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Appl. Environ. Microbiol. doi:10.1128/AEM.00878-08
Copyright (c) 2008, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts

Susanne Schmitt*, Hilde Angermeier, Roswitha Schiller, Niels Lindquist, and Ute Hentschel

University of Wuerzburg, Research Center for Infectious Diseases, Roentgenring 11, D-97070 Wuerzburg, Germany; University of North Carolina at Chapel Hill, Institute of Marine Sciences, 3431 Arendell Street, Morehead City, NC 28557, USA

* To whom correspondence should be addressed. Email: s.schmitt{at}auckland.ac.nz.


   Abstract

Many marine sponges, hereafter termed "high microbial abundance" (HMA) sponges, harbour large and complex microbial consortia including bacteria and archaea within their mesohyl matrix. To investigate vertical microbial transmission as a strategy to maintain these complex associations an extensive phylogenetic analysis was carried out with 16S rRNA gene sequences of reproductive (n=136) and adult (n=88) material from 5 different Caribbean species, as well as all published 16S rRNA gene sequences from sponge offspring (n=116). The overall microbial diversity in sponge reproductive stages is high including members of at least 13 bacterial and one archaeal phyla. In total, 28 vertical transmission (VT)-clusters, defined as clusters of phylotypes that are found both in the adult sponge and its offspring, were identified. They are distributed among at least 10 bacterial and one archaeal phyla demonstrating that the complex adult microbial community is collectively transmitted through reproductive stages. An indication of host species-specificity and cospeciation was not observed. Mechanistic insights were provided using a combined electron microscopy (TEM) and fluorescence in-situ hybridization (FISH) analysis and an indirect mechanism of vertical transmission via nurse cells is proposed for the oviparous sponge Ectyoplasia ferox. Based on these phylogenetic and mechanistic results we suggest the following "symbiont transmission model": entire microbial consortia are vertically transmitted in sponges. While vertical transmission is clearly present, additional environmental transfer between adult individuals of the same and even different species might obscure possible signals of cospeciation. We propose that associations of HMA sponges with highly sponge-specific microbial communities are maintained by this combination of vertical and horizontal symbiont transmission.







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