Growth and Thallus Morphogenesis of Ulva mutabilis (Chlorophyta) Depends on A Combination of Two Bacterial Species Excreting Regulatory Factors

Journal of Phycology

Volumn 48, Issue 6, 2012, Pages 1433-1447

  Spoerner, Michael ^a   Wichard, Thomas ^b,c   Bachhuber, Tanja ^c   Stratmann, Johannes ^c   Oertel, Wolfgang ^c  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Axenic alga; Cytophaga sp; Developmental mutant; Differentiation; Roseobacter sp; Symbiosis; Thallus morphology; Ulva mutabilis

Indexed keywords

ALGAE; BACTERIA (MICROORGANISMS); CHLOROPHYTA; CYTOPHAGA; HALOMONAS; ROSEOBACTER; SULFITOBACTER; ULVA; ULVA MUTABILIS;

EID: 84870939222     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2012.01231.x     Document Type: Article

References (53)

1. Allgaier, M., Uphoff, H., Felske, A. & Wagner-Dobler, I. 2003. Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats. Appl. Environ. Microbiol. 69:5051-9.
2. Blomster, J., Maggs, C. A. & Stanhope, M. J. 1998. Molecular and morphological analysis of Enteromorpha intestinalis and E. compressa (Chlorophyta) in the British Isles. J. Phycol. 34:319-40.
3. Brodie, J., Maggs, C. A. & John, D. M. 2007. Green seaweeds of Britain and Ireland. British Phycological Society, Dunmurry, 242 pp.
4. Burggraf, S., Olsen, G. J., Stetter, K. O. & Woese, C. R. 1992. A phylogenetic analysis of Aquifex pyrophilus Syst. Appl. Microbiol. 15:352-6.
5. Callow, J. A. & Callow, M. E. 2005. The spore adhesive system of Ulva Phycologia 44:35.
6. Callow, J. A., Osborne, M. P., Callow, M. E., Baker, F. & Donald, A. M. 2003. Use of environmental scanning electron microscopy to image the spore adhesive of the marine alga Enteromorpha in its natural hydrated state. Colloid Surface B 27:315-21.
7. Felsenstein, J. 1982. Numerical methods for inferring evolutionary trees. Q. Rev. Biol. 57:379-404.
8. Fitch, W. M. 1971. Toward defining course of evolution - minimum change for a specific tree topology. Syst. Zool. 20:406-16.
9. Fjeld, A. 1970. A chromosomal factor exerting a predetermining effect on morphogenesis in multicellular green alga Ulva mutabilis Genet. Res. 15:309-16.
10. Fjeld, A. 1971. Genetic control of cellular differentiation in Ulva mutabilis. 2. Induced chimeras. Hereditas Genetiskt Arkiv 69:59-66.
11. Fjeld, A. 1972. Genetic control of cellular differentiation in Ulva mutabilis. Gene effects in early development. Dev. Biol. 28:326-43.
12. Fjeld, A. & Løvlie, A 1976. Genetics of multicellular marine algae. In Lewin, R. A. [Ed.] The Genetics of Algae, Botanical Monographs. University of California Press, Berkeley.
13. Føyn, B. 1958. Über die Sexualität und den Generationswechsel von Ulva mutabilis Arch. Protistenkd. 102:473-80.
14. Føyn, B. 1959. Geschlechtskontrollierte Vererbung bei der marinen Grünalge Ulva mutabilis Arch. Protistenkd. 118:236-53.
15. Føyn, B. 1960. Sex-linked inheritance in Ulva Biol. Bull. 118:407-11.
16. Fries, L. 1975. Some observations on morphology of Enteromorpha linza and Enteromorpha compressa in axenic culture. Bot. Mar. 18:251-3.
17. Fries, L. & Aberg, S. 1978. Morphogenetic effects of phenylacetic and p-OH-phenylacetic acid on green alga Enteromorpha compressa (L) Grev in axenic culture. Z. Pflanzenphysiol. 88:383-8.
18. Hayden, H. S., Blomster, J., Maggs, C. A., Silva, P. C., Stanhope, M. J. & Waaland, J. R. 2003. Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur. J. Phycol. 38:277-94.
19. Hori, H., Lim, B. L. & Osawa, S. 1985. Evolution of green plants as deduced from 5s ribosomal-RNA sequences. Proc. Natl. Acad. Sci. U. S. A. 82:820-3.
20. Hornsey, I. S. & Hide, D. 1976. The production of antimicrobial compounds by British marine algae. III. Distribution of antimicrobial activity within the thallus. Brit. Phycol. J. 11:175-81.
21. Hoxmark, R. C. 1975. Experimental analysis of life cycle of Ulva mutabilis Bot. Mar. 18:123-9.
22. Joint, I., Tait, K. & Wheeler, G. 2007. Cross-kingdom signalling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva Philos. T. Roy. Soc. B 362:1223-33.
23. Leliaert, F., Zhang, X. W., Ye, N. H., Malta, E., Engelen, A. H., Mineur, F., Verbruggen, H. & De Clerck, O. 2009. Research note: identity of the Qingdao algal bloom. Phycol. Res. 57:147-51.
24. Lewis, L. A. & McCourt, R. M. 2004. Green algae and the origin of land plants. Am. J. Bot. 91:1535-56.
25. Løvlie, A. 1964. Genetic control of division rate and morphogenesis in Ulva mutabilis Føyn. C. R. Trav. Lab. Carlsberg 34:77-168.
26. Løvlie, A. 1968. On the use of a multicellular alga (Ulva mutabilis Føyn) in the study of general aspects of growth and differentiation. Nytt. Mag. Zool. 16:39-49.
27. Løvlie, A. 1969. Cell size, nucleic acids, and synthetic efficiency in the wild type and a growth mutant of the multicellular alga Ulva mutabilis Føyn. Dev. Biol. 20:349-67.
28. Løvlie, A. & Bråten, T. 1970. On mitosis in multicellular alga Ulva mutabilis Føyn. J. Cell Sci. 6:109-29.
29. Løvlie, A. & Bryhni, E. 1978. On the relation between sexual and parthenogenetic reproduction in haplo-diplontic algae. Bot. Mar. 21:155-63.
30. Marshall, K., Joint, I., Callow, M. E. & Callow, J. A. 2006. Effect of marine bacterial isolates on the growth and morphology of axenic plantlets of the green alga Ulva linza Microb. Ecol. 52:302-10.
31. Matsuo, Y., Imagawa, H., Nishizawa, M. & Shizuri, Y. 2005. Isolation of an algal morphogenesis inducer from a marine bacterium. Science 307:1598.
32. Matsuo, Y., Suzuki, M., Kasai, H., Shizuri, Y. & Harayama, S. 2003. Isolation and phylogenetic characterization of bacteria capable of inducing differentiation in the green alga Monostroma oxyspermum Environ. Microbiol. 5:25-35.
33. Nakanishi, K., Nishijima, M., Nishimura, M., Kuwano, K. & Saga, N. 1996. Bacteria that induce morphogenesis in Ulva pertusa (Chlorophyta) grown under axenic conditions. J. Phycol. 32:479-82.
34. Olsen, G. J., Lane, D. J., Giovannoni, S. J., Pace, N. R. & Stahl, D. A. 1986. Microbial ecology and evolution - a ribosomal RNA approach. Annu. Rev. Microbiol. 40:337-65.
35. Patel, P., Callow, M. E., Joint, I. & Callow, J. A. 2003. Specificity in the settlement - modifying response of bacterial biofilms towards zoospores of the marine alga Enteromorpha Environ. Microbiol. 5:338-49.
36. Provasoli, L. 1958. Effect of plant hormones on Ulva Biol. Bull. 114:375-84.
37. Provasoli, L. & Pintner, I. J. 1964. Symbiotic relationships between microorganisms and seaweeds. Am. J. Bot. 51:681-5.
38. Reichardt, W. 1974. Ecophysiology of some aquatic bacteria from Flavobacterium-Cytophaga group. Zbl. Bakt. Orig. A 227:85-93.
39. Reichenbach, H. 2006. The order Cytophagales. Prokaryotes 7:549-90.
40. Schreiber, E. 1927. Die Reinkultur von marinen Phytoplankton und deren Bedeutung für die Erforschung der Produktionsfähigkeit des Meerwassers. Wiss. Meeresuntersuch., N.F. 10:1-34.
41. Shiba, T. 1991. Roseobacter litoralis gen-nov, sp-nov, and Roseobacter denitrificans sp-nov, aerobic pink-pigmented bacteria which contain bacteriochlorophyll a Syst. Appl. Microbiol. 14:140-5.
42. Shiba, T. & Imhoff, J. F 2005. Genus XVIII: Roseobacter. In Staley, J. T., Boone, D. R., Brenner, D. J., De Vos, P., Goodfellow, M., Krieg, N. R., Rainey, F. A., Garrity, G. M., Schleifer, K.-H. & Garrity, G. [Eds.] Bergey's Manual of Systematic Bacteriology. Springer, New York212-3.
43. Sneed, J. M. & Pohnert, G. 2010. The green macroalga Dictyosphaeria ocellata influences the structure of the bacterioplankton community through differential effects on individual bacterial phylotypes. FEMS Microbiol. Ecol. 75:242-54.
44. Sorakin, D. Y., Rainey, F. A., Webb, R. I. & Fuerst, J. A 2005. Genus XXV: Sulfitobacter. In Staley, J. T., Boone, D. R., Brenner, D. J., De Vos, P., Goodfellow, M., Krieg, N. R., Rainey, F. A., Garrity, G. M., Schleifer, K.-H. & Garrity, G. [Eds.] Bergey's Manual of Systematic Bacteriology. Springer, New York224-8.
45. Stanley, M. S., Callow, M. E. & Callow, J. A. 1999. Monoclonal antibodies to adhesive cell coat glycoproteins secreted by zoospores of the green alga Enteromorpha Planta 210:61-71.
46. Stirk, W. A., Novak, O., Hradecka, V., Pencik, A., Rolcik, J., Strnad, M. & Van Staden, J. 2009. Endogenous cytokinins, auxins and abscisic acid in Ulva fasciata (Chlorophyta) and Dictyota humifusa (Phaeophyta): towards understanding their biosynthesis and homoeostasis. Eur. J. Phycol. 44:231-40.
47. Stratmann, J., Paputsoglu, G. & Oertel, W. 1996. Differentiation of Ulva mutabilis (Chlorophyta) gametangia and gamete release are controlled by extracellular inhibitors. J. Phycol. 32:1009-21.
48. Tait, K., Joint, I., Daykin, M., Milton, D. L., Williams, P. & Camara, M. 2005. Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms. Environ. Microbiol. 7:229-40.
49. Tatewaki, M. 1983. Morphogenesis of Monostroma oxyspermum (Kutz) Doty (Chlorophyceae) in axenic culture, especially in bialgal culture. J. Phycol. 19:409-16.
50. Viaroli, P., Bartoli, M., Azzoni, R., Giordani, G., Mucchino, C., Naldi, M., Nizzoli, D. & Taje, L. 2005. Nutrient and iron limitation to Ulva blooms in a eutrophic coastal lagoon (Sacca di Goro, Italy). Hydrobiologia 550:57-71.
51. Vroeland, R. H 2005. Genus I. Halomonas. In Brenner, D. J., Krieg, N. R., Staley, J. R. & Garrity, G. M. [Eds.] Bergey's Manual of Systematic Bacteriology. Springer, New York300-13.
52. Wichard, T. & Oertel, W. 2010. Gametogenesis and gamete release of Ulva mutabilis and Ulva lactuca (Chlorophyta): regulatory effects and chemical characterization of the "swarming inhibitor". J. Phycol. 46:248-59.
53. Woodman, M. E 2008. Direct PCR of intact bacteria (colony PCR) Curr. Prot. Microbiol. 9:A.3D.1-6.