Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences

Inter-generational transmission of microbial symbionts in the marine sponge Chondrilla australiensis (Demospongiae)

Kayley M. Usher A E , David C. Sutton A , Simon Toze B , John Kuo C and Jane Fromont D
+ Author Affiliations
- Author Affiliations

A Discipline of Microbiology, School of Biomedical and Chemical Sciences, University of Western Australia, M502, 35 Stirling Highway, Crawley, WA 6009, Australia.

B CSIRO Land and Water, Private Bag No. 5, PO Wembley, Wembley, WA 6913, Australia.

C Centre for Microscopy and Microanalysis, University of Western Australia, M010, 35 Stirling Highway, Crawley, WA 6009, Australia.

D Western Australian Museum, Locked Bag 49, Welshpool, WA 6986, Australia.

E Corresponding author. Email:

Marine and Freshwater Research 56(2) 125-131
Submitted: 27 December 2004  Accepted: 8 February 2005   Published: 12 April 2005


Mechanisms for the biparental transmission of microbial symbionts to offspring in the marine sponge Chondrilla australiensis are reported. The observation of microbial mutualists in the sperm of C. australiensis is the first report of this kind in any organism, as far as we are aware. The developing eggs were shown by transmission electron microscopy (TEM) to incorporate intercellular cyanobacterial and bacterial symbionts. Nurse cells appeared to transport cyanobacterial symbionts from the surface layers of the sponge to eggs deeper in the matrix, where they were incorporated into the egg cytoplasm prior to spawning. This suggests that a host mechanism exists to actively recognise and incorporate symbionts, ensuring that larvae contain these mutualists before settlement. In addition, an average of 1.64% of mature sperm of C. australiensis contained cyanobacterial symbionts in their cytoplasm. The successful transmission of cyanobacterial symbionts to larvae was demonstrated by autofluorescent microscopy and TEM. The occurrence of organisms with functional mechanisms for transmission of symbionts from both parents to offspring provides the potential for new insights into the nature of host–symbiont interactions.

Extra keywords: cyanobacteria, symbiosis, Synechococcus spongiarum, vertical transmission.


We would like to thank the Australasian Diving Academy, Claremont, Western Australia, for subsidising diving expenses and Dr Kathy Heel for assistance with flow cytometry. This study was supported by a grant from the Australian Biological Resources Study.


Afzelius, B. A. , Alberti, G. , Dallai, R. , Godula, J. , and Witalinski, W. (1989). Virus and rickettsia-infected sperm cells in arthropods. Journal of Invertebrate Research 53, 365–377.
CrossRef |

Arillo, A. , Bavestrello, G. , Burlando, B. , and Sarà, M. (1993). Metabolic integration between symbiotic cyanobacteria and sponges: a possible mechanism. Marine Biology 117, 159–162.
CrossRef |

Cheshire, A. C. , Wilkinson, C. R. , Seddon, S. , and Westphalen, G. (1997). Bathymetric and seasonal changes in photosynthesis and respiration of the phototrophic sponge Phyllospongia lamellosa in comparison with respiration by the heterotrophic sponge Ianthella basta on Davies Reef, Great Barrier Reef. Marine and Freshwater Research 48, 589–599.
CrossRef |

Dey J., Aravena-Roman M., Mee B. J., Fromont J., and Sutton D. C. (2004). Bacterial diversity and antibiotic activity in temperate Australian marine sponges. In ‘Proceedings of the 6th International Sponge Conference, Rapallo, Italy 2002’. (Eds M. Pansini, R. Pronzato, G. Bavestrello and R. Manconi.) pp. 263–277. Bollettino del Musei e deggli Instituti Biologici dell’Universita di Genoa.

Diaz M. C. (1996). Molecular and ecological studies of sponge-microbial associations. Ph.D. Thesis, University of California, Santa Cruz, CA.

Diaz M. C. (1999). Perspectives on sponge-cyanobacterial symbioses. In ‘Proceedings of the 5th International Sponge Symposium, 1998, Brisbane’. (Ed. J. N. A. Hooper.) Memoirs of the Queensland Museum, Vol. 44. p. 154. [Abstract]

Diaz, M. C. , and Ward, B. B. (1997). Sponge-mediated nitrification in tropical benthic communities. Marine Ecology Progress Series 156, 97–107.

Edgar G. J. (1997). Kingdom Animalia. Phylum Porifera. In ‘Australian Marine Life: The Plants and Animals of Temperate Waters’. p. 115. (Reed Books: Melbourne, Australia.)

Frank, S. A. (1996). Host-symbiont conflict over the mixing of symbiotic lineages. Proceedings of the Royal Society of London. Series B. Biological Sciences 263, 339–344.

Gaino, E. , and Sarà, M. (1994). An ultrastructural comparative study of the eggs of two species of Tethya (Porifera, Demospongiae). Invertebrate Reproduction & Development 26, 99–106.

Gaino, E. , Burlando, B. , Buffa, P. , and Sarà, M. (1987). Ultrastructural study of the mature egg of Tethya citrina Sarà and Melone (Porifera, Demospongiae). Gamete Research 16, 259–265.
CrossRef | PubMed |

Gallissian, M.-F. , and Vacelet, J. (1976). Ultrastructure de quelques stades de l’ovogenènse de spongiaires du genre Verongia (Dictyoceratida). Annales des Sciences Naturelles Zoologie et Biologie Animale 18, 381–404.

Herre, E. A. , Knowlton, N. , Mueller, U. G. , and Rehner, S. A. (1999). The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends in Ecology & Evolution 14, 49–53.
CrossRef | PubMed |

Hinde R. (1986). Symbiosis between aquatic invertebrates and algae. In ‘Parasitology-Quo Vadit?’ (Ed. M. J. Howell.) pp. 383–390. (Australian Academy of Science: Canberra, Australia.)

Hoekstra R. F. (1990). Evolution of unipatental inheritance of cytoplasmic DNA. In ‘Organizational Constraints on the Dynamics of Evolution’. (Eds J. Maynard Smith and G. Vida.) pp. 269–280. (Manchester University Press: Manchester, UK.)

Kaye, H. R. (1991). Sexual reproduction in four Caribbean commercial sponges. 11. Oogenesis and transfer of bacterial symbionts. Invertebrate Reproduction & Development 19, 13–24.

Law, R. , and Hutson, V. (1992). Intracellular symbionts and the evolution of uniparental cytoplasmic inheritance. Proceedings of the Royal Society of London. Series B. Biological Sciences 248, 69–77.

Lévi, C. , and Lévi, P. (1976). Embryogenèse de Chondrosia reniformis (Nardo), Démosponge ovipare, et transmission des bactéries symbiontiques. Annales des Sciences Naturelles Zoologie et Biologie Animale 18, 367–380.

Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. The Journal of Cell Biology 17, 208–212.
CrossRef | PubMed |

Sarà, M. , Bavestrello, G. , Cattaneo-Vietti, R. , and Cerrano, C. (1998). Endosymbiosis in sponges: relevance for epigenesis and evolution. Symbiosis 25, 57–70.

Scalera Liaci, L. , Sciscioli, M. , and Materrese, A. (1971). La reproduzione sessuale di alcuni Tetractinomorpha (Porifera). Atti Della Societa Peloritana De Scienze Fisiche Matematiche E Naturale 17, 235–245.

Scalera Liaci, L. , Sciscioli, M. , and Matarrese, A. (1973). Raffronto tra il comportamento sessuale di alcune Ceractinomorpha. Revista di Biologica 66, 135–153.

Sciscioli, M. , Scalera Liaci, L. , Lepore, E. , and Gherardi, M. (1989). Indagine ultrastrutturale sugli ovociti di Erylus discophorus. (Schmidt) (Porifera, Tetractinellida). Oebalia 15, 939–941.

Sciscioli, M. , Scalera Liaci, L. , Lepore, E. , Gherardi, M. , and Simpson, T. L. (1991). Ultrastructural study of the mature egg of the marine sponge Stelletta grubii (Porifera Demospongiae). Molecular Reproduction and Development 28, 346–350.
CrossRef | PubMed |

Sciscioli, M. , Lepore, E. , Gherardi, M. , and Scalera Liaci, L. (1994). Transfer of symbiotic bacteria in the mature oocyte of Geodia cydonium (Porifera, Demosponsgiae): an ultrastructural study. Cahiers de Biologie Marine 35, 471–478.

Sears, B. B. (1980). Elimination of plastids during spermatogenesis and fertilization in the plant kingdom. Plasmid 4, 233–255.
CrossRef | PubMed |

Simpson T. L. (1984). Chapter 7. Gamete, embryo, larval development. In ‘The Cell Biology of Sponges’. pp. 341–413. (Springer-Verlag: Berlin.)

Spurr, A. R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructure Research 26, 31–43.
CrossRef | PubMed |

Unson, M. D. , Holland, N. D. , and Faulkner, D. J. (1994). A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Marine Biology 119, 1–11.
CrossRef |

Usher, K. M. , Kuo, J. , Fromont, J. , and Sutton, D. C. (2001). Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461, 15–23.
CrossRef |

Usher, K. M. , Fromont, J. , Sutton, D. C. , and Toze, S. (2004a). The biogeography and phylogeny of unicellular cyanobacterial symbionts in selected sponges from Australia and the Mediterranean. Microbial Ecology 48, 167–177.
CrossRef | PubMed |

Usher, K. M. , Sutton, D. C. , Toze, S. , Kuo, J. , and Fromont, J. (2004b). Sexual reproduction in Chondrilla australiensis (Porifera; Demospongiae). Marine and Freshwater Research 55, 123–134.
CrossRef |

Usher, K. M. , Sutton, D. C. , Toze, S. , Kuo, J. , and Fromont, J. (2004c). The biogeography and phylogeny of Chondrilla species (Demospongiae) in Australia. Marine Ecology Progress Series 270, 117–127.

Usher, K. M. , Toze, S. , Fromont, J. , Kuo, J. , and Sutton, D. C. (2004d). A new species of cyanobacterial symbiont from the marine sponge Chondrilla nucula. Symbiosis 36, 183–192.

Vacelet, J. (1975). Étude en microscopie électronique de l’association entre bactéries et spongiaires du genre Verongia (Dictyoceratida). Journal de Microscopie et de Biologie Cellulaire 23, 271–288.

Vacelet, J. , Fiala-Médioni, A. , Fisher, C. R. , and Boury-Esnault, N. (1996). Symbiosis between methane-oxidizing bacteria and a deep-sea carnivorous cladorhizid sponge. Marine Ecology Progress Series 145, 77–85.

Wilkinson C. R. (1979). Nutrient translocation from symbiotic cyanobacteria to coral reef sponges. In ‘Colloques Internationaux du CNRS. No 291. Biologie des Spongiaries’. (Eds C. Levi and N. Boury-Esnault.) pp. 373–380. (Editions du Centre national de la recherche scientifique: Paris.)

Wilkinson, C. R. (1984). Immunological evidence for the Precambrian origin of bacterial symbiosis in marine sponges. Proceedings of the Royal Society of London. Series B. Biological Sciences 220, 509–517.

Wilkinson, C. R. (1987). Significance of microbial symbionts in sponge evolution and ecology. Symbiosis 4, 135–146.

Wilkinson C. R. (1992). Symbiotic interactions between marine sponges and algae. In ‘Algae and Symbiosis: Plants, Animals, Fungi, Viruses. Interactions Explored’. (Ed. W. Reisser.) pp. 112–151. (Biopress Ltd: Bristol, UK.)

Wilkinson C. R., and Garrone R. (1980). Nutrition of marine sponges. Involvement of symbiotic bacteria in the uptake of dissolved carbon. In ‘Nutrition in the Lower Metazoa’. (Eds D. C. Smith and Y. Tiffon.) pp. 157–161. (Pergamon Press: Oxford, UK.)

Yamamura, N. (1993). Vertical transmission and evolution of mutualism from parasitism. Theoretical Population Biology 44, 95–109.
CrossRef |

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