Host rules: spatial stability of bacterial communities associated with marine sponges (Irciniaspp.) in the Western Mediterranean Sea

Abstract

Dispersal limitation and environmental selection are the main processes shaping free-living microbial communities, but host-related factors may also play a major role in structuring symbiotic communities. Here, we aimed to determine the effects of isolation-by-distance and host species on the spatial structure of sponge-associated bacterial communities using as a model the abundant demosponge genus Ircinia. We targeted three co-occurring Ircinia species and used terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA gene sequences to explore the differentiation of their bacterial communities across a scale of hundreds of kilometres in the Western Mediterranean Sea. Multivariate analysis and nonmetric multidimensional scaling plots of T-RFLP profiles showed that bacterial communities in Ircinia sponges were structured by host species and remained stable across sampling locations, despite geographic distances (80-800 km) and diverse local conditions. While significant differences among some locations were observed in Ircinia variabilis-derived communities, no correlation between geographic distance and community similarity was consistently detected for symbiotic bacteria in any host sponge species. Our results indicate that bacterial communities are mostly shaped by host species-specific factors and suggest that evolutionary processes acting on long-term symbiotic relationships have favored spatial stability of sponge-associated bacterial communities.

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

“…For example, the second most abundant OTU that differentiated intertidal and subtidal H. heliophila was classified as the alphaproteobacterium Thalassobaculum litoreum, which has been shown to possess nitrate reductase enzymes (55). While nitrate reductase activity has yet to be demonstrated in this sponge holobiont, cytoplasmic and periplasmic nitrate reductase genes (narG and napA) have been detected in multiple sponge microbiomes (56) and other nitrogen cycling pathways have been reported in the H. heliophila microbiome (amoA genes from ammonia-oxidizing archaea) (15). Further research is necessary to demonstrate the functional implications of the observed microbial community shifts, as different microbial communities can be functionally equivalent (56) and a rich biodiversity of rare symbionts exists within H. heliophila.…”

“…Rare microbial taxa, which can represent a large proportion (Ͼ90%) of the diversity of microbes found in marine sponges, exhibit similar levels of host species specificity, as reported for more dominant symbiont taxa (13). Next-generation sequencing has provided insight into the extraordinary diversity of these lowabundance microbial taxa, often referred to as the "rare biosphere" (14), but further research is necessary to understand how they are shaped by their environment.Recent studies report spatially and temporally stable microbial communities in multiple sponge species collected across geographic distances of hundreds of kilometers (8,15,16), seasonal and annual time scales (17,18), and depths of 10 to 100 m (19). In some cases, however, local environmental conditions may drive intraspecific differences in sponge microbial community structure.…”

“…Recent studies report spatially and temporally stable microbial communities in multiple sponge species collected across geographic distances of hundreds of kilometers (8,15,16), seasonal and annual time scales (17,18), and depths of 10 to 100 m (19). In some cases, however, local environmental conditions may drive intraspecific differences in sponge microbial community structure.…”

Gene Expression Dynamics Accompanying the Sponge Thermal Stress Response

“…In one example, 454 pyrosequencing of the 16S rRNA metagenome revealed that exposure to 31°C had no effect on the bacterial biosphere within the Great Barrier sponge Rhopaloeides odorabile [14]. Likewise, in the Mediterranean Sea sponge Ircinia spp ., neither thermal stress combined with food shortage nor large fluctuations in temperature and irradiance disrupted the stability of the sponge-bacteria partnership [15,16]. The importance of cell-cell signaling genes in the maintenance or breakdown of the sponge-bacteria interaction during thermal stress events has been explored to some extent [17].…”

Emerging Sponge Models of Animal-Microbe Symbioses

“…Host species appears to be the main factor driving microbial diversity (Erwin et al, 2012; Easson and Thacker, 2014), although environmental factors (e.g., intertidal vs. subtidal habitat, Weigel and Erwin, 2016; depth, Steinert et al, 2016; location, Pita et al, 2013b) can also cause intraspecific variability. Also, differences in symbiont density within the mesohyl (i.e., high microbial abundance HMA sponges vs. low microbial abundance LMA sponges; Gloeckner et al, 2014) have an impact on microbial community composition as well as on the host pumping rate and other metabolic parameters (Weisz et al, 2008; Ribes et al, 2012).…”