Advertisement

Marine Biology

, Volume 156, Issue 10, pp 2011–2020 | Cite as

Inception of formation and early morphogenesis of the bacterial light organ of the sea urchin cardinalfish, Siphamia versicolor

  • Paul V. Dunlap
  • Yutaka Kojima
  • Shigeo Nakamura
  • Masaru Nakamura
Original Paper

Abstract

The cardinalfish Siphamia versicolor (Perciformes: Apogonidae) forms a bioluminescent symbiosis with the marine luminous bacterium Photobacterium mandapamensis, harboring the bacteria in a ventral, disc-shaped light organ and using the bacterial light apparently for counterillumination and attracting prey. Little definitive information has been available on the developmental and microbiological events surrounding the initiation of symbiosis, a critical stage in the life history of the fish, in S. versicolor or any of the many other species of bacterially luminous fish. To identify the stage at which light organ formation begins, to determine the origin of cells forming the light organ, and to characterize its bacterial colonization status during development, early developmental stages of S. versicolor obtained and reared from wild-caught mouth-brooding males were examined with histological and microbiological methods. A light organ primordium was not evident in embryos, post-embryos, or pre-release larvae, whereas the light organ began to form within 1 day of release of full-term pre-flexion larvae from the mouths of male fish. Analysis of post-release larvae revealed that the light organ arises from a proliferation and differentiation of intestinal epithelial cells, and that it quickly develops structural complexity, including the formation of chambers and gaps contiguous with the intestinal epithelium. However, the nascent light organ remained uncolonized by the symbiotic bacteria through several days of post-release development, even in the presence of high numbers of the symbiotic bacteria. These results demonstrate that the inception of light organ formation in S. versicolor occurs independently of its symbiotic bacteria and that receptivity to bacterial colonization apparently requires substantial post-release development of the light organ. Larvae therefore most likely acquire their symbiotic bacteria from seawater, during or shortly after the transition from the pre-flexion to the flexion developmental stage.

Keywords

Great Barrier Reef Early Developmental Stage Symbiotic Bacterium Light Organ Male Fish 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank D. Sorenson and M. Dzaman, University of Michigan, for assistance with histology, R. Murata, Tropical Biosphere Research Center (TBRC), University of the Ryukyus, for guidance in histological methods, and R. Suwa, M. Alam, Y. Kobayashi, and T. Sagawa (TBRC) for technical support. Support was provided by the University of the Ryukyus via a Visiting Professorship to P. Dunlap. This study is a contribution from Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus.

References

  1. Baldwin CC, Johnson GD (1995) A larva of the Atlantic flashlight fish, Kryptophaneron alfredi (Beryciformes: Anomalopidae), with a comparison of beryciform and stephanoberyciform larvae. Bull Mar Sci 56:1–24Google Scholar
  2. Callahan SM, Dunlap PV (2000) LuxR- and acyl-homoserine-lactone-controlled non-lux genes define a quorum-sensing regulon in Vibrio fischeri. J Bacteriol 182:2811–2822PubMedCrossRefGoogle Scholar
  3. Claes MF, Dunlap PV (2000) Aposymbiotic culture of the sepiolid squid Euprymna scolopes: role of the symbiotic bacterium Vibrio fischeri in host animal growth, development, and light organ morphogenesis. J Exp Zool 286:280–296PubMedCrossRefGoogle Scholar
  4. Dunlap PV, Kita-Tsukamoto K (2006) Luminous bacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes, a handbook on the biology of bacteria, ecophysiology and biochemistry, 3rd edn. Springer, New York, pp 863–892Google Scholar
  5. Dunlap PV, McFall-Ngai MJ (1987) Initiation and control of the bioluminescent symbiosis between Photobacterium leiognathi and leiognathid fish. Ann New York Acad Sci 503:269–283CrossRefGoogle Scholar
  6. Dunlap PV, Jiemjit A, Ast JC, Pearce MM, Marques RR, Lavilla-Pitogo CR (2004) Genomic polymorphism in symbiotic populations of Photobacterium leiognathi. Environ Microbiol 6:145–158PubMedCrossRefGoogle Scholar
  7. Dunlap PV, Ast JC, Kimura S, Fukui A, Yoshino T, Endo H (2007) Phylogenetic analysis of host-symbiont specificity and codivergence in bioluminescent symbioses. Cladistics 23:507–532CrossRefGoogle Scholar
  8. Dunlap PV, Davis KM, Tomiyama S, Fujino M, Fukui A (2008) Developmental and microbiological analysis of the inception of bioluminescent symbiosis in the marine fish Nuchequula nuchalis (Perciformes: Leiognathidae). Appl Environ Microbiol 74:7471–7481PubMedCrossRefGoogle Scholar
  9. Eibl-Eibesfeldt I (1961) Eine Symbiose zwischen Fischen (Siphamia versicolor) und Seeigeln. Z Tierpsychol 18:56–59Google Scholar
  10. Froese R, Pauly D (2008) FishBase. World Wide Web electronic publication. www.fishbase.org, version (10/2008)
  11. Haneda Y (1965) Observations on a luminous apogonid fish, Siphamia versicolor, and on others of the same genus. Sci Rep Yokosuka Cy Mus 11:1–12Google Scholar
  12. Harms JW (1928) Bau und entwicklung eines eigenartigen leuchtorgans bei Equula spec. Z wiss Zool 131:157–179Google Scholar
  13. Hastings JW (1971) Light to hide by: ventral luminescence to camouflage the silhouette. Science 173:1016–1017PubMedCrossRefGoogle Scholar
  14. Hastings JW, Nealson KH (1981) The symbiotic luminous bacteria. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes: a handbook on habitats, isolation, and identification of bacteria. Springer-Verlag, Berlin, pp 1332–1345Google Scholar
  15. Herring PJ, Morin JG (1978) Bioluminescence in fish. In: Herring PJ (ed) Bioluminescence in action. Academic Press, London, pp 273–329Google Scholar
  16. Iwai T (1958) A study of the luminous organ of the apogonid fish Siphamia versicolor (Smith and Radcliffe). J Wash Acad Sci 48:267–270Google Scholar
  17. Iwai T (1971) Structure of luminescent organ of apogonid fish, Siphamia versicolor. Japanese J Icthyol 18:125–127Google Scholar
  18. Jordan AR, Bruce BD (1993) Larval development of three roughy species complexes (Pisces: Trachichthyidae) from southern Australian waters, with comments on the occurrence of orange roughy Hoplostethus atlanticus. Fish Bull US 91:76–86Google Scholar
  19. Kaeding AJ, Ast JC, Pearce MM, Urbanczyk H, Kimura S, Endo H, Nakamura M, Dunlap PV (2007) Phylogenetic diversity and co-symbiosis in the bioluminescent symbioses of Photobacterium mandapamensis. Appl Environ Microbiol 73:3173–3182PubMedCrossRefGoogle Scholar
  20. Konishi Y, Okiyama M (1997) Morphological development of four trachichthyid larvae (Pisces: Beryciformes), with comments on trachichthyoid relationships. Bull Mar Sci 60:66–88Google Scholar
  21. Leis JM, Bullock S (1986) The luminous cardinalfish Siphamia (Pisces, Apogonidae): development of larvae and the luminous organ. In: Uyeno T, Arai R, Taniuchi T, Matsuura K (eds) Indo-pacific fish biology: proceedings of the second international conference on Indo-pacific fish. Japanese Ichthyol Soc, Tokyo, pp 703–714Google Scholar
  22. McFall-Ngai MJ (1983a) Adaptation for reflection of bioluminescent light in the gasbladder of Leiognathus equulus (Perciformes: Leiognathidae). J Exp Zool 227:23–33PubMedCrossRefGoogle Scholar
  23. McFall-Ngai MJ (1983b) The gasbladder as a central component of the leiognathid bacterial light organ symbiosis. Am Zool 23:907Google Scholar
  24. McFall-Ngai MJ, Dunlap PV (1983) Three new modes of luminescence in the leiognathid fish Gazza minuta (Perciformes: Leiognathidae): discrete projected luminescence, ventral body flash and buccal luminescence. Mar Biol 73:227–237CrossRefGoogle Scholar
  25. McFall-Ngai MJ, Morin JG (1991) Camouflage by disruptive illumination in leiognathids, a family of shallow-water, bioluminescent fish. J Exp Biol 156:119–137Google Scholar
  26. McFall-Ngai MJ, Ruby EG (1991) Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 254:1491–1494PubMedCrossRefGoogle Scholar
  27. Morin JG, Harrington A, Nealson K, Krieger N, Baldwin TO, Hastings JW (1975) Light for all reasons: versatility in the behavioral repertoire of the flashlight fish. Science 190:74–76Google Scholar
  28. Munk O, Hansen K, Herring PJ (1998) On the development and structure of the escal light organ of some melanocetid deep sea anglerfish (Pisces: Ceratioidei). J Mar Biol Assoc UK 78:1321–1335CrossRefGoogle Scholar
  29. Ruby EG (1996) Lessons from a cooperative, bacterial-animal association: the Vibrio fischeri-Euprymna scolopes light organ symbiosis. Annu Rev Microbiol 50:591–624PubMedCrossRefGoogle Scholar
  30. Sasaki A, Ikejima K, Aoki S, Azuma N, Kashimura N, Wada M (2003) Field evidence for bioluminescent signaling in the pony fish, Leiognathus elongatus. Environ Biol Fish 66:307–311CrossRefGoogle Scholar
  31. Sparks JS, Dunlap PV, Smith WL (2005) Evolution and diversification of a sexually dimorphic luminescent system in ponyfish (Teleostei: Leiognathidae), including diagnoses for two new genera. Cladistics 21:305–327CrossRefGoogle Scholar
  32. Tominaga Y (1964) Notes on the fishes of the genus Siphamia (Apogonidae), with a record of S. versicolor from the Ryukyu Islands. Japanese J Ichthyol 12:10–17Google Scholar
  33. Urbanczyk H, Ast JC, Higgins MJ, Carson J, Dunlap PV (2007) Reclassification of Vibrio fischeri, Vibrio logei, Vibrio salmonicida and Vibrio wodanis as Aliivibrio fischeri gen. nov., comb. nov., Aliivibrio logei comb. nov., Aliivibrio salmonicida comb. nov., and Aliivibrio wodanis comb. nov. Int J System Evol Microbiol 57:2823–2829CrossRefGoogle Scholar
  34. Wada M, Azuma N, Mizuno N, Kurokura H (1999) Transfer of symbiotic luminous bacteria from parental Leiognathus nuchalis to offspring. Mar Biol 135:683–687CrossRefGoogle Scholar
  35. Yamada K, Haygood M, Kabasawa H (1979) On fertilization and early development in the pine-cone fish, Monocentris japonicus. Ann Rep Keikyu Aburatsubo Mar Park Aquar 10:31–38Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Paul V. Dunlap
    • 1
  • Yutaka Kojima
    • 2
  • Shigeo Nakamura
    • 2
  • Masaru Nakamura
    • 2
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA
  2. 2.Tropical Biosphere Research CenterUniversity of the RyukyusMotobuJapan

Personalised recommendations