Vertical Transmission of a Phylogenetically Complex Microbial Consortium in the Viviparous SpongeIrcinia felix

Abstract

Many marine demosponges contain large amounts of phylogenetically complex yet highly sponge-specific microbial consortia within the mesohyl matrix, but little is known about how these microorganisms are acquired by their hosts. Settlement experiments were performed with the viviparous Caribbean demosponge Ircinia felix to investigate the role of larvae in the vertical transmission of the sponge-associated microbial community. Inspections by electron microscopy revealed large amounts of morphologically diverse microorganisms in the center of I. felix larvae, while the outer rim appeared to be devoid of microorganisms. In juveniles, microorganisms were found between densely packed sponge cells. Denaturing gradient gel electrophoresis (DGGE) was performed to compare the bacterial community profiles of adults, larvae, and juvenile sponges. Adults and larvae were highly similar in DGGE band numbers and banding patterns. Larvae released by the same adult individual contained highly similar DGGE banding patterns, whereas larvae released by different adult individuals showed slightly different DGGE banding patterns. Over 200 bands were excised, sequenced, and phylogenetically analyzed. The bacterial diversity of adult I. felix and its larvae was comparably high, while juveniles showed reduced diversity. In total, 13 vertically transmitted sequence clusters, hereafter termed "IF clusters," that contained sequences from both the adult sponge and offspring (larvae and/or juveniles) were found. The IF clusters belonged to at least four different eubacterial phyla and one possibly novel eubacterial lineage. In summary, it could be shown that in I. felix, vertical transmission of microorganisms through the larvae is an important mechanism for the establishment of the sponge-microbe association.Sponges (Porifera) are evolutionarily ancient metazoa that first appeared in Precambrian times nearly 600 million years ago (28). Today, an estimated 13,000 species, classified in three classes (Demospongiae, Calcarea, and Hexactinellida) populate virtually all aquatic habitats from shallow tropical reefs to the polar seas and the deep ocean and even freshwater lakes and rivers (20). A great diversity of sponges occurs on coral reefs, where they exhibit a wide range of shapes and colors. Sponges have a primitive morphology, as they lack true organs or tissues. Instead, sponges possess totipotent, mobile cells freely scattered in an extracellular matrix called the mesohyl, which is covered by a single cell layer, the pinacoderm. Inhalant and exhalant canals in the mesohyl build an aquiferous system through which water is pumped actively by flagellated choanocytes (3). As filter feeders, sponges efficiently take up nutrients like organic particles and microorganisms from the seawater, leaving the expelled water essentially sterile (37,39,57). Reproduction occurs either oviparously or viviparously. In oviparous sponges, gametes are released into the water during large, synchronized spawning events, with fertilization occurring outside the ...

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).…”

The HMA-LMA Dichotomy Revisited: an Electron Microscopical Survey of 56 Sponge Species

“…A typical HMA sponge contains 10 8 to 10 10 microorganisms/g sponge tissue, which can make up to 20%-35% of the sponge biomass (Reiswig, 1981;Webster et al, 2001;Hentschel et al, 2012); in contrast, only 10 5 to 10 6 bacteria/g sponge tissue are found in LMA sponges, which is roughly equivalent to the microbial abundances in seawater (Hentschel et al, 2006). This pattern extends to reproductive propagules in that the larvae of HMA sponges contain dense bacterial assemblages at the larval center, while the interior of LMA sponge larvae is largely free of microbes (Ereskovsky and Tokina, 2004;Maldonado, 2007;Schmitt et al, 2007;Gloeckner et al, 2013a, b). Vertical microbial transmission from the parent to the larva, a hallmark of symbiotic hostmicrobe associations (Bright and Bulgheresi, 2010), is now considered an important and presumably evolutionarily ancient component of HMA sponge symbioses.…”

Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential

“…Similarly diverse microbial communities were found in larvae of the sponges Corticium sp. (366) and Ircinia felix (352), using 16S rRNA-based approaches, such as gene libraries, FISH, and DGGE. Broad congruence between larva-and adult-associated microbial communities in these studies indicated that a significant subset of the resident microbes is transferred in this way.…”