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Association between the mollusc bivalve Loripes lucinalis and a Chlamydia-like organism, with comments on its pathogenic impact, life cycle and possible mode of transmission

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Abstract

Loripes lucinalis is a littoral bivalve which has already been confirmed to harbour endo-cellular sulfur-oxidizing bacteria within its gills. Examination of the digestive gland of L. lucinalis collected from the Moulin Blanc Beach in the Bay of Brest (Brittany, France) revealed the existence of an additional association involving a Chlamydia-like organism. Three different forms of Chlamydia-like bacteria were observed: reticulate rod-shaped cells, electron-dense cells and enlarged cells. The reticulate rod-shaped cells and the electron-dense bodies are thought to represent the germinal initial body and infectious form of the bacteria, respectively. The enlarged cells were always associated with what are believed to be spherical or icosahedral phages. Initial infestation seems to occur by phagocytosis at the apical pole of the digestive cells of the tubule and duct epithelia. Within the host cell, the bacteria undergo binary fission and budding, forming an inclusion which gradually fills up the cell. Inclusions are generally between 15 and 30 μm in size, and > 85% of all individuals examined possessed inclusion bodies. The level of infestation varied between individuals, some being heavily colonized, but did not seem to be related to season. Histological and ultrastructural observations suggest that, once developed, the colony has three possible fates: (1) the cells will degenerate due to phage infection; (2) colony overcrowding will occur, causing the development of electron-dense bodies that will be released into the lumen; (3) the entire membrane-bound inclusion will be released into the lumen and subsequently into the pallial cavity. Inclusions within the pallial cavity may be ingested by the host or may even be phagocytized by bacteriocyte cells of the gill. It is proposed that this association could be a form of symbiosis and that L. lucinalis may, therefore, be a rare example of an organism adapted to harbour two very different symbioses.

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References

  • Bouvy M, Soyer J, Cahet G, Descolas-Gros C, Thiriot-Quiévreux C, Soyer-Gobillard MO (1989) Chemoautotrophic metabolism of intracellular gill bacteria in the marine bivalve Spisula subtruncata (da Costa). Neth J Sea Res 23: 29–34

    Google Scholar 

  • Buchanan JS (1978) Cytological studies on a new species of Rickettsia found in association with a phage in the digestive gland of the marine bivalve mollusc, Tellina tenuis (da Costa). J Fish Dis 1: 27–43

    Google Scholar 

  • Buchanan JS (1979) Ultrastructural studies of a Rickettsia-like organism (with phage) from the digestive gland of the marine bivalve, Tellina tenuis (da Costa). Haliotis 1977(8):309–316

    Google Scholar 

  • Cajaraville MP, Angulo E (1991) Chlamydia-like organisms in digestive and duct cells of mussels from the Basque coast. J Invert Path 58: 381–386

    Google Scholar 

  • Cary SC, Vetter RD, Felbeck H (1989) Habitat characterization and nutritional strategies of the endosymbiont-bearing bivalve Lucinoma aequizonata. Mar Ecol Prog Ser 55:31–45

    Google Scholar 

  • Cavanaugh CM (1983) Symbiotic chemoautotrophic bacteria in marine invertebrates from sulphide-rich habitats. Nature, Lond 302(5903): 58–61

    Google Scholar 

  • Charlesworth B (1991) Living together. Nature, Lond 352: p. 391

    Google Scholar 

  • Comps M (1983) Etude morphologique d'une infection rickettsienne de la palourde Ruditapes philippinarum Adam et Reeves. Revue Trav Inst (scient tech). Pêch marit 46: 141–145

    Google Scholar 

  • Conway NM, Howes BL, McDowell Capuzzo JE, Turner RD, Cavanaugh CM (1992) Characterization and site description of Solemya borealis (Bivalvia; Solemyidae), another bivalvebacteria symbiosis. Mar Biol 112: 601–613

    Google Scholar 

  • Dando PR, Southward AJ (1986) Chemoautotrophy in bivalve molluscs of the genus Thyasira. J mar biol Ass UK 66: 915–929

    Google Scholar 

  • Dando PR, Southward AJ, Southward EC (1986) Chemoautotrophic symbionts in the gills of the bivalve mollusc Lucinoma borealis and the sediment chemistry of its habitat. Proc R Soc 227: 227–247

    Google Scholar 

  • Dando PR, Southward AJ, Southward EC, Terwilliger NB, Terwilliger RC (1985) Sulphur-oxidizing bacteria and haemoglobin in gills of the bivalve mollusc Myrtea spinifera. Mar Ecol Prog Ser 23: 85–98

    Google Scholar 

  • Diouris M, Moraga D, Le Pennec M, Herry A, Donval A (1988) Chimioautotrophie et nutrition chez les Lucinacea, bivalves littoraux de milieux réducteurs. I. Activités enzymatiques des bactéries chimioautotrophes associées aux branchies. Haliotis 18: 195–205

    Google Scholar 

  • Distel DL, Felbeck H (1987) Endosymbiosis in the lucinid clams Lucinoma aequizonata, Lucinoma annulata and Lucinoma floridana: a reexamination of the functional morphology of the gills as bacteria-bearing organs. Mar Biol 96:79–86

    Google Scholar 

  • Donval A, Le Pennec M, Herry A, Diouris M (1989) Nutritional adaptations of littoral bivalve molluscs to reducing biotopes. In: Ryland JS, Tyler PA (eds) Reproduction, genetics and distribution of marine organisms. Olsen, Fredensborg. Denmark, pp 373–378

    Google Scholar 

  • Elston R (1986) Occurrence of branchial rickettsiales-like infections in two bivalve molluscs, Tapes japonica and Patinopecten yessoensis, with comments on their significances. J Fish Dis 9: 69–71

    Google Scholar 

  • Elston RA, Peacock MG (1984) A rickettsiales-like infection in the Pacific razor clam, Siliqua patuld. J Invert Path 44: 84–96

    Google Scholar 

  • Felbeck H, Childress JJ, Somero GN (1981) Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats. Nature, Lond 293: 291–293

    Google Scholar 

  • Fiala-Médioni A, Alayse AM, Cahet G (1986) Evidence of in situ uptake and incorporation of bicarbonate and amino acids by a hydrothermal vent mussel. J exp mar biol Ecol 96: 191–198

    Google Scholar 

  • Fisher CR (1990) Chemoautotrophic and methanotrophic symbiosis in marine invertebrates. Rev aquat Sciences 2: 399–436

    Google Scholar 

  • Fisher MR, Hand SC (1984) Chemoautotrophic symbionts in the bivalve Lucina floridana from seagrass beds. Biol Bull mar biol Lab, Woods Hole 167: 445–459

    Google Scholar 

  • Fries CR, Grant DM (1991) Rickettsiae in gill epithelial cells of the hard clam, Mercenaria mercenaria. J Invert Path 57: 166–171

    Google Scholar 

  • Fries CR, Grant DM (1992) Ehrlichia-like microorganisms in hemocytes in the gills of the marine bivalve, Mercenaria mercenaria. J Invert Path 59: 210–211

    Google Scholar 

  • Fries CR, Grau SB, Tripp MR (1991) Rickettsiae in the cytoplasm of gill epithelial cells of the soft-shelled clam, Mya arenaria. J Invert Path 57: 443–445

    Google Scholar 

  • Gabe M (1968) Techniques histologiques. Paris-VIc, Masson et Cie

    Google Scholar 

  • Harshbarger JC, Chang SC, Otto SV (1976) Chlamydiae (with phages). Mycoplasma and Rickettsiae in Chesapeake Bay bivalves. Science, NY 196: 666–668

    Google Scholar 

  • Herry A (1988) Chimioautotrophie bactérienne dans la branchie de quatre espèces de Lucinacea (Bivalvia). Thèse 3ème cycle Océanographie biologique. Université de Bretagne Occidentale, Brest

    Google Scholar 

  • Herry A, Diouris M, Le Pennec M (1989) Chemoautotrophic symbionts and translocation of fixed carbon from bacteria to host tissues in the littoral bivalve Loripes lucinalis (Lucinidae). Mar Biol 101: 305–312

    Google Scholar 

  • Herry A, Le Pennec M (1987) Ultrastructure of the gonad of a deep hydrothermal vent mytilid from the east Pacific Rise. Haliotis 16: 295–307

    Google Scholar 

  • Herry A, Le Pennec M, Johnson M (1994) Bacteria-host relationships in the bivalve mollusc Loripes lucinalis. Acta Microbiol immunol hung 41: 273–281

    Google Scholar 

  • Joly J, Comps M (1980) Etude d'un micro-organisme de type chlamydien chez la palourde Ruditapes decussatus L. Revue Trav Inst (scient tech) Pêch marit 44: 285–287

    Google Scholar 

  • Le Pennec M, Herry A, Diouris M, Moraga D, Donval A (1988) Chimioautotrophie et nutrition chez les Lucinacea, bivalves littoraux de milieux réducteurs. II. Caractéristiques morphologiques des bactéries symbiotiques et modifications structurales adaptives des branchies de l'hôte. Haliotis 18: 207–217

    Google Scholar 

  • Morrison C, Shum G (1983) Rickettsia in the kidney of the bay scallop Argopecten irradians (Lamarck). J Fish Dis 6: 537–541

    Google Scholar 

  • Otto SV, Harshbarger JC, Chang SC (1979) Status of selected unicellular eucaryote pathogens, and prevalence and histopathology of inclusions containing obligate procaryote parasites, in commercial bivalve mollusks, from Maryland estuaries. Haliotis 1977(8): 285–295

    Google Scholar 

  • Owen G (1974) Feeding and digestion in the Bivalvia. Adv comp Physiol Biochem 5: 1–35

    Google Scholar 

  • Pappalardo R, Bonami J (1980) Etude histopathologique et ultrastructurale d'une maladie rickettsienne chez le crabe Carcinus mediterranens czerniavski (crustacé décapode). Revue Trav Inst (scient tech) Pêch marit 44: 277–283

    Google Scholar 

  • Saffo MB (1991) Symbiosis in evolution. In: Dudley EC (ed) The unity of evolutionary biology. (Proceedings of the Fourth International Congress of Systematic and Evolutionary Biology) Discorides Press, Portland, Oregon, pp 674–680

    Google Scholar 

  • Saffo MB (1992) Coming to terms with a field: words and concepts in symbiosis. Symbiosis 14: 17–31

    Google Scholar 

  • Somero GN, Childress JJ, Aderson AE (1989) Transport, metabolism and detoxification of hydrogen sulfide in animals from sulfide-rich marine environments. Rev aquat Sciences 1: 591–614

    Google Scholar 

  • Southward EC (1986) Gill symbionts in thyasirids and other bivalve molluscs. J mar biol Ass UK 66: 889–914

    Google Scholar 

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Communicated by A. Rodríguez, Puerto Real

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Johnson, M.A., Le Pennec, M. Association between the mollusc bivalve Loripes lucinalis and a Chlamydia-like organism, with comments on its pathogenic impact, life cycle and possible mode of transmission. Marine Biology 123, 523–530 (1995). https://doi.org/10.1007/BF00349231

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  • DOI: https://doi.org/10.1007/BF00349231

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