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Archives of Microbiology

, Volume 154, Issue 5, pp 496–503 | Cite as

Relationship of the luminous bacterial symbiont of the Caribbean flashlight fish, Kryptophanaron alfredi (family Anomalopidae) to other luminous bacteria based on bacterial luciferase (luxA) genes

  • Margo G. Haygood
Original Papers

Abstract

Flashlight fishes (family Anomalopidae) have light organs that contain luminous bacterial symbionts. Although the symbionts have not yet been successfully cultured, the luciferase genes have been cloned directly from the light organ of the Caribbean species, Kryptophanaron alfredi. The goal of this project was to evaluate the relationship of the symbiont to free-living luminous bacteria by comparison of genes coding for bacterial luciferase (lux genes). Hybridization of a luxAB probe from the Kryptophanaron alfredi symbiont to DNAs from 9 strains (8 species) of luminous bacteria showed that none of the strains tested had lux genes highly similar to the symbiont. The most similar were a group consisting of Vibrio harveyi, Vibrio splendidus and Vibrio orientalis. The nucleotide sequence of the luciferase α subunit gene luxA of the Kryptophanaron alfredi symbiont was determined in order to do a more detailed comparison with published luxA sequences from Vibrio harveyi, Vibrio fischeri and Photobacterium leiognathi. The hybridization results, sequence comparisons and the mol% G+C of the Kryptophanaron alfredi symbiont luxA gene suggest that the symbiont may be considered as a new species of luminous Vibrio related to Vibrio harveyi.

Key words

Bioluminescence Symbiosis Kryptophanaron alfredi 

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References

  1. Baldwin TO, Devine JH, Heckel RC, Lin J-W, Shadel GS (1989) The complete nucleotide sequence of the lux regulon of V. fischeri and the luxABN region of Photobacterium leiognathi and the mechanism of control of bacterial bioluminescence. J Biolumin Chemilumin 4:326–341CrossRefGoogle Scholar
  2. Baumann P, Baumann L, Bang SS, Woolkalis MJ (1980) Reevaluation of the taxonomy of Vibrio, Beneckea, and Photobacterium: Abolition of the genus Beneckea. Curr Microbiol 4:127–132CrossRefGoogle Scholar
  3. Belas R, Mileham A, Simon M, Silverman M (1984) Transposon mutagenosis of marine Vibrio spp. J Bacteriol 158:890–896PubMedPubMedCentralGoogle Scholar
  4. Cohn DH, Mileham AJ, Simon MI, Nealson KH, Rausch SK, Bonam D, Baldwin TO (1985) Nucleotide sequence of the luxA gene of Vibrio harveyi and the complete amino acid sequence of the α subunit of bacterial luciferase. J Biol Chem 260:6139–6146PubMedGoogle Scholar
  5. Colin PL, Arneson DW, Smith-Vaniz WF (1979) Rediscovery and redescription of the Caribbean Anomalopid fish Kryptophanaron alfredi Silvester and Fowler (Pisces: Anomalopidae). Bull Mar Sci 29:312–319Google Scholar
  6. Distel DL, Lane DJ, Olsen GJ, Giovanonni SJ, Pace B, Pace NR, Stahl DA, Felbeck H (1988) Sulfur-oxidizing bacterial endosymbionts: analysis of phylogeny and specificity by 16S rRNA sequences. J Bacteriol 170:2506–2510CrossRefGoogle Scholar
  7. Ditta G, Stanfield S, Corbin D, Helinski DR (1980) Broad hostrange DNA cloning system for Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci USA 77:7347–7351CrossRefGoogle Scholar
  8. Fitzgerald JM (1977) Classification of luminous bacteria from the light organ of the Australian pinecone fish, Cleidopus gloriamaris. Arch Microbiol 112:153–156CrossRefGoogle Scholar
  9. Foran DR, Brown WM (1988) Nucleotide sequence of the luxA and luxB genes of the bioluminescent marine bacterium Vibrio fischeri. Nucl Acids Res 16:777CrossRefGoogle Scholar
  10. Hada HS, Stemmler J, Grossbard ML, West PA, Potrikus CJ, Hastings JW, Colwell RR (1985) Characterization of non-O1 serovar Vibrio cholerae (Vibrio albensis). Syst Appl Microbiol 6:203–209CrossRefGoogle Scholar
  11. Halverson LJ, Stacey G (1986) Signal exchange in plant-microbe interactions. Microbiol Rev 50:193–215PubMedPubMedCentralGoogle Scholar
  12. Harvey EN (1912) A fish, with a luminous organ, designed for the growth of luminous bacteria. Science NS 53:314–315Google Scholar
  13. Haygood MG, Cohn DH (1986) Luciferase genes cloned from the unculturable luminous bacterial symbiont of the Caribbean flashlight fish, Kryptophanaron alfredi. Gene 45:203–209CrossRefGoogle Scholar
  14. Haygood MG, Tebo BM, Nealson KH (1984) Luminous bacteria of a monocentrid fish (Monocentris japonicus) and two anomalopid fishes (Photoblepharon palpebratus and Kryptophanaron alfredi): population sizes and growth within the light organs, and rates of release into the seawater. Marine Biol 78:249–254CrossRefGoogle Scholar
  15. Herdman M, Janvier M, Waterbury JB, Rippka R, Stanier R, Mandel M (1979) Deoxyribonucleic acid base composition of cyanobacteria. J Gen Microbiol 111:63–71CrossRefGoogle Scholar
  16. Herring PJ (1975) Bacterial bioluminescence in some argentinoid fishes. In: Barnes H (ed) Proc 9th Eur Mar Biol Symp (1975), Aberdeen University Press, Aberdeen, UK, pp 563–572Google Scholar
  17. Herring PJ (1987) Systematic distribution of bioluminescence in living organisms. J Biolumin Chemilumin 1:147–163CrossRefGoogle Scholar
  18. Herring PJ, Morin JG (1978) Bioluminescence in fishes. In: Herring PJ (ed) Bioluminescence in action. Academic Press, London, pp 273–329Google Scholar
  19. Illarionov BA, Protopopova M, Karginov VA, Mertvetsov NP, Gitelson JI (1988) Nucleotide sequence of part of Photobacterium leiognathi lux region. Nucl Acids Res 16:9855CrossRefGoogle Scholar
  20. Jensen JM, Tebo BM, Baumann P, Mandel M, Nealson KH (1980) Characterization of Alteromonas hanedai (sp. nov), a nonfermentative luminous species of marine origin. Curr Microbiol 3:311–315CrossRefGoogle Scholar
  21. Johnson GD, Rosenblatt RH (1988) Mechanisms of light occlusion in flashlight fishes, family Anomalopidae (Teleostei: Beryciformes), and the evolution of the group. Zool J Linn Soc 94:65–96CrossRefGoogle Scholar
  22. Johnston TC, Thompson RB, Baldwin TO (1986) Nucleotide sequence of the luxB gene of Vibrio harveyi and the complete amino acid sequence of the β subunit of bacterial luciferase. J Biol Chem 261:4805–4811PubMedGoogle Scholar
  23. Kessel M (1977) The ultrastructure of the relationship between the luminous organ of the teleost fish Photoblepharon palpebratus and its symbiotic bacteria. Cytobiologie 15:145–158Google Scholar
  24. Leisman G, Cohn DH, Nealson KH (1980) Bacterial origin of luminescence in marine animals. Science 208:1271–1273CrossRefGoogle Scholar
  25. Mierendorf RC, Pfeffer D (1987) Direct sequencing of denatured plasmid DNA. Methods Enzymol 152:556–562CrossRefGoogle Scholar
  26. Miyamoto CM, Graham AF, Meighen EA (1988) Nucleotide sequence of the luxC gene and the upstream DNA from the bioluminescent system of Vibrio harveyi. Nucl Acids Res 16:1551–1562CrossRefGoogle Scholar
  27. Nealson KH (1977) Autoinduction of bacterial luciferase. Arch Microbiol 112:73–79CrossRefGoogle Scholar
  28. Nealson KH, Hastings JW (1977) Low oxygen is optimal for luciferase synthesis in some bacteria. Arch Microbiol 112:9–16CrossRefGoogle Scholar
  29. Nealson KH, Hastings JW (1979) Bacterial bioluminescence: its control and ecological significance. Microbiol Rev 43:496–518PubMedPubMedCentralGoogle Scholar
  30. Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26:74–86CrossRefGoogle Scholar
  31. Reichelt JL, Nealson KH, Hastings JW (1977) The specificity of symbiosis: pony fish and luminescent bacteria. Arch Microbiol 112:157–161CrossRefGoogle Scholar
  32. Ruby EG, Morin JG (1978) Specificity of symbiosis between deepsea fishes and psychrotrophic luminous bacteria. Deep-Sea Res 25:161–167CrossRefGoogle Scholar
  33. Ruby EG, Nealson KH (1976) Symbiotic association of Photobacterium fischeri with the marine luminous fish Monocentris japonica: A model of symbiosis based on bacterial studies. Biol Bull 151:574–586CrossRefGoogle Scholar
  34. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467CrossRefGoogle Scholar
  35. Silvester CF, Fowler HW (1926) A new genus and species of phosphorescent fish, Kryptophanaron alfredi. Proc Acad Natl Sci Philadelphia 78:245–247Google Scholar
  36. Stahl DA, Lane DJ, Olsen GJ, Pace NR (1984) Analysis of hydrothermal vent-associated symbionts by ribosomal RNA sequences. Science 14:409–411CrossRefGoogle Scholar
  37. Thomas GM, Poinar GO (1979) Xenorhabdus gen. nov., a genus of entomopathogenic, nematophilic bacteria of the family Enterobacteriaceae. Int J Syst Bacteriol 29:352–360CrossRefGoogle Scholar
  38. Yang Y, Yeh LP, Cao L, Baumann P, Baumann JS Tang, Beaman B (1983) Characterization of marine luminous bacteria isolated of the coast of China and description of Vibrio orientalis sp. nov. Curr Microbiol 8:95–100CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • Margo G. Haygood
    • 1
    • 2
  1. 1.Marine Biology Research Division, A-002, Scripps Institution of OceanographyUniversity of California, San DiegoLa JollaUSA
  2. 2.Center for Molecular GeneticsUniversity of California, San DiegoLa JollaUSA

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