Vertical transmission and successive location of symbiotic bacteria during embryo development and larva formation in Corticium candelabrum (Porifera: Demospongiae)

Abstract

This study reports on the transfer of heterotrophic bacteria from parental tissue to oocytes in the Mediterranean bacteriosponge Corticium candelabrum (Homosclerophorida) and the description of the successive locations of the microsymbionts during embryo development through transmission and scanning electron microscopy. Eight different types of symbiotic bacteria are described morphologically. These eight bacteria morphotypes are found in both adult individuals and larvae. Symbiotic bacteria are transferred to oocytes, but not to spermatocytes. Bacteria are first located at the oocyte periphery below a thick collagen layer and then they migrate to the oocyte cytoplasm, forming spherical clusters. After cleavage, the bacteria can be found in the free space between blastomeres but mainly accumulate at the embryo periphery below the follicular cells that surround the embryo. Once the blastocoel is formed, the symbiotic bacteria move to this central cavity where they actively divide by bipartition, increasing their number considerably. Many examples of phagocytosed bacteria in the proximal zone of the larval cells are observed at this stage. Consequently, bacteria may represent a complementary source of energy for free larvae and settlers before they are able to capture food from the surrounding water.

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

“…Innate immune genes are of interest because of their hypothesized roles in invertebrates in establishing and maintaining bacterial symbiont communities (Nyholm and Graf, 2012). As discussed above, both our histological data and that of other studies report that phagocytosis of symbionts can occur at least during the larval stage in some sponge species (Ereskovsky and Tokina, 2004;de Caralt et al, 2007). It is unknown whether this occurs because larvae do not yet possess a well-developed immune system to select for or against specific types of bacteria, or because the bacteria themselves lack mechanisms to evade detection and consumption.…”

“…Despite the phagocytosis, abundance of the OTU 1 morphotype increases substantially from embryonic to larval stages, and we continue to see evidence of phagocytosis in the free-swimming larvae. Other studies have also reported phagocytosis of symbionts during the larval stage, and the use of symbiotic bacteria as a nutrition source in the non-feeding sponge larva has been suggested to contribute to lengthening the planktonic phase or even to increasing settlement success of competent larvae (Ereskovsky and Tokina, 2004;de Caralt et al, 2007). In the context of the latter proposition, it is interesting that, in A. queenslandica, OTU 1 constitutes as much as 85% of the total microbiome of larvae that have developmentally matured such that they are competent to settle.…”

“…In an ontogenetic context, numerous studies have demonstrated vertical inheritance of putatively core symbionts during development of embryos and larvae, based on evidence from electron microscopy (see for example Ereskovsky et al, 2005;Oren et al, 2005;Maldonado, 2007;Schmitt et al, 2008) or sequencing of prokaryotic 16S rRNA gene amplicons (see for example Oren et al, 2005;Enticknap et al, 2006;Schmitt et al, 2007Schmitt et al, , 2008Sharp et al, 2007;Steger et al, 2008;Lee et al, 2009;Webster et al, 2010;Gloeckner et al, 2012). Horizontal transmission, characterized by de novo symbiont acquisition from the environment with each new generation, has also been identified in several sponges (de Caralt et al, 2007;Maldonado, 2007;Schmitt et al, 2007;Gloeckner et al, 2013) and could include the introduction into the microbiome of opportunistic, non-core bacterial species. In the absence of complete ontogenetic perspectives, however, the nature and extent of microbiome compositional changes through the host life cycle are unknown, including whether fidelity of core, vertically-inherited symbionts is challenged at any stage.…”

Latitudinal variation in the microbiome of the sponge Ircinia campana correlates with host haplotype but not anti-predatory chemical defense

“…In host-associated micro bial communities, dispersal is dictated by transmission mode: the passage of symbiont taxa via vertical (parent-to-offspring) or horizontal (environmental acquisition) means. Vertical symbiont transmission is documented in numerous sponges (Ereskovsky et al 2005, Oren et al 2005, Enticknap et al 2006, de Caralt et al 2007, Sharp et al 2007, Lee et al 2009, Schöttner et al 2013, including the genus Ircinia (Schmitt et al 2007), and links the evolutionary trajectory of host and symbiont. Accordingly, reproductive isolation of host populations may restrict (Marty & Pawlik 2015), indicated by the dashed line the exchange of vertically transmitted microbes or genes that regulate the microbiome between host populations, resulting in divergent microbial communities over time (Schöttner et al 2013, Easson & Thacker 2014.…”

Evidence for Vertical Transmission of Bacterial Symbionts from Adult to Embryo in the Caribbean SpongeSvenzea zeai

“…(25), Spongia sp. (25), Halisarca dujardini (10), and Corticium candelabrum (8). However, all of these studies employed transmission and scanning electron microscopy and could only examine the presence of bacteria in maternal sponges, oocytes, or larvae at the morphological level, with no determination of microbial identity.…”