Molecular Microbial Diversity Survey of Sponge Reproductive Stages and Mechanistic Insights into Vertical Transmission of Microbial Symbionts

Abstract

Many marine sponges, hereafter termed high-microbial-abundance (HMA) sponges, harbor large and complex microbial consortia, including bacteria and archaea, within their mesohyl matrices. To investigate vertical microbial transmission as a strategy to maintain these complex associations, an extensive phylogenetic analysis was carried out with the 16S rRNA gene sequences of reproductive (n ‫؍‬ 136) and adult (n ‫؍‬ 88) material from five different Caribbean species, as well as all published 16S rRNA gene sequences from sponge offspring (n ‫؍‬ 116). The overall microbial diversity, including members of at least 13 bacterial phyla and one archaeal phylum, in sponge reproductive stages is high. In total, 28 vertical-transmission clusters, defined as clusters of phylotypes that are found both in adult sponges and their offspring, were identified. They are distributed among at least 10 bacterial phyla and one archaeal phylum, demonstrating that the complex adult microbial community is collectively transmitted through reproductive stages. Indications of host-species specificity and cospeciation were not observed. Mechanistic insights were provided using a combined electron microscopy and fluorescence in situ hybridization 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.Sponges (phylum Porifera) are evolutionarily ancient Metazoa whose origin dates back about 600 million years to the Precambrian (26). With 7,000 formally described species and an estimated 15,000 extant species, sponges are among the most diverse marine invertebrate groups and are important components of all aquatic habitats, including freshwater environments, tropical reefs, and even the deep sea (19). Despite an enormous range of shapes, colors, and sizes, all sponges possess a relatively simple body plan which is adapted to a filter-feeding lifestyle (4). Large volumes of seawater are pumped through canals embedded in an extracellular matrix (55), termed the mesohyl, and microorganisms and small unicellular eukaryotes are taken up from the seawater with high efficiency, leaving the expelled water essentially sterile (37, 54).Numerous sponges live in permanent and close associations with microorganisms, and many of them host phylogenetically diverse populations of microbes (15,17,49). These microorganisms are located mainly extracellularly in the sponge mesohyl in high concentrations, contributing up to 40% of the sponge's biomass and...

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

“…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). Such a combination of vertical and horizontal/environmental symbiont transmission would explain the lack of correlation between microbial community similarity and sponge phylogeny seen in this and previous studies.…”

Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea

“…There is some consensus that sponge-speciesspecific microbial communities are maintained by vertical transmission of specific microbes across different generations of sponges, which is well supported by a number of studies covering sponges of different species or from different oceans (Sharp et al, 2007;Schmitt et al, 2008;Steger et al, 2008;Lee et al, 2009a). Under this scenario, one would believe that ancestral symbionts might have colonized a sponge host before sponge speciation and then coevolved with the host.…”

Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons

“…These communities, which can include bacteria, archaea and eukaryotic microorganisms, are often quite specific to sponges, with many microbial phylotypes appearing to live exclusively within sponge hosts and not in the surrounding seawater (Hentschel et al, 2002;Taylor et al, 2007b;Schmitt et al, 2008). Although our understanding of the microbial diversity in sponges is rapidly improving, much remains unknown about the activity of these microbes (Taylor et al, 2007a).…”

“…The analysis of 16S rRNA genes through clone libraries and fingerprinting approaches such as denaturing gradient gel electrophoresis (DGGE) has greatly extended our knowledge about the phylogenetic richness of sponge-associated bacteria and archaea (Webster et al, 2001(Webster et al, , 2004Hentschel et al, 2002;Taylor et al, 2004Taylor et al, , 2007bHolmes and Blanch, 2006;Longford et al, 2007;Schmitt et al, 2007Schmitt et al, , 2008Thiel et al, 2007;Mohamed et al, 2008b;Zhu et al, 2008). Researchers in other systems have taken this approach one step further, yielding insights into both richness and activity by comparing 16S rRNA gene-and 16S rRNA-derived sequences, respectively (Moeseneder et al, , 2005Winter et al, 2001;Troussellier et al, 2002;Mills et al, 2005;Gentile et al, 2006;Martinez et al, 2006;Brinkmann et al, 2008;McIlroy et al, 2008;West et al, 2008;Rodriguez-Blanco et al, 2009).…”