Skip to main content

Advertisement

Log in

Epibiotic Vibrio Luminous Bacteria Isolated from Some Hydrozoa and Bryozoa Species

  • Original Article
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Luminous bacteria are isolated from both Hydrozoa and Bryozoa with chitinous structures on their surfaces. All the specimens of the examined hydroid species (Aglaophenia kirchenpaueri, Aglaophenia octodonta, Aglaophenia tubiformis, Halopteris diaphana, Plumularia setacea, Ventromma halecioides), observed under blue light excitation, showed a clear fluorescence on the external side of the perisarc (chitinous exoskeleton) around hydrocladia. In the bryozoan Myriapora truncata, luminous bacteria are present on the chitinous opercula. All the isolated luminous bacteria were identified on the basis of both phenotypic and genotypic analysis. The isolates from A. tubiformis and H. diaphana were unambiguously assigned to the species Vibrio fischeri. In contrast, the isolates from the other hydroids, phenotypically assigned to the species Vibrio harveyi, were then split into two distinct species by phylogenetic analysis of 16S rRNA gene sequences and DNA–DNA hybridization experiments. Scanning electron microscopy analysis and results of culture-based and culture-independent approaches enabled us to establish that luminous vibrios represent major constituents of the bacterial community inhabiting the A. octodonta surface suggesting that the interactions between luminous bacteria and the examined hydrozoan and bryozoan species are highly specific. These interactions might have epidemiological as well as ecological implications because of the opportunistic pathogenicity of luminous Vibrio species for marine organisms and the wide-distribution of the hydrozoan and bryozoan functioning as carriers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Alcaide E, Gil Sanz C, Esteve D, Sanjuan D, Amaro C, Silveira L (2001) Vibrio harveyi disease in seahorse, Hippocampus sp. J Fish Dis 2:311–313

    Article  Google Scholar 

  2. Almashanu S, Gendler I, Hadar R, Kuhn J (1996) Interspecific luciferase b subunit hybrids between Vibrio harveyi, Vibrio fischeri and Photobacterium leiognathi. Prot Eng 9:803–809

    Article  CAS  Google Scholar 

  3. Alsina M, Blanch AR (1994) A set of keys for biochemical identification of environmental Vibrio species. J Appl Bacteriol 76:79–85

    PubMed  CAS  Google Scholar 

  4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  5. Baumann P, Baumann L (1984) Genus II. Photobacterium Beijerinck 1889. In: Kreig NR, Holt JG (eds) Bergey's manual of systematic bacteriology, vol. 1. Williams & Wilkins, Baltimore

    Google Scholar 

  6. Baumann P, Baumann L, Bang SS, Woolkalis MJ (1980) Revaluation of the taxonomy of Vibrio, Beneckea, and Photobacterium-abolition of the genus Beneckea. Curr Microbiol 4:127–133

    Article  Google Scholar 

  7. Baumann PS, Schubert RHW (1984) The family II Vibrionaceae Veron. In: Krieg NR (ed) Bergey's manual of systematic bacteriology, vol. 1. Williams & Williams, Baltimore

    Google Scholar 

  8. Berger LR, Reynolds DM (1958) The chitinase system of a strain of Streptomyces griseus. Biochem Biophys Acta 29:522–534

    Article  PubMed  CAS  Google Scholar 

  9. Boero F, Gravili C, Pagliara P, Piraino S, Bouillon J, Schmid V (1998) The cnidarian premises of metazoan evolution: from triploblasty, to coelom formation, to metamere. Ital J Zool 65:5–9

    Article  Google Scholar 

  10. Boettcher KJ, Ruby EG (1990) Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J Bacteriol 172:3701–3706

    PubMed  CAS  Google Scholar 

  11. Bouillon J (1995) Classe des Hydrozoaires (Hydrozoa Owen, 1843). In: Grassé PP, Doumenc D (eds) Traité de Zoologie. Masson, Paris

    Google Scholar 

  12. Bouillon J, Medel MD, Pagès F, Gili JM, Boero F, Gravili C (2004) Fauna of the Mediterranean Hydrozoa. Sci Mar 68:5–438

    Google Scholar 

  13. Brown JK (1994) Bootstrap hypothesis tests for evolutionary trees and other dendrograms. Proc Natl Acad Sci U S A 91:12293–12297

    Article  PubMed  CAS  Google Scholar 

  14. Carli A, Pane L, Casareto L, Bertone S, Pruzzo C (1993) Occurrence of Vibrio alginolyticus in Ligurian coast rock pools (Tyrrhenian Sea, Italy) and its association with the copepod Tigriopus fulvus (Fisher 1860). Appl Environ Microbiol 59:1960–1962

    PubMed  CAS  Google Scholar 

  15. Carman KR, Dobbs FC (1997) Epibiotic microorganisms on copepods and other aquatic crustaceans. Micros Res Tech 37:116–135

    Article  CAS  Google Scholar 

  16. DeLoney CR, Bartley TM, Visick KL (2002) Role for phosphoglucomutase in Vibrio fischeriEuprymna scolopes symbiosis. J Bacteriol 184:5121–5129

    Article  PubMed  CAS  Google Scholar 

  17. Di Giacomo M, Paolino M, Silvestro D, Vigliotta G, Imperi F, Visca P, Alifano P, Parente D (2007) Microbial community structure and dynamics of dark fire-cured tobacco fermentation. Appl Environ Microbiol 73:825–837

    Article  PubMed  CAS  Google Scholar 

  18. Ducklow HW, Mitchell R (1979) Bacterial populations and adaptations in the mucus layers on living corals. Limnol Oceanogr 24:4715–4725

    Google Scholar 

  19. Farmer JJ III, Janda JM, Brenner FW, Cameron DN, Birkhead KM (2005) Genus 1. Vibrio Pacini 1854, 411AL. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey's manual of systematic bacteriology the proteobacteria part B the gammaproteobacteria vol. 2. 2nd edn. Springer, New York

    Google Scholar 

  20. Fletcher M, Marshall KC (1982) Are solid surfaces of ecological significance to aquatic bacteria? Adv Microbial Ecol 6:199–236

    CAS  Google Scholar 

  21. Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548

    PubMed  CAS  Google Scholar 

  22. Garrity G, Brenner DJ, Krieg NR, Staley JR (2005) Bergey's manual of systematic bacteriology, 2nd edn. Williams & Wilkins, Baltimore

    Google Scholar 

  23. Gillis M, De Ley J, De Cleene M (1970) The determination of molecular weight of bacterial genome DNA from renaturation rates. Eur J Biochem 12:143–153

    Article  PubMed  CAS  Google Scholar 

  24. Gomez-Gil B, Soto-Rodríguez S, García-Gasca A, Roque A, Vazquez-Juarez R, Thompson FL, Swings J (2004) Molecular identification of Vibrio harveyi-related isolates associated with diseased aquatic organisms. Microbiology 150:1769–1777

    Article  PubMed  CAS  Google Scholar 

  25. Hood MA, Meyers SP (1977) Microbiological and chitinoclastic activities associated with Penaeus setiferus. J Oceanogr Soc Jpn 33:235–241

    Article  CAS  Google Scholar 

  26. Jawahar AT, Keleemur RM, Leema JMT (1996) Bacterial disease in cultured spiny lobster, Panulirus homarus (Linnaeus). J Aquacult Trop 11:187–192

    Google Scholar 

  27. Johnson CR, Muir DG, Reysenbach AL (1991) Characteristic bacteria associated with surfaces of coralline algae: a hypothesis for bacterial induction of marine invertebrate larvae. Mar Ecol Prog Ser 74:281–294

    Article  Google Scholar 

  28. Kaneko T, Colwell RR (1975) Adsorption of Vibrio parahaemolyticus onto chitin and copepods. Appl Microbiol 29:269–274

    PubMed  CAS  Google Scholar 

  29. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  30. Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci U S A 82:6955–6959

    Article  PubMed  CAS  Google Scholar 

  31. Lavilla-Pitogo CR, Leano EM, Paner MG (1990) Occurrence of luminous bacterial disease of Penaeus monodon larvae in the Philippines. Aquaculture 91:1–13

    Article  Google Scholar 

  32. Lavilla-Pitogo CR, Leano EM, Paner MG (1998) Mortalities of pond-cultured juvenile shrimp, Penaeus monodon, associated with dominance of luminescent vibrios in the rearing environment. Aquaculture 164:337–349

    Article  Google Scholar 

  33. Lee K-H, Ruby EG (1995) Symbiotic role of the viable but nonculturable state of Vibrio fischeri in Hawaiian coastal seawater. Appl Environ Microbiol 61:278–283

    PubMed  CAS  Google Scholar 

  34. Maugeri TL, Carbone M, Fera MT, Irrera GP, Gugliandolo C (2004) Distribution of potentially pathogenic bacteria as free living and plankton associated in a marine coastal zone. J Appl Microbiol 97:354–361

    Article  PubMed  CAS  Google Scholar 

  35. McCann J, Stabb EV, Millikan DS, Ruby EG (2003) Population dynamics of Vibrio fischeri during infection of Euprymna scolopes. Appl Environ Microbiol 69:5928–5934

    Article  PubMed  CAS  Google Scholar 

  36. McConaughy BL, Laird CD, McCarthy BJ (1969) Nucleic acid reassociation in formamide. Biochemistry 8:3289–3295

    Article  PubMed  CAS  Google Scholar 

  37. Nealson HK, Haygood GM, Tebo MB, Roman M, Miller E, McCosker EJ (1984) Contribution by symbiotically luminous fishes to the occurrence and bioluminescence of luminous bacteria in seawater. Microb Ecol 10:69–77

    Article  Google Scholar 

  38. Nishiguchi MK, Ruby EG, McFall-Ngai MJ (1998) Competitive dominance among strains of luminous bacteria provides an unusual form of evidence for parallel evolution in sepiolid squid–Vibrio symbioses. Appl Environ Microbiol 64:3209–3213

    PubMed  CAS  Google Scholar 

  39. Pass DA, Dybdahl R, Mannion MM (1987) Investigation into the causes of mortality of the pearl oyster, Pinctada maxima (Jamson), in Western Australia. Aquaculture 65:149–169

    Article  Google Scholar 

  40. Pizzuto M, Hirst RG (1995) Classification of isolates of Vibrio harveyi virulent to Penaeus monodon larvae by protein profile analysis and M13 DNA fingerprinting. Dis Aquat Org 21:61–68

    Article  Google Scholar 

  41. Pujalte MJ, Ortigosa M, Macian MC, Garay E (1999) Aerobic and facultative anaerobic heterotrophic bacteria associated to Mediterranean oysters and seawater. Int Microbiol 2:259–266

    PubMed  CAS  Google Scholar 

  42. Ramesh A, Venugopalan VK (1984) Colloque International de bactériologie marine. Actes de colloques. IFREMER, CNRS, Brest, pp 1–5

    Google Scholar 

  43. Riedl R (1970) Fauna und Flora der Adria, 2nd edn. Verlag Paul Parey, Hamburg

    Google Scholar 

  44. Rosowski JR (1992) Specificity of bacterial attachment sites on the filamentous diatom Navicula confervacea (Bacillariophyceae). Can J Microbiol 38:676–686

    Article  CAS  Google Scholar 

  45. Roszak DB, Colwell RR (1987) Survival strategies of bacteria in the natural environment. Microbiol Rev 51:365–379

    PubMed  CAS  Google Scholar 

  46. Ruby EG, Lee K-H (1998) The Vibrio fischeriEuprymna scolopes light organ association: current ecological paradigms. Appl Environ Microbiol 64:805–812

    PubMed  CAS  Google Scholar 

  47. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  48. Sambrook J, Russel DW (2001) Molecular cloning in laboratory. Manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  49. Santavy DL, Colwell RR (1990) Comparison of bacterial communities associated with the Caribbean sclerosponge Ceratoporella nicholsoni and ambient seawater. Mar Ecol Prog Ser 67:73–82

    Article  Google Scholar 

  50. Stabili L, Gravili C, Piraino S, Boero F, Alifano P (2006) Vibrio harveyi associated with Aglaophenia octodonta (Hydrozoa, Cnidaria). Microb Ecol 52:603–608

    Article  PubMed  CAS  Google Scholar 

  51. Tamplin ML, Gauzens AL, Huq AL, Sack DA, Colwell RR (1990) Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl Environ Microbiol 56:1977–1980

    PubMed  CAS  Google Scholar 

  52. Thompson FL, Gevers D, Thompson CC, Dawyndt P, Naser S, Hoste B, Munn CB, Swings J (2005) Phylogeny and molecular identification of vibrios on the basis of multilocus sequence analysis. Appl Environ Microbiol 71:5107–5115

    Article  PubMed  CAS  Google Scholar 

  53. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  54. Thompson FL, Hoste B, Vandemeulebroecke K, Engelbeen K, Denys R, Swings J (2002) Vibrio trachuri Iwamoto et al. 1995 is a junior synonym of Vibrio harveyi (Johnson and Shunk 1936) Baumann et al. 1981. Int J Syst Evol Microbiol 52:973–976

    Article  PubMed  CAS  Google Scholar 

  55. Thompson FL, Hoste B, Vandemeulebroecke K, Swings J (2001) Genomic diversity amongst Vibrio isolates from different sources determined by fluorescent amplified fragment length polymorphism. Syst Appl Microbiol 24:520–538

    Article  PubMed  CAS  Google Scholar 

  56. Venkateswaran K, Kim SW, Nakano H, Onbè T, Hashimoto H (1989) The association of Vibrio parahaemolyticus serotypes with zooplankton and its relationship with bacterial indicators of pollution. Syst Appl Microbiol 11:194–201

    Google Scholar 

  57. Vidgen M, Carson J, Higgins M, Owens L (2006) Changes to the phenotypic profile of Vibrio harveyi when infected with the Vibrio harveyi myovirus-like (VHML) bacteriophage. J Appl Microbiol 100:481–487

    Article  PubMed  CAS  Google Scholar 

  58. Vigliotta G, Nutricati E, Carata E, Tredici SM, De Stefano M, Pontieri P, Massardo DR, Prati MV, De Bellis L, Alifano P (2007) Clonothrix fusca Roze 1896, a filamentous, sheathed, methanotrophic gamma-proteobacterium. Appl Environ Microbiol 73:3556–3565

    Article  PubMed  CAS  Google Scholar 

  59. Visick KL, McFall-Ngai MJ (2000) An exclusive contract: specificity in the Vibrio fischeriEuprymna scolopes partnership. J Bacteriol 182:1779–1787

    Article  PubMed  CAS  Google Scholar 

  60. Walls JT, Ritz DA, Blackman MJ (1993) Fouling, surface bacteria and antibacterial agents of four bryozoan species found in Tasmania, Australia. Exp Mar Biol Ecol 169:1–13

    Article  CAS  Google Scholar 

  61. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464

    Article  Google Scholar 

  62. West PA, Colwell RR (1984) Identification and classification of vibrionaceae: an overview. In: Colwell RR (ed) Vibrios in the environment. Wiley, New York

    Google Scholar 

  63. Whistler CA, Ruby EG (2003) GacA regulates symbiotic colonization traits of Vibrio fischeri and facilitates a beneficial association with an animal host. J Bacteriol 185:7202–7212

    Article  PubMed  CAS  Google Scholar 

  64. Zorrilla I, Arijo S, Chabrillon M, Diaz P, Martinez-Manzanares E, Balebona MC, Morinigo MA (2002) Vibrio species isolated from diseased farmed sole, Solea senegalensis. J Fish Dis 26:103–108

    Article  Google Scholar 

Download references

Acknowledgements

Financial support was provided by MURST (COFIN and FIRB projects) and the European Community (MARBEF and IASON networks). Christian Vaglio helped in the field. Thanks are due to Dr. Marcella Elia for the technical assistance in the scanning electron microscopy.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. Stabili.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stabili, L., Gravili, C., Tredici, S.M. et al. Epibiotic Vibrio Luminous Bacteria Isolated from Some Hydrozoa and Bryozoa Species. Microb Ecol 56, 625–636 (2008). https://doi.org/10.1007/s00248-008-9382-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-008-9382-y

Keywords

Navigation