1887

Abstract

Several rickettsia-like diseases have been reported in arthropods (insects and crustaceans), some of which result in significant losses of economically important species such as shrimp and crabs. This study reports on the molecular pathology of a recently emerged disease of the European shore crab, , termed milky disease – named as a result of the unusual milky appearance of the haemolymph (blood). This disease was more prevalent (>26 %) during summer months when the water temperature in a pilot crab farm was approximately 19 °C. The putative causative agent of the disease was a Gram-negative bacterium that could not be cultured on a range of agar-based growth media. Diseased crabs showed significant reductions in free blood cell numbers and total serum protein. Such animals also displayed raised levels of glucose and ammonium in blood. Ultrastructural and hybridization studies revealed that the causative agent associated with milky disease multiplied in the fixed phagocytes of the hepatopancreas (digestive gland), ultimately to be released into the haemolymph, where the circulating blood cells showed little response to the presence of these agents. Attempts to induce the infection by short-term temperature stress failed, as did transmission experiments where healthy crabs were fed infected tissues from milky disease affected individuals. Sequence analysis of the 16S rRNA gene from the milky disease bacteria indicated that they are a previously undescribed species of -proteobacteria with little phylogenetic similarity to members of the order Rickettsiales.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/008391-0
2007-09-01
2020-04-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/9/2839.html?itemId=/content/journal/micro/10.1099/mic.0.2007/008391-0&mimeType=html&fmt=ahah

References

  1. Alborali L.. 2006; Climatic variations related to fish diseases and production. Vet Res Commun30:Suppl. 193–97
    [Google Scholar]
  2. Au C., Dean P., Reynolds S. E., ffrench-Constant R. H.. 2004; Effect of the insect pathogenic bacterium Photorhabdus on insect phagocytes. Cell Microbiol6:89–95
    [Google Scholar]
  3. Bauchau A. G.. 1981; Crustaceans. In Invertebrate Blood Cellsvol. 2 pp386–420 Edited by Ratcliffe N. A., Rowley A. F.. London: Academic Press Inc;
  4. Bergmeyer H. V.. 1984; Methods of Enzymatic Analysis. Metabolites I: Carbohydrates, 3rd edn. Weinheim: Verlag Chemie;
  5. Boettcher K. J., Geaghan K. K., Maloy A. P., Barber B. J.. 2005; Roseovarius crassostreae sp. nov., a member of the Roseobacter clade and the apparent cause of juvenile oyster disease (JOD) in cultured Eastern oysters. Int J Syst Evol Microbiol55:1531–1537
    [Google Scholar]
  6. Bolz D. F., Howel J. A.. 1978; Colorimetric Determination of Non-Metals London: Wiley;
  7. Brown M. V., Schwalbach M. S., Hewson I., Fuhrman J. A.. 2005; Coupling 16S-ITS rDNA clone libraries and automated ribosomal intergenic spacer analysis to show marine microbial diversity: development and application to a time series. Environ Microbiol7:1466–1479
    [Google Scholar]
  8. Chisholm J. R. S., Smith V. J.. 1994; Variation in antibacterial activity in the haemocytes of the shore crab, Carcinus maenas, with temperature. J Mar Biol Assoc UK74:82–979
    [Google Scholar]
  9. Factor J. A., Naar M.. 1990; The digestive system of the lobster, Homarus americanus: II. Terminal hepatic arterioles of the digestive gland. J Morphol206:283–291
    [Google Scholar]
  10. Friedman C. S., Andree K. B., Beauchamp K. A., Morre J. D., Robbins T. T., Shields J. D., Hedrick R. P.. 2000; ‘Candidatus Xenohaliotis californiensis’, a newly described pathogen of abalone, Haliotis spp., along the west coast of North America. Int J Syst Evol Microbiol50:847–855
    [Google Scholar]
  11. Hall M. R., van Ham E. H.. 1998; The effects of different types of stress on blood glucose in the giant tiger prawn Penaeus monodon. J World Aquacult Soc29:290–299
    [Google Scholar]
  12. Hari R. E., Livingstone D. M., Siber R., Burkhardt-Holm P., Güttinger H.. 2006; Consequences of climatic change for water temperature and brown trout populations in alpine rivers and streams. Global Change Biol12:10–26
    [Google Scholar]
  13. Harvell C. D., Kim K., Burkholder J. M., Colwell R. R., Epstein P. R., Grimes D. J., Hofmann E. E., Lipp E. K., Osterhaus A. D. M. E.. other authors 1999; Emerging marine diseases – climate links and anthropogenic factors. Science285:1505–1510
    [Google Scholar]
  14. Harvell C. D., Mitchell C. E., Ward J. R., Altizer S., Dobson A. P., Ostfeld R. S., Samuel M. D.. 2002; Climate warming and disease risks for terrestrial and marine biota. Science296:2158–2162
    [Google Scholar]
  15. Hebel D. K., Jones M. B., Depledge M. H.. 1997; Responses of crustaceans to contaminant exposure: a holistic approach. Estuarine Coastal Shelf Sci44:177–184
    [Google Scholar]
  16. Johnson P. T.. 1980; Histology of the Blue Crab, Callinectes sapidus. A Model for the Decapoda New York: Praeger Publishers;
    [Google Scholar]
  17. Kimura M.. 1980; A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol16:111–120
    [Google Scholar]
  18. Kumar S., Tamura K., Nei M.. 2004; mega3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform5:150–163
    [Google Scholar]
  19. Lafferty K. D., Porter J. W., Ford S. E.. 2004; Are diseases increasing in the ocean?. Annu Rev Ecol Evol Syst35:31–54
    [Google Scholar]
  20. Lane D. J.. 1991; 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics pp115–175 Edited by Stackebrandt E., Goodfellow M. Chichester: Wiley;
  21. Lau W. W. Y., Armhurst E. V.. 2006; Detection of glycolate oxidase gene glcD diversity among cultured and environmental marine bacteria. Environ Microbiol8:1688–1702
    [Google Scholar]
  22. Le Moullac G., Haffner P.. 2000; Environmental factors affecting immune responses in Crustacea. Aquaculture191:121–131
    [Google Scholar]
  23. Loy J. K., Dewhirst F. E., Weber W., Frelier P. F., Garbar T. L., Tasca S. I., Templeton J. W.. 1996; Molecular phylogeny and in situ detection of the etiologic agent of necrotizing hepatopancreatitis in shrimp. Appl Environ Microbiol62:3439–3445
    [Google Scholar]
  24. Marchesi J. R., Sato T., Weightman J. I., Martin T. A., Fry J. C., Hiom S. J., Wade W. G.. 1998; Design and evaluation of useful bacterium specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol64:795–799
    [Google Scholar]
  25. Nunan L. M., Noble B., Le Groumelle M., Lightner D. V.. 2003; Experimental infection of Penaeus vannamei by a rickettsia-like bacterium (RLB) originating from P. monodon. Dis Aquat Organ54:43–48
    [Google Scholar]
  26. Poulos B. T., Mari J., Bonami J. R., Redman R., Lightner D. V.. 1994; Use of non-radioactively labelled DNA probes for the detection of baculovirus from Penaeus monodon by in situ hybridisation on fixed tissues. J Virol Methods49:187–194
    [Google Scholar]
  27. Powell A., Rowley A. F.. 2007; The effect of dietary chitin supplementation on the survival and immune reactivity of the shore crab, Carcinus maenas. Comp Biochem Physiol A Mol Integr Physiol147:122–128
    [Google Scholar]
  28. Ratcliffe N. A., Rowley A. F., Fitzgerald S. W., Rhodes C. P.. 1985; Invertebrate immunity: basic concepts and recent advances. Int Rev Cytol97:184–350
    [Google Scholar]
  29. Romero X., Turnbull J. F., Jiménez R.. 2000; Ultrastructure and cytopathology of a rickettsia-like organism causing systemic infection in the redclaw crayfish, Cherax quadricarinatus (Crustacea: Decapoda), in Ecuador. . J Invertebr Pathol76:95–104
    [Google Scholar]
  30. Sagrista E., Durfort M.. 1990; Ultrastructural study of hemocytes and phagocytes associated with hemolymphatic vessels in the hepatopancreas of Palaemonetes zariquieyi (Crustacea, Decapoda. J Morphol206:173–180
    [Google Scholar]
  31. Saitou N., Nei M.. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol4:406–425
    [Google Scholar]
  32. Subasinghe R.. 1997; Fish health and quarantine. In Review of the State of World Aquaculture 1997 (FAO Fisheries Circular 886) Rome: FAO;
    [Google Scholar]
  33. Tan C. K.. 1998; The characterization of a Rickettsiales isolated from Cheraxi quadiacarinatus. PhD Thesis James Cook University; Australia:
    [Google Scholar]
  34. Tan C. K., Owens L.. 2000; Infectivity, transmission and 16S rRNA sequencing of a rickettsia, Coxiella cheraxi sp. nov., from freshwater crayfish Cherax quadricarinatus. Dis Aquat Organ41:115–122
    [Google Scholar]
  35. Tops S., Lockwood W., Okamura B.. 2006; Temperature-driven proliferation of Tetracapsuloides bryosalmonae in bryozoan hosts portends salmonid declines. Dis Aquat Organ70:227–236
    [Google Scholar]
  36. Van Handel E.. 1965; Microseparation of glycogen, sugars and lipids. Anal Biochem11:266–271
    [Google Scholar]
  37. Wang F.-I., Chen J.-C.. 2006; The immune response of tiger shrimp Penaeus monodon and its susceptibility to Photobacterium damselae subsp. damselae under temperature stress. Aquaculture258:34–41
    [Google Scholar]
  38. Wickins J. F., Lee D. O'C.. 2002; Crustacean Farming: Ranching and Culture, 2nd edn. Oxford, Blackwell Science:
  39. Yoganandhan K., Thirupathi S., Sahul Hameed A. S.. 2003; Biochemical, physiological and haematological changes in white spot syndrome virus-infected shrimp, Penaeus indicus. Aquaculture221:1–11
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/008391-0
Loading
/content/journal/micro/10.1099/mic.0.2007/008391-0
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error