Severe hurricanes increase recruitment and gene flow in the clonal sponge Aplysina cauliformis.

Upright branching sponges, such as Aplysina cauliformis, provide critical three-dimensional habitat for other organisms and assist in stabilizing coral reef substrata, but are highly susceptible to breakage during storms. Breakage can increase sponge fragmentation, contributing to population clonality and inbreeding. Conversely, storms could provide opportunities for new genotypes to enter populations via larval recruitment, resulting in greater genetic diversity in locations with frequent storms. The unprecedented occurrence of two Category 5 hurricanes in close succession during 2017 in the U.S. Virgin Islands (USVI) provided a unique opportunity to evaluate whether recolonization of newly available substrata on coral reefs was due to local (e.g. re-growth of remnants, fragmentation, larval recruitment) or remote (e.g. larval transport and immigration) sponge genotypes. We sampled A. cauliformis adults and juveniles from four reefs around St. Thomas and two in St. Croix (USVI). Using a 2bRAD protocol, all samples were genotyped for single-nucleotide polymorphisms (SNPs). Results showed that these major storm events favoured sponge larval recruitment but did not increase the genetic diversity of A. cauliformis populations. Recolonization of substratum post-storms via clonality was lower (15%) than expected and instead was mainly due to sexual reproduction (85%) via local larval recruitment. Storms did enhance gene flow among and within reef sites located south of St. Thomas and north of St. Croix. Therefore, populations of clonal marine species with low pelagic dispersion, such as A. cauliformis, may benefit from increased frequency and magnitude of hurricanes for the maintenance of genetic diversity and to combat inbreeding, enhancing the resilience of Caribbean sponge communities to extreme storm events.

Microbial dysbiosis reflects disease resistance in diverse coral species.

Disease outbreaks have caused significant declines of keystone coral species. While forecasting disease outbreaks based on environmental factors has progressed, we still lack a comparative understanding of susceptibility among coral species that would help predict disease impacts on coral communities. The present study compared the phenotypic and microbial responses of seven Caribbean coral species with diverse life-history strategies after exposure to white plague disease. Disease incidence and lesion progression rates were evaluated over a seven-day exposure. Coral microbiomes were sampled after lesion appearance or at the end of the experiment if no disease signs appeared. A spectrum of disease susceptibility was observed among the coral species that corresponded to microbial dysbiosis. This dysbiosis promotes greater disease susceptiblity in coral perhaps through different tolerant thresholds for change in the microbiome. The different disease susceptibility can affect coral's ecological function and ultimately shape reef ecosystems.

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

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.

Bleaching events regulate shifts from corals to excavating sponges in algae-dominated reefs.

Changes in coral-sponge interactions can alter reef accretion/erosion balance and are important to predict trends on current algal-dominated Caribbean reefs. Although sponge abundance is increasing on some coral reefs, we lack information on how shifts from corals to bioeroding sponges occur, and how environmental factors such as anomalous seawater temperatures and consequent coral bleaching and mortality influence these shifts. A state transition model (Markov chain) was developed to evaluate the response of coral-excavating sponges (Cliona delitrix Pang 1973) after coral bleaching events. To understand possible outcomes of the sponge-coral interaction and build the descriptive model, sponge-corals were monitored in San Andres Island, Colombia (2004-2011) and Fort Lauderdale, Florida (2012-2013). To run the model and determine possible shifts from corals to excavating sponges, 217 coral colonies were monitored over 10 years (2000-2010) in Fort Lauderdale, Florida, and validated with data from 2011 to 2015. To compare and test its scalability, the model was also run with 271 coral colonies monitored in St. Croix, US Virgin Islands over 7 years (2004-2011), and validated with data from 2012 to 2015. Projections and sensitivity analyses confirmed coral recruitment to be key for coral persistence. Excavating sponge abundance increased in both Fort Lauderdale and St. Croix reefs after a regional mass bleaching event in 2005. The increase was more drastic in St. Croix than in Fort Lauderdale, where 25% of the healthy corals that deteriorated were overtaken by excavating sponges. Projections over 100 years suggested successive events of coral bleaching could shift algae-coral dominated reefs into algae-sponge dominated. The success of excavating sponges depended on the intensity of coral bleaching and consequent coral mortality. Thus, the proportion of C. delitrix excavating sponges is a sensitive indicator for the intensity and frequency of recent disturbance on Caribbean coral reefs.

Diversity, structure and convergent evolution of the global sponge microbiome.

Sponges (phylum Porifera) are early-diverging metazoa renowned for establishing complex microbial symbioses. Here we present a global Porifera microbiome survey, set out to establish the ecological and evolutionary drivers of these host-microbe interactions. We show that sponges are a reservoir of exceptional microbial diversity and major contributors to the total microbial diversity of the world's oceans. Little commonality in species composition or structure is evident across the phylum, although symbiont communities are characterized by specialists and generalists rather than opportunists. Core sponge microbiomes are stable and characterized by generalist symbionts exhibiting amensal and/or commensal interactions. Symbionts that are phylogenetically unique to sponges do not disproportionally contribute to the core microbiome, and host phylogeny impacts complexity rather than composition of the symbiont community. Our findings support a model of independent assembly and evolution in symbiont communities across the entire host phylum, with convergent forces resulting in analogous community organization and interactions.

Population structure and dispersal of the coral-excavating sponge Cliona delitrix.

Some excavating sponges of the genus Cliona compete with live reef corals, often killing and bioeroding entire colonies. Important aspects affecting distribution of these species, such as dispersal capability and population structure, remain largely unknown. Thus, the aim of this study was to determine levels of genetic connectivity and dispersal of Cliona delitrix across the Greater Caribbean (Caribbean Sea, Bahamas and Florida), to understand current patterns and possible future trends in their distribution and effects on coral reefs. Using ten species-specific microsatellite markers, we found high levels of genetic differentiation between six genetically distinct populations: one in the Atlantic (Florida-Bahamas), one specific to Florida and four in the South Caribbean Sea. In Florida, two independent breeding populations are likely separated by depth. Gene flow and ecological dispersal occur among other populations in the Florida reef tract, and between some Florida locations and the Bahamas. Similarly, gene flow occurs between populations in the South Caribbean Sea, but appears restricted between the Caribbean Sea and the Atlantic (Florida-Bahamas). Dispersal of C. delitrix was farther than expected for a marine sponge and favoured in areas where currents are strong enough to transport sponge eggs or larvae over longer distances. Our results support the influence of ocean current patterns on genetic connectivity, and constitute a baseline to monitor future C. delitrix trends under climate change.

Reconstruction of family-level phylogenetic relationships within Demospongiae (Porifera) using nuclear encoded housekeeping genes.

BACKGROUND: Demosponges are challenging for phylogenetic systematics because of their plastic and relatively simple morphologies and many deep divergences between major clades. To improve understanding of the phylogenetic relationships within Demospongiae, we sequenced and analyzed seven nuclear housekeeping genes involved in a variety of cellular functions from a diverse group of sponges. METHODOLOGY/PRINCIPAL FINDINGS: We generated data from each of the four sponge classes (i.e., Calcarea, Demospongiae, Hexactinellida, and Homoscleromorpha), but focused on family-level relationships within demosponges. With data for 21 newly sampled families, our Maximum Likelihood and Bayesian-based approaches recovered previously phylogenetically defined taxa: Keratosa(p), Myxospongiae(p), Spongillida(p), Haploscleromorpha(p) (the marine haplosclerids) and Democlavia(p). We found conflicting results concerning the relationships of Keratosa(p) and Myxospongiae(p) to the remaining demosponges, but our results strongly supported a clade of Haploscleromorpha(p)+Spongillida(p)+Democlavia(p). In contrast to hypotheses based on mitochondrial genome and ribosomal data, nuclear housekeeping gene data suggested that freshwater sponges (Spongillida(p)) are sister to Haploscleromorpha(p) rather than part of Democlavia(p). Within Keratosa(p), we found equivocal results as to the monophyly of Dictyoceratida. Within Myxospongiae(p), Chondrosida and Verongida were monophyletic. A well-supported clade within Democlavia(p), Tetractinellida(p), composed of all sampled members of Astrophorina and Spirophorina (including the only lithistid in our analysis), was consistently revealed as the sister group to all other members of Democlavia(p). Within Tetractinellida(p), we did not recover monophyletic Astrophorina or Spirophorina. Our results also reaffirmed the monophyly of order Poecilosclerida (excluding Desmacellidae and Raspailiidae), and polyphyly of Hadromerida and Halichondrida. CONCLUSIONS/SIGNIFICANCE: These results, using an independent nuclear gene set, confirmed many hypotheses based on ribosomal and/or mitochondrial genes, and they also identified clades with low statistical support or clades that conflicted with traditional morphological classification. Our results will serve as a basis for future exploration of these outstanding questions using more taxon- and gene-rich datasets.

Clionapyrrolidine A--a metabolite from the encrusting and excavating sponge Cliona tenuis that kills coral tissue upon contact.

The Caribbean encrusting and excavating sponge Cliona tenuis successfully competes for space with reef corals by undermining, killing, and displacing live coral tissue at rates of up to 20 cm per year. The crude extract from this sponge, along with the more polar partitions, kills coral tissue and lowers the photosynthetic potential of coral zooxanthellae. We used a bioassay-guided fractionation of the extract to identify the compound(s) responsible. The crude extract, the aqueous partition, and compound 1, herein named clionapyrrolidine A [(-)-(5S)-2-imino-1-methylpyrrolidine-5-carboxylic acid], when incorporated into gels at close to natural volumetric concentrations, killed coral tissue when brought into forced contact with live coral for periods of 1-4 days. This is the first report of a pure chemical produced by a sponge that kills coral tissue upon direct contact. The results are consistent with the localized coral death that occurs when C. tenuis-colonized coral fragments are thrown forcibly against live coral during storms. However, healed C. tenuis fragments placed directly onto live coral were killed readily by coral defenses, and fragments placed in close proximity to coral did not have any effect on the adjacent coral tissue. Solutions of clionapyrrolidine A in sea water were only slightly toxic against live coral. Hence, the coral death naturally brought about by C. tenuis when undermining live coral does not occur through external release of allelochemicals; below-polyp mechanisms must be explored further. N-acetylhomoagmatine (2), originally isolated from Cliona celata from the Northeastern Atlantic, was also assayed for comparison purposes because of its structural similarity to siphonodictidine, a toxic compound produced by a coral excavating sponge of the genus Aka. The lack of activity of N-acetylhomoagmatine at close to natural concentrations seems to indicate that the guanidine moiety, which is also present in siphonodictidine, is not a sufficiently strong structural motif for activity against corals.