Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association

Abstract

Marine sponges host diverse communities of microbial symbionts that expand the metabolic capabilities of their host, but the abundance and structure of these communities is highly variable across sponge species. Specificity in these interactions may fuel host niche partitioning on crowded coral reefs by allowing individual sponge species to exploit unique sources of carbon and nitrogen, but this hypothesis is yet to be tested. Given the presence of high sponge biomass and the coexistence of diverse sponge species, the Caribbean Sea provides a unique system in which to investigate this hypothesis. To test for ecological divergence among sympatric Caribbean sponges and investigate whether these trends are mediated by microbial symbionts, we measured stable isotope (δ13C and δ15N) ratios and characterized the microbial community structure of sponge species at sites within four regions spanning a 1700 km latitudinal gradient. There was a low (median of 8.2 %) overlap in the isotopic niches of sympatric species; in addition, host identity accounted for over 75% of the dissimilarity in both δ13C and δ15N values and microbiome community structure among individual samples within a site. There was also a strong phylogenetic signal in both δ15N values and microbial community diversity across host phylogeny, as well as a correlation between microbial community structure and variation in δ13C and δ15N values across samples. Together, this evidence supports a hypothesis of strong evolutionary selection for ecological divergence across sponge lineages and suggests that this divergence is at least partially mediated by associations with microbial symbionts.

Antibacterial scalarane fromDoriprismatica stellatanudibranchs (Gastropoda, Nudibranchia), egg ribbons, and their dietary spongeSpongiacf.agaricina(Demospongiae, Dictyoceratida)

“…Sponges are known to host complex symbiont communities, with up to 30–60% as microbial biomass [ 13 , 77 ]. These highly species-specific communities are most probably vertically transmitted [ 78 ] and were shown to share and cover various core functions of sponge metabolism by functionally equivalent symbionts, analogous enzymes, or biosynthetic pathways [ 16 , 79 – 80 ]. Another Spongia species, S. officinalis , was shown to harbour bacteria with terpenoid cyclases/protein prenyltransferases responsible for a wide chemodiversity of terpenoid natural products [ 14 , 81 ].…”

“…Sponges (Porifera), for example, represent one of the main sources of marine bioactive natural products, due to their impressive chemical armoury [4]. These specialized metabolites can be produced either by the sponge itself or by associated microbial symbionts [9][10][11][12][13][14][15][16]. Their production is assumed to be useful against numerous environmental stress factors, such as predation, pathogens, overgrowth by fouling organisms, or competition for space [4,10,15,17].…”

Microbiomes and host genetics provide evidence for ecological diversification among Caribbean members of the sponge genusIrciniaNardo, 1833

“…Isotopic data represented by sympatric, though phylogenetically distant host taxa support the hypothesis that this pattern of beta diversity among the microbiome compositions translates to divergent niche inhabitation among sponge species and potentially facilitates their coexistence on the same reef (C. J. Freeman et al, 2020).…”

The relationship between microbiomes and selective regimes in the sponge genusIrcinia

“…The microbiomes can also be divergent among host species [21] which, combined with the metabolic diversity of the microbes, supports the hypothesis that the microbiome acts as a mechanism for ecological diversification within sponges. This evolutionary model has received some of its strongest support in recent work investigating the bulk isotopic enrichment levels of sympatric sponge species [32], where both microbiome compositions and isotopic enrichment values were divergent among host taxa within geographic sites, identifying the microbiomes as being not only a mechanism for accessing novel resources but also a means for alleviating resource competition. Granted that microbiomes hold the potential to unlock access to new resources, they might also enable ecological diversification among incipient sponge species.…”

“…To perform this study, we first tested whether active control of microbiomes by the hosts is evidenced throughout Ircinia by characterizing beta diversity among the microbial consortia of the hosts and surrounding seawater using 16S rRNA metabarcoding. Second, we tested whether this control translates to dissimilar microbiome compositions among Ircinia host species, several of which we delimited using 2bRAD (RADseq) data, as the possession of unique microbiomes is congruent with prior evidence of ecological diversification within sponges [32].…”