryochloris marina," in Algae and Cyanobacteria in Extreme Environments, ed. J. Seckbach (Berlin: Springer), 101-123.
47. Kühl, M., Cohen, Y., Dalsgaard, T., Jørgensen, B. B., and Revsbech, N. P. (1995). The microenvironment and photo-synthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar. Ecol. Progr. Ser. 117, 159-172.
48. Kühl, M., Lassen, C., and Jørgensen, B.B. (1994). Light penetration and light intensity in sandy sediments measured with irradiance and scalar irradiance fiber-optic microprobes. Mar. Ecol. Progr. Ser. 105,139-148.
49. Kühl, M., Rickelt, L. F., and Thar, R. (2007b). Combined imaging of bacteria and oxygen in biofilms. Appl. Environ. Microbiol. 73, 6289-6295.
50. Kühl, M., Chen, M., Ralph, P. J., Schreiber, U., and Larkum, A. W. D. (2005). A niche for cyanobacteria containing chlorophyll d. Nature 433, 820.
51. Kühl, M., Holst, G., Larkum, A. W. D., and Ralph, P. J. (2008). Imaging of oxygen dynamics within the endolithic algal community of the massive coral Porites lobata (Dana). J. Phycol. 44, 541-550.
52. Kühl, M., and Jørgensen, B. B. (1994). The light field of micro-benthic communities: radiance distribution and microscale optics of sandy coastal sediments. Limnol. Oceanogr. 39, 1368-1398.
53. Kühl, M., and Larkum, A. W.D. (2002). "The microenvironment and photo-synthetic performance of Prochloron sp. in symbiosis with didemnid ascidians," in Symbioses, Mechanisms and Model Systems, ed. J. Seckbach (Dordrecht: Kluwer Academic Publisher), 273-290.
54. Kühl, M., and Polerecky, L. (2008). Functional and structural imag ing of phototrophic microbial commmunities and symbioses. Aquat. Microb. Ecol. 53, 99-118.
55. Kühl, M., and Revsbech, N. P. (2001). "Biogeochemical microsensors for boundary layer studies," in The Benthic Bounday Layer, eds B. P. Boudreau and B. B. Jørgensen (Oxford: Oxford University Press), 180-210.
56. La Roche, J., Van Der Stay, G. W. M., Partensky, F., Ducret, A., Aebersold, R., Li, R., et al. (1996). Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc. Natl. Acad. Sci. U.S.A. 93, 15244-15248.
57. Lafargue, F., and Duclaux, D. (1979). Premier exemple, en Atlantique tropical, d'une association symbiotique entre une ascidia didemnidae et unecyanophyce e chroococcale: Trididemnum cyanophorum nov. sp. et Synechocystis trididemni nov. sp. Ann. Inst. Oceanogr. (Paris) 55, 163-184.
58. Larkum, A. W. D., Chen, M., Li, Y., Schliep, M., Trampe, E., West, J., et al. (2012). A novel epiphytic chlorophyll d-containing cyanobacterium isolated from a mangrove-asscociated red alga. J. Phycol. doi:10.1111/j.1529-8817.2012.01233.x. [Epub ahead of print].
59. Larkum, A. W. D., and Kühl, M. (2005). Chlorophyll d: the puzzle resolved. Trends Plant Sci. 10,355-357.
60. Larsen, M., Borisov, S. M., Grunwald, B., Klimant, I., and Glud, R. N. (2011). A simple and inexpensive high resolution color ratiometric planar optode imaging approach: application to oxygen and pH sensing. Limnol. Oceanogr. Methods 9, 348-360.
61. Larsson, J., Nylander, J. A. A., and Bergman, B. (2011). Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits. BMC Evol. Biol. 11, 187. doi:10.1186/1471-2148-11-187
62. Lesser, M. P., Mazel, C. H., Gorbunov, M. Y., and Falkowski, P. G. (2004). Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305,997-1000.
63. Lesser, M. P., and Stochaij, W. R. (1990). Photoadaptation and protection against active forms of oxygen in the symbiotic prokary-ote Prochloron sp. and its ascidian host. Appl. Environ. Microbiol. 56, 1530-1535.
64. Lewin, R. A. (1977). Prochloron, type genus of the Prochlorophyta. Phycologia 16, 217. Lewin, R. A., and Cheng, L. (1975). Associations of microscopic algae with didemnid ascidians. Phycologia 14,149-152.
65. Lewin, R. A., and Cheng, L. (1989). Prochloron, a Microbial Enigma. New York: Chapmann and Hall.
66. Lewin, R. A., Cheng, L., and Matta, J. (1984). Diurnal rhytm in the cell-division frequency of Prochloron (Prochlorophyta) in nature. Phycologia 23, 505-507.
67. Lewin, R. A., and Pardy, R. L. (1981). Photosynthetic activity of Prochloron, and translocation of metabolites to its ascidian host. Phycologia 20,109-109.
68. Lewin, R. A., and Withers, N.W. (1975). Extraordinary pigment composition of a prokaryotic alga. Nature 256, 735-737.
69. López-Legentil, S., Song, B., Bosch, M., Pawlik, J. R., and Turon, X. (2011). Cyanobacterial diversity and a new acaryochloris-like symbiont from Bahamian seasquirts. PLoS ONE 6, e23938. doi:10.1371/journal.pone.0023938
70. Magnusson, S. H., Fine, M., and Kühl, M. (2007). Light microclimate of endolithic phototrophs in the scleractinian corals Montipora monasteriata and Porites cylindrica. Mar. Ecol. Prog. Ser. 332, 119-128.
71. Martínez-García, M., Díaz-Valdés, M., Wanner, G., Ramos-Esplá, A., and Antón, J. (2007). Microbial community associated with the colonial ascidian Cystodytes dellechiajei. Environ. Microbiol. 9, 521-534.
72. Maruyama, T., Hirose, E., and Ishikura, M. (2003). Ultraviolet-light-absorbing tunic cells in didemnid ascidians hosting a symbiotic photo-oxygenic prokaryote, Prochloron. Biol. Bull. 204, 109-113.
73. Maurice, C. (1888). Etude monographique d'une espece d'Ascidies composee. Arch. Biol. (Liege) 8, 205-405.
74. Mayr, T., Borisov, S. M., Abel, T., Enko, B., Waich, K., Mistlberger, G., et al. (2009). Light harvesting as a simple and versatile way to enhance brightness of luminescent sensors. Anal. Chem. 15, 6541-6545.
75. McCourt, R. M., Michaels, A. F., and Hoshaw, R. W (1984). Seasonality of symbiotic Prochloron (Prochlorophyta) and its Didemnid host in the northern Gulf of California. Phycologia 23, 95-101.
76. Menezes, C. B., Bonugli-Santos, R. C., Miqueletto, P. B., Passarini, M. R. Z., Silva, C. H. D., Justo, M. R., et al. (2010). Microbial diversity associated with algae, ascidians and sponges from the north coast of São Paulo state, Brazil. Microbiol. Res. 165,466-482.
77. Münchhoff, J., Hirose, E., Maruyama, T., Sunairi, M., Burns, B. P., and Neilan, B. A. (2007). Host specificity and phylogeography of the prochlorophyte Prochloron sp., an obligate symbiont in didemnid ascidians. Environ. Microbiol. 9, 890-899.
78. Murray, J. W., Duncan, J., and Barber, J. (2006). CP43-like chlorophyll binding proteins: structural and evolutionary implications. Trends Plant Sci. 11, 152-158.
79. Newcomb, E. H., and Pugh, T. D. (1975). Blue-green algae associated with ascidians of the Great Barrier Reef. Nature 253, 533-534.
80. Odintsov,V. S. (1991). Nitrogen fixation in Prochloron (Prochlorophyta)-ascidian associationsis Prochloron responsible. Endocytobiosis Cell Res. 7, 253-258.
81. Olson, R. R. (1986). Light-enhanced growth of the ascidian Didemnum molle/Prochloron sp. symbiosis. Mar. Biol. 93, 437-442.
82. Olson, R. R., and Porter, J. W. (1985). "Insitu measurement of photosynthesis and respiration in the Didemnum molle-Prochloron symbiosis," in Proceedings of the 5th International Coral Reef Symposium, Tahiti.
83. Paerl, H. W (1984). N2 fixation (nitrogenase activity) attributable to a specific Prochloron (Prochlorophyta)-ascidian association in Palau, Micronesia. Mar. Biol. 81,251-254.
84. Palenik, B., and Haselkorn, R. (1992). Multiple evolutionary origins of prochlorophytes, the chlorophyll b containing prokaryotes. Nature 355, 265-267.
85. Palinska, K. A. (2008). "Cyanobacteria," in Encyclopedia of Life Sciences (Chichester: Wiley). doi:10.1002/9780470015902.a0000454.pub2. Available at: http://onlinelibrary.wiley.com/doi/10.1002/9780470015902.a0000454.pub2/pdf
86. Parry, D. L. (1985). Nitrogen assimilation in the symbiotic marine algae Prochloron spp. Mar. Biol. 87, 219-222.
87. Parry, D. L. (1986). Prochloron on the sponge Aplysilla sp. Bull. Mar. Sci. 38,388-390.
88. Partensky, F., and Garczarek, L. (2003). "The photosynthetic apparatus of chlorophyll b-and d-containing Oxychlorobacteria," in Photosynthesis in Algae, eds. A. W. D. Larkum, S. E. Douglas, and J. A. Raven (Dordrecht: Kluwer), 29-62.
89. Patterson, G. M., and Withers, N. W. (1982). Laboratory cultivation of Prochloron, a tryptophan auxotroph. Science 217,1034-1035.
90. 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.
91. Ralph, P. J., Schreiber, U., Gademann, R., Kühl, M., and Larkum, A. W. D. (2005). Coral photobiology studied with a new imaging PAM fluorometer. J. Phycol. 41, 335-342.
92. Revsbech, N. P. (1989) An oxygen microsensor with a guard cathode. Limnol. Oceanogr. 34,474-478.
93. Schliep, M., Cavigliasso, G., Quinnell, R. G., Stranger, R., and Larkum, A. W. D. (2012). Formyl group modification of chlorophyll a: a major evolutionary mechanism in oxygenic photosynthesis. Plant Cell Environ. doi:10.1111/pce. 12000. [Epub ahead of print].
94. Schmidt,E.W.,andDonia,M.S. (2010). Life in cellulose houses: symbiotic bacterial biosynthesis of ascidian drugs and drug leads. Curr. Opin. Biotechnol. 21,827-833.
95. Schmidt, E. W., Donia, M. S., McIntosh, J. A., Fricke, W E, and Ravel, J. (2012). Origin and variation of tunicate secondary metabolites. J. Nat. Prod. 75, 295-304.
96. Schmidt, E. W., Nelson, J. T., Rasko, D. A., Sudek, S., Eisen, J. A., Haygood, M. G., et al. (2005). Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc. Natl. Acad. Sci. U.S.A. 102,7315-7320.
97. Schreiber, U., Gademann, R., Bird, P., Ralph, P., Larkum, A. W. D., and Kühl, M. (2002). Apparent light requirement for activation of photosynthesis upon rehydration of dessicated beachrock microbial mats. J. Phycol. 38, 125-134.
98. Schreiber, U., Gademann, R., Ralph, P. J., and Larkum, A. W D. (1997). Assessment of photosynthetic performance of Prochloron in Lissoclinum patella in hospite by chlorophyll fluorescence measurements. Plant Cell Physiol. 38, 945-951.
99. Smith, H. G. (1935). On the presence of algae in certain ascidians. Ann. Mag. Nat. Hist. 15,615-626.
100. Staal, M., Borisov, S., Rickelt, L. F., Klimant, I., and Kühl, M. (2011).Ultrabright planar optodes for luminescence life-time based microscopic imaging of O2 dynamics in biofilms. J. Microbiol. Methods 85, 67-74.
101. Stal, L. J., and Moezelaar, R. (1997). Fermentation in cyanobacteria. FEMS Microbiol Rev. 21, 179-211.
102. Stal, L. J., and Zehr, J. P. (2008). "Cyanobacterial nitrogen fixation in the ocean: diversity, regulation, and ecology," in The Cyanobacteria: Molecular Biology, Genomics and Evolution, eds. E. Flores, and A. Herrero (Norfolk: Caister Academic Press), 423-446.
103. Steunou, A.-S., Jensen, S. I., Brecht, E., Becraft, E. D., Bateson, M. M., Kilian, O., et al. (2008). Regulation of nif gene expression and the energetics of N2 fixation over the diel cycle in a hot spring microbial mat. ISME J. 2, 364-378.
104. Stomp, M., Huisman, J., Stal, L. J., and Matthijs, H. C. P. (2007a). Colorful niches of phototrophic microorganisms shaped by vibrations of the water molecule. ISME J. 1, 271-282.
105. Stomp, M., Huisman, J., Vörös, L., Pick, F. R., Laamanen, M., Haverkamp, T., et al. (2007b). Colourful coexistence of red and green picocyanobacteria in lakes and seas. Ecol. Lett. 10, 290-298.
106. Swift, H., and Leser, G. P. (1989). Cytochemical studies on prochlorophytes: localization of DNA and ribulose 1,5-bisphosphate carboxylase oxygenase. J. Phycol. 25, 751-761.
107. Tait, E., Carman, M., and Sievert, S. M. (2007). Phylogenetic diversity of bacteria associated with ascidians in Eel Pond (Woods Hole, Massachusetts, USA). J. Exp. Mar. Biol. Ecol. 342, 138-146.
108. Tokioka, T. (1942). Ascidians found on the mangrove trees in Lwayama Bay, Palau. Palau Trop. Biol. Station Stud. 2, 499-507.
109. Trampe, E., Kolbowski, J., Schreiber, U., and Kühl, M. (2011). Rapid assessment of different oxygenic phototrophs and single cell photosynthesis with multicolour variable chlorophyll fluorescence imaging. Mar. Biol. 158,1667-1675.
110. Vogelmann, T. C. (1993). Plant tissue optics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 231-251.
111. Vogelmann, T. C., and Björn, L. O. (1986). Plants as light traps. Physiol. Plant. 68, 704-708.
112. Wangpraseurt, D., Larkum, A. W. D., Ralph, P. J., and Kühl, M. (2012). Light gradients and optical microniches in coral tissues. Front. Microbiol. 3:316. doi:10.3389/fmicb.2012.00316
113. Yokobori, S., Kurabayashi, A., Neilan, B. A., Maruyama, T., and Hirose, E. (2006). Multiple origins of the ascidian-Prochloron symbiosis: molecular phylogeny of photosymbiotic and nonsymbiotic colonial ascidians inferred from 18S rDNA sequences. Mol. Phylogenet. Evol. 40, 8-19.
114. Zhaxybayeva, O., Gogarten, J. P., Charlebois, R. L., Doolittle, W. F., and Papke, R. T. (2006). Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res. 16, 1099-1108.