Phylogenetic signal in the community structure of host-specific microbiomes of tropical marine sponges.

Cole G Easson,Robert W Thacker

doi:10.3389/fmicb.2014.00532

Abstract

Sponges (Porifera) can host diverse and abundant communities of microbial symbionts that make crucial contributions to host metabolism. Although these communities are often host-specific and hypothesized to co-evolve with their hosts, correlations between host phylogeny and microbiome community structure are rarely tested. As part of the Earth Microbiome Project (EMP), we surveyed the microbiomes associated with 20 species of tropical marine sponges collected over a narrow geographic range. We tested whether (1) univariate metrics of microbiome diversity displayed significant phylogenetic signal across the host phylogeny; (2) host identity and host phylogeny were significant factors in multivariate analyses of taxonomic and phylogenetic dissimilarity; and (3) different minimum read thresholds impacted these results. We observed significant differences in univariate metrics of diversity among host species for all read thresholds, with strong phylogenetic signal in the inverse Simpson's index of diversity (D). We observed a surprisingly wide range of variability in community dissimilarity within host species (4–73%); this variability was not related to microbial abundance within a host species. Taxonomic and phylogenetic dissimilarity were significantly impacted by host identity and host phylogeny when these factors were considered individually; when tested together, the effect of host phylogeny was reduced, but remained significant. In our dataset, this outcome is largely due to closely related host sponges harboring distinct microbial taxa. Host identity maintained a strong statistical signal at all minimum read thresholds. Although the identity of specific microbial taxa varied substantially among host sponges, closely related hosts tended to harbor microbial communities with similar patterns of relative abundance. We hypothesize that microbiomes with low D might be structured by regulation of the microbial community by the host or by the presence of competitively dominant symbionts that are themselves under selection for host specificity.

Highlights

Marine sponges are globally distributed and perform critical ecological functions in benthic ecosystems (Rützler, 2012; Van Soest et al, 2012)
We found significant phylogenetic signal in D (K = 0.591, P = 0.003, Figure 3), with three representatives of order Verongida (A. cauliformis, A. crassa, and A. fulva), along with E. formosus, all displaying relatively high values of D, while five representatives of order Poecilosclerida (I. birotulata, L. colombiensis, Mycale spp., and T. ignis) all displayed very low values of D
Previous researchers have used a wide variety of techniques to document that sponge-associated microbial communities are largely host specific (e.g., Erwin et al, 2012a; Reveillaud et al, 2014), but host phylogenetic relatedness has only rarely been included as a specific factor influencing microbiome community structure (Schöttner et al, 2013)

Summary

Introduction

Marine sponges are globally distributed and perform critical ecological functions in benthic ecosystems (Rützler, 2012; Van Soest et al, 2012). Sponges are active participants in the carbon, nitrogen, and sulfur cycles, performing aerobic and anaerobic processes that benefit the broader community (Taylor et al, 2007; Schläppy et al, 2010; Maldonado et al, 2012; Schöttner et al, 2013). Sponges play a critical role in pelagic–benthic coupling, transferring pelagic carbon and nitrogen to benthic food webs (Lesser, 2006; De Goeij et al, 2013). The diverse communities of microbial symbionts hosted by marine sponges are hypothesized to be the primary drivers of these essential nutrient cycles (Maldonado et al, 2012; Thacker and Freeman, 2012). The diversity of sponge-associated microbiomes is unmatched by other invertebrate hosts, such that their complexity is frequently compared to that of mammalian gut microbiomes (Webster et al, 2010; Reveillaud et al, 2014)

Methods

Results

Conclusion