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RESEARCH ARTICLE
Contents Vol 56(2)

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: kusher@cyllene.uwa.edu.au

Marine and Freshwater Research 56(2) 125-131 https://doi.org/10.1071/MF04304
Submitted: 27 December 2004  Accepted: 8 February 2005   Published: 12 April 2005

Abstract

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.


Acknowledgments

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.


References

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 | GoogleScholarGoogle Scholar | 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.
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.
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 | GoogleScholarGoogle Scholar | PubMed | 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. (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 | GoogleScholarGoogle Scholar |