Host-specificity among abundant and rare taxa in the sponge microbiome

Abstract

Microbial communities have a key role in the physiology of the sponge host, and it is therefore essential to understand the stability and specificity of sponge-symbiont associations. Host-specific bacterial associations spanning large geographic distance are widely acknowledged in sponges. However, the full spectrum of specificity remains unclear. In particular, it is not known whether closely related sponges host similar or very different microbiota over wide bathymetric and geographic gradients, and whether specific associations extend to the rare members of the sponge microbiome. Using the ultra-deep Illumina sequencing technology, we conducted a comparison of sponge bacterial communities in seven closely related Hexadella species with a well-resolved host phylogeny, as well as of a distantly related sponge Mycale. These samples spanned unprecedentedly large bathymetric (15-960 m) gradients and varying European locations. In addition, this study included a bacterial community analysis of the local background seawater for both Mycale and the widespread deep-sea taxa Hexadella cf. dedritifera. We observed a striking diversity of microbes associated with the sponges, spanning 47 bacterial phyla. The data did not reveal any Hexadella microbiota co-speciation pattern, but confirmed sponge-specific and species-specific host-bacteria associations, even within extremely low abundant taxa. Oligotyping analysis also revealed differential enrichment preferences of closely related Nitrospira members in closely related sponges species. Overall, these results demonstrate highly diverse, remarkably specific and stable sponge-bacteria associations that extend to members of the rare biosphere at a very fine phylogenetic scale, over significant geographic and bathymetric gradients.

Figure 1

Map displaying sampling locations of deep-sea sites (star shape) and shallow-water ones (square shape). The boundary between shallow-water and deep sea was defined at a depth of 50 m, as previously used for corals (Cairns, 2007). Map was provided by the project Hotspot Ecosystem Research and Man's Impact on European Seas (HERMIONE).

Figure 2

Dendogram of microbial communities (UPGMA:Unweighted Pair Group Method with Arithmetic Mean) using Jaccard. The scale bar represents binary Jaccard distances.

Figure 3

Venn diagram of the shared and specific bacterial OTUs across the Hexadella, Mycale and seawater biomes. (a) Analysis of 58 sponge and seawater samples. (b) Analysis of 27 sponge and seawater samples from the same French and Irish locations.

Figure 4

Top: Stack-bar figure for Nitrospira oligotypes among the seven Hexadella species, Mycale and seawater samples. Bottom: corresponding percent abundance of Nitrospira per sample (Square root transformed).

Figure 5

Biomarker detection analysis (LEfSe) on Nitrospira oligotypes of H. dedritifera, H. cf. dedritifera, Mycale sp. and seawater communities. LEfSe identified two biomarkers (A and B) oligotypes that are differentially abundant and with a LDA larger than 5 in the classes of H. cf. dedritifera and of Mycale sp. and seawater, respectively. The mean and median relative abundance of the biomarker oligotypes are indicated with solid and dashed lines, respectively.