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

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.

Endosymbiotic Yeast Maternally Transmitted in a Marine Sponge

“…1a-c; 2a). The latter, which occur at densities of 4.4 Ϯ 2.3 cells per 10 m 2 , are virtually identical to those described as "complex yolk bodies" in the eggs of both Mediterranean populations of Chondrilla nucula (Gaino, 1980) and the Australian C. australiensis (Usher et al, 2001(Usher et al, , 2004b. However, the chitin-targeted gold marker selectively labeled the electronclear envelope of these presumed yolk inclusions, revealing that they are fungus cells rather than yolk (Fig.…”

“…Previous investigations of microsymbionts in Mediterranean Chondrilla nucula (Gaino, 1980) and in Pacific C. australiensis (Usher et al, 2001(Usher et al, , 2004b reported abundant symbiotic bacteria and cyanobacteria in both adult tissues and eggs, but no presence of fungi. However, these reports documented subspherical yolk inclusions that are virtually identical in size and substructure to the endosymbiotic yeast described herein.…”

Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges

“…Such a co-speciation pattern, where closely related sponges contain more similar microbial communities compared with distantly related sponges, would be expected if sponge symbionts were strictly transmitted via reproductive stages to the next generation. Vertical transmission of single lineages and of complex microbial communities has been shown for several sponges including some of the species investigated in this study (Usher et al, 2001;Oren et al, 2005;Enticknap et al, 2006;Schmitt et al, 2007;Sharp et al, 2007). However, it was previously proposed that vertical transmission is not the only mechanism of symbiont acquisition and that sponge symbionts may additionally be acquired from the seawater (Taylor et al, 2007;Schmitt et al, 2008;Webster et al, 2010).…”

Biogeography and phylogeny of Chondrilla species (Demospongiae) in Australia

“…It is possible that the presence of symbiotic cyanobacteria in the eggs of C. australiensis (Usher et al 2001) may increase the survival time and dispersal ability of both the eggs and larvae of this sponge in the water column by providing photosynthates, as suggested for the larvae of corals that contain algae (Richmond 1990). …”

“…Individuals of Chondrilla australiensis were observed fragmenting hand-sized pieces during the late austral summer period, when they are developing gametes (Usher et al 2001), and eggs have been found in drifting fragments of both C. australiensis and Chondrilla sp. 2 (K. M. Usher & J. Fromont pers.…”