Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix

Abstract

Sponges occur across diverse marine biomes and host internal microbial communities that can provide critical ecological functions. While strong patterns of host specificity have been observed consistently in sponge microbiomes, the precise ecological relationships between hosts and their symbiotic microbial communities remain to be fully delineated. In the current study, we investigate the relative roles of host population genetics and biogeography in structuring the microbial communities hosted by the excavating sponge Cliona delitrix. A total of 53 samples, previously used to demarcate the population genetic structure of C. delitrix, were selected from two locations in the Caribbean Sea and from eight locations across the reefs of Florida and the Bahamas. Microbial community diversity and composition were measured using Illumina‐based high‐throughput sequencing of the 16S rRNA V4 region and related to host population structure and geographic distribution. Most operational taxonomic units (OTUs) specific to Cliona delitrix microbiomes were rare, while other OTUs were shared with congeneric hosts. Across a large regional scale (>1,000 km), geographic distance was associated with considerable variability of the sponge microbiome, suggesting a distance–decay relationship, but little impact over smaller spatial scales (<300 km) was observed. Host population structure had a moderate effect on the structure of these microbial communities, regardless of geographic distance. These results support the interplay between geographic, environmental, and host factors as forces determining the community structure of microbiomes associated with C. delitrix. Moreover, these data suggest that the mechanisms of host regulation can be observed at the population genetic scale, prior to the onset of speciation.

Host species determine symbiotic community composition in Antarctic sponges (Porifera: Demospongiae)

“…This spatial stability was also documented in the present study for dominant OTUs in D. antarctica and S. antarcticus across a geographic scale <700 km. These results are in agreement with a recent study in the Caribbean that found little variations in the sponge microbiome of Cliona delitrix over small geographic scales (<300 km), while a considerable geographic distance impact over a large regional scale (>1,000 km) was reported (Easson et al 2020). To date, published data support the combination of host identity, geography, and environment as the main forces determining the structure of sponge microbiomes (Webster et al 2010; Schmitt et al 2012; Easson et al 2020).…”

“…These results are in agreement with a recent study in the Caribbean that found little variations in the sponge microbiome of Cliona delitrix over small geographic scales (<300 km), while a considerable geographic distance impact over a large regional scale (>1,000 km) was reported (Easson et al 2020). To date, published data support the combination of host identity, geography, and environment as the main forces determining the structure of sponge microbiomes (Webster et al 2010; Schmitt et al 2012; Easson et al 2020). In Antarctica in particular, the microbial signature of sponges might be also related to a biogeographic partitioning of Southern Ocean microorganisms caused by the Polar Front, such as the deficit of Cyanobacteria in Antarctica (Wilkins et al 2013), as evidenced in the present and previous studies (Rodríguez-Marconi et al 2015; Cárdenas et al 2018; Moreno-Pino et al 2020).…”

“…Host identity seems to be the strongest driving force in determining the composition of sponge symbiont assemblages. However, associated microbial communities could be slightly influenced by biogeography and environmental factors defining a microbial signature for a particular habitat (Kennedy et al 2014; Rodríguez-Marconi et al 2015; Easson et al 2020). In future studies, the use of metagenomics (Moreno-Pino et al 2020) and metatranscriptomics will allow the recovery of functional genes and improve our understanding of the physiological roles of Antarctic sponge-associated microbiota.…”

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

“…Thus, genetic distances among these Ircinia appear to correspond to dissimilarities among their microbiome compositions, a pattern congruent with previous studies in I. campana (Griffiths et al, 2019) and C. delitrix (Easson et al, 2020). Our data further support the developing hypothesis that divergence in microbiome compositions coincides with genetic splits among host sponge lineages, and here we demonstrate that this phenomenon is also active among multiple congeneric, possibly incipient, sponge species inhabiting the same immediate geographic vicinity.…”

“…However, tests of ecological divergence among congeneric or incipient sponge species are few in number because the datatypes required to provide the necessary level of phylogenetic resolution among the host lineages, such as genome-wide SNP data, are seldom used in conjunction with metabarcoding or metagenomic censuses of microbiomes in sponges. To our knowledge only two studies have implemented such a study design by evaluating both microsatellite and 16S rRNA data, one in Ircinia campana Lamarck, 1814 (Griffiths et al, 2019) and the other in Cliona delitrix Pang, 1973(Easson et al, 2020. In both systems, a positive correlation between genetic distance and beta diversity in microbiome composition was observed, suggesting that the development of distinct microbiome compositions coincides with genetic divergence between sponge lineages prior to or contemporaneously with the onset of speciation.…”