Diversity in the globally intertwined giant barrel sponge species complex

This thesis describes the genetic and prokaryotic diversity of giant barrel sponges. Although it was originally believed that the giant barrel sponges in the AtlanticOcean and the Indo-Pacific Ocean were two different species, our analyses showed thatthere are several species in both ocean basins. Even more remarkable, is that each species is most closely related to a species in the other ocean basin. According to our analysis, there are threegiant barrel sponge species in the Atlantic Ocean, and, at least, six in the Indo-Pacific Ocean. Sponges house a large and diverse community of microorganisms. It is generally believed thatthese microorganisms play a central role in the physiological processes in the host. It appears that the region in which a giant barrel sponge occursmainly determines the composition of their microbial community. However, if you lookat a smaller scale within a region, for example within one reef or around an island suchas Curaçao, it appears that not only is the geographical location important, but the hostspecies to which an individual belongs also plays an important role.Environmental Biolog

Metabolic variation in Caribbean giant barrel sponges: influence of age and sea-depth

NWO# 16.161.301Environmental Biolog

Influence of the geographical location on the metabolic production of giant barrel sponges (Xestospongia spp.) revealed by metabolomics tools

Animal science

Lock, stock and two different barrels: comparing the genetic composition of morphotypes of the Indo-Pacific sponge Xestospongia testudinaria

The giant barrel sponge Xestospongiatestudinaria is an ecologically important species that is widely distributed across the Indo-Pacific. Little is known, however, about the precise biogeographic distribution and the amount of morphological and genetic variation in this species. Here we provide the first detailed, fine-scaled (<200 km(2)) study of the morphological and genetic composition of X. testudinaria around Lembeh Island, Indonesia. Two mitochondrial (CO1 and ATP6 genes) and one nuclear (ATP synthase β intron) DNA markers were used to assess genetic variation. We identified four distinct morphotypes of X. testudinaria around Lembeh Island. These morphotypes were genetically differentiated with both mitochondrial and nuclear markers. Our results indicate that giant barrel sponges around Lembeh Island, which were all morphologically identified as X. testudinaria, consist of at least two different lineages that appear to be reproductively isolated. The first lineage is represented by individuals with a digitate surface area, CO1 haplotype C5, and is most abundant around the harbor area of Bitung city. The second lineage is represented by individuals with a predominantly smooth surface area, CO1 haplotype C1 and can be found all around Lembeh Island, though to a lesser extent around the harbor of Bitung city. Our findings of two additional unique genetic lineages suggests the presence of an even broader species complex possibly containing more than two reproductively isolated species. The existence of X. testudinaria as a species complex is a surprising result given the size, abundance and conspicuousness of the sponge.The project was supported by the Percy Sladen Memorial Fund of the Linnean Society of London and the Treub-Maatschappij Fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank the Research Centre for Oceanography of the Indonesian Institute of Sciences (RCO-LIPI) for allowing us to use their research facilities and the University of Sam Ratulangi (UNSRAT) for logistic support. We thank Lin Dong, Peter Kuperus and Betsie Voetdijk for advice and help with molecular lab techniques. Hans Breeuwer provided valuable comments on the original manuscript.publishe

The sponge microbiome within the greater coral reef microbial metacommunity

Much recent marine microbial research has focused on sponges, but very little is known about how the sponge microbiome fits in the greater coral reef microbial metacommunity. Here, we present an extensive survey of the prokaryote communities of a wide range of biotopes from Indo-Pacific coral reef environments. We find a large variation in operational taxonomic unit (OTU) richness, with algae, chitons, stony corals and sea cucumbers housing the most diverse prokaryote communities. These biotopes share a higher percentage and number of OTUs with sediment and are particularly enriched in members of the phylum Planctomycetes. Despite having lower OTU richness, sponges share the greatest percentage (>90%) of OTUs with >100 sequences with the environment (sediment and/or seawater) although there is considerable variation among sponge species. Our results, furthermore, highlight that prokaryote microorganisms are shared among multiple coral reef biotopes, and that, although compositionally distinct, the sponge prokaryote community does not appear to be as sponge-specific as previously thought.publishe

Resilience to Disturbance Despite Limited Dispersal and Self-Recruitment in Tropical Barrel Sponges: Implications for Conservation and Management

While estimates of connectivity are important for effective management, few such estimates are available for reef invertebrates other than for corals. Barrel sponges are one of the largest and most conspicuous members of the coral reef fauna across the Indo-Pacific and given their large size, longevity and ability to process large volumes of water, they have a major role in reef functioning. Here we used a panel of microsatellite markers to characterise the genetic structure of two barrel sponge species, Xestospongia testudinaria and a currently undescribed Xestospongia species. We sampled across seven populations in the Wakatobi Marine National Park, SE Sulawesi (Indonesia) spanning a spatial scale of approximately 2 to 70 km, and present the first estimates of demographic connectivity for coral reef sponges. Genetic analyses showed high levels of genetic differentiation between all populations for both species, but contrasting patterns of genetic structuring for the two species. Autocorrelation analyses showed the likely dispersal distances of both species to be in the order of 60 and 140 m for Xestopongia sp. and Xestospongia testudinaria, respectively, which was supported by assignment tests that showed high levels of self-recruitment (>80%). We also found consistently high inbreeding coefficients across all populations for both species. Our study highlights the potential susceptibility of barrel sponges to environmental perturbations because they are generally long-lived, slow growing, have small population sizes and are likely to be reliant on self-recruitment. Surprisingly, despite these features we actually found the highest abundance of both barrel sponge species (although they were generally smaller) at a site that has been severely impacted by humans over the last fifty years. This suggests that barrel sponges exhibit environmental adaptation to declining environmental quality and has important implications for the management and conservation of these important reef species. © 2014 Bell et al

Compositional analysis of bacterial communities in seawater, sediment, and sponges in the Misool coral reef system, Indonesia

Sponge species have been deemed high microbial abundance (HMA) or low microbial abundance (LMA) based on the composition and abundance of their microbial symbionts. In the present study, we evaluated the richness and composition of bacterial communities associated with one HMA sponge (Xestospongia testudinaria; Demospongiae: Haplosclerida: Petrosiidae), one LMA sponge (Stylissa carteri; Demospongiae: Scopalinida - Scopalinidae), and one sponge with a hitherto unknown microbial community (Aaptos suberitoides; Demospongiae: Suberitida: Suberitidae) inhabiting the Misool coral reef system in the West Papua province of Indonesia. The bacterial communities of these sponge species were also compared with seawater and sediment bacterial communities from the same coastal coral reef habitat. Using a 16S rRNA gene barcoded pyrosequencing approach, we showed that the most abundant phylum overall was Proteobacteria. The biotope (sponge species, sediment or seawater) explained almost 84% of the variation in bacterial composition with highly significant differences in composition among biotopes and a clear separation between bacterial communities from seawater and S. carteri; X. testudinaria and A. suberitoides and sediment. The Chloroflexi classes SAR202 and Anaerolineae were most abundant in A. suberitoides and X. testudinaria and both of these species shared several OTUs that were largely absent in the remaining biotopes. This suggests that A. suberitoides is a HMA sponge. Although similar, the bacterial communities of S. carteri and seawater were compositionally distinct. These results confirm compositional differences between sponge and non-sponge biotopes and between HMA and LMA sponges.publishe

Viral ecogenomics across the Porifera

BackgroundViruses directly affect the most important biological processes in the ocean via their regulation of prokaryotic and eukaryotic populations. Marine sponges form stable symbiotic partnerships with a wide diversity of microorganisms and this high symbiont complexity makes them an ideal model for studying viral ecology. Here, we used morphological and molecular approaches to illuminate the diversity and function of viruses inhabiting nine sponge species from the Great Barrier Reef and seven from the Red Sea.ResultsViromic sequencing revealed host-specific and site-specific patterns in the viral assemblages, with all sponge species dominated by the bacteriophage order Caudovirales but also containing variable representation from the nucleocytoplasmic large DNA virus families Mimiviridae, Marseilleviridae, Phycodnaviridae, Ascoviridae, Iridoviridae, Asfarviridae and Poxviridae. Whilst core viral functions related to replication, infection and structure were largely consistent across the sponge viromes, functional profiles varied significantly between species and sites largely due to differential representation of putative auxiliary metabolic genes (AMGs) and accessory genes, including those associated with herbicide resistance, heavy metal resistance and nylon degradation. Furthermore, putative AMGs varied with the composition and abundance of the sponge-associated microbiome. For instance, genes associated with antimicrobial activity were enriched in low microbial abundance sponges, genes associated with nitrogen metabolism were enriched in high microbial abundance sponges and genes related to cellulose biosynthesis were enriched in species that host photosynthetic symbionts.ConclusionsOur results highlight the diverse functional roles that viruses can play in marine sponges and are consistent with our current understanding of sponge ecology. Differential representation of putative viral AMGs and accessory genes across sponge species illustrate the diverse suite of beneficial roles viruses can play in the functional ecology of these complex reef holobionts