Biogeography rather than association with cyanobacteria structures symbiotic microbial communities in the marine sponge Petrosia ficiformis

Abstract

The sponge Petrosia ficiformis is ubiquitous in the Mediterranean Sea and Eastern Atlantic Ocean, hosting a diverse assemblage of bacteria, including, in illuminated sites, cyanobacteria. Two closely related sponge color morphs have been described, one inside caves and at their entrance (white/pink), and one on the rocky cliffs (violet). The presence of the different morphs and their ubiquity in the Mediterranean (from North-West to South-East) provides an opportunity to examine which factors mostly affect the associated microbial communities in this species: (i) presence of phototrophic symbionts or (ii) biogeography. 16S rRNA gene tag pyrosequencing data of the microbial communities revealed that Chloroflexi, Gammaproteobacteria, and Acidobacteria dominated the bacterial communities of all sponges analyzed. Chlorophyll a content, TEM observations and DNA sequence data confirmed the presence of the cyanobacterium Synechococcus feldmannii in violet and pink morphs of P. ficiformis and their absence in white color morphs. Rather than cyanobacterial symbionts (i.e., color morphs) accounting for variability in microbial symbiont communities, a biogeographic trend was observed between P. ficiformis collected in Israel and Italy. Analyses of partial 18S rRNA and mitochondrial cytochrome c oxidase subunit I (COX1) gene sequences revealed consistent genetic divergence between the violet and pink-white morphotypes of P. ficiformis. Overall, data indicated that microbial symbiont communities were more similar in genetically distinct P. ficiformis from the same location, than genetically similar P. ficiformis from distant locations.

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

“…In particular, the bacterial symbionts that coexist with sponges provide their hosts with an extended multitude of metabolic functions that include nitrogen and phosphorous cycling, sulfur oxidation, carbon fixation, conversion of dissolved organic matter, and the production of secondary metabolites that serve the sponge in defense against predation (Taylor et al, 2007;Fan et al, 2012;Hentschel et al, 2012;de Goeij et al, 2013;Wilson et al, 2014;Zhang et al, 2015). The nature of bacterial community-specificity has been explored for multiple sponge species across a variety of phylogenetic, spatial, and temporal scales, revealing that adult sponge microbiomes generally are dominated by core symbionts that comprise a mix of both specialists and generalists (Webster et al, , 2010Schmitt et al, 2011;Erwin et al, 2012Erwin et al, , 2015Simister et al, 2012;Blanquer et al, 2013;Taylor et al, 2013;Easson and Thacker, 2014;Burgsdorf et al, 2015a;Thomas et al, 2016).…”

Intraspecific Variation in Microbial Symbiont Communities of the Sun Sponge, Hymeniacidonheliophila, from Intertidal and Subtidal Habitats

“…In addition, abiotic factors such as light, nutrient concentrations, and temperature can drive intraspecific variation in sponge microbial symbiont communities. Individual Petrosia ficiformis sponges growing in well-illuminated habitats harbor cyanobacterial symbionts, while those growing in shaded areas, including caves, do not (21). A study near a highly polluted estuary in Brazil noted that nutrient concentrations played a role in the structuring of the different archaeal communities of conspecific sponges (23).…”

“…In some cases, however, local environmental conditions may drive intraspecific differences in sponge microbial community structure. For example, microbial symbionts of Mycale hentscheli differed over spatial and temporal scales (20) and symbionts of Petrosia ficiformis differed by location within the Mediterranean Sea (21). Biotic factors, including the presence of diseased tissue, have been shown to affect microbial community structure in Aplysina cauliformis (22).…”

Living inside a sponge skeleton: the association of a sponge, a macroalga and a diatom

“…The association with endozoic algae could have high ecological implications in localities where photosynthetic sponges reach considerable sizes and abundances. The most frequent association among photosynthetic organisms and Porifera occurs with cyanobacteria (Burgsdorf et al 2014), which are generally transmitted to the sponge's descendants by vertical transmission (Lemloh et al 2009) but different paths can also be present (Maldonado and Riesgo 2009). Concerning the studied population of Dysidea pallescens, the passage of the algal symbionts to the offspring (vertical transmission via sponge larvae) has not been documented.…”

“…(Corallini and Gaino 2003). Many sponges are symbiotic with fungi (Gaino et al 2014) and photosynthetic organisms such as cyanobacteria (Arillo et al 1993;Burgsdorf et al 2014;Gaino et al 2006), diatoms Cerrano et al 2004a, b), zoochlorellae (Van Trigt 1918), zooxanthellae , and macroalgae (Bergquist and Tizard 1967;Davy et al 2002;Dawson 1953;Rützler 1990;Trautman and Hinde 2001;Trautman et al 2000Trautman et al , 2003Tronchin et al 2006), with possible benefits for both partners. The host may obtain fixed carbon or nitrogen from the symbiont, while algae exploit the host's catabolites, gain protection from grazers and ultraviolet radiation and increase dispersal capacity through fragmentation (Ávila et al 2007;Rützler 1990;Wilkinson and Fay 1979).…”