Variability in Host Specificity and Functional Potential of Antarctic Sponge-Associated Bacterial Communities

Sponge-associated microorganisms are essential for sponge survival. They play an important role in recycling nutrients and, therefore, in the maintenance of the ecosystem. These microorganisms are diverse, species-specific, and different from those in the surrounding seawater. Bacterial sponge symbionts have been extensively studied in the tropics; however, little is known about these microorganisms in sponges from high-latitude environments. Sponges can cover up to 80% of the benthos in Antarctica and are crucial architects for the marine food web. In this study, we present analyses of the bacterial symbionts of three sponges: Haliclona (Rhizoniera) sp., Hymeniacidon torquata, and Isodictya kerguelenensis from the Western Antarctic Peninsula (WAP) with the aim to determine variations on the specificity of the bacteria–sponge interactions and potential signatures on their predicted functional profiles. We use high-throughput 16S rRNA gene sequencing of 30 sponge individuals inhabiting South Bay (Palmer Archipelago, WAP) to describe their microbiome taxonomy and diversity and predict potential functional profiles based on this marker gene. Our work shows similar bacterial community composition profiles among the same sponge species, although the symbiotic relationship is not equally conserved among the three Antarctic sponges. The number of species-specific core operational taxonomic units (OTUs) of these Antarctic sponges was low, with important differences between the total abundance accounted for these OTUs. Only eight OTUs were shared between the three sponge species. Analyses of the functional potential revealed that despite the high host–symbiont specificity, the inferred functions are conserved among these microbiomes, although with differences in the abundance of specific functions. H. torquata showed the highest level of intra-specificity and a higher potential of pathways related to energy metabolism, metabolisms of terpenoids and polyketides, and biosynthesis of other secondary metabolites. Overall, this work shows variations in the specificity of the sponge-associated bacterial communities, differences in how hosts and symbionts establish their relations, and in their potential functional capabilities.

Bioactivity Screening of Antarctic Sponges Reveals Anticancer Activity and Potential Cell Death via Ferroptosis by Mycalols

Sponges are known to produce a series of compounds with bioactivities useful for human health. This study was conducted on four sponges collected in the framework of the XXXIV Italian National Antarctic Research Program (PNRA) in November-December 2018, i.e., Mycale (Oxymycale) acerata, Haliclona (Rhizoniera) dancoi, Hemimycale topsenti, and Hemigellius pilosus. Sponge extracts were fractioned and tested against hepatocellular carcinoma (HepG2), lung carcinoma (A549), and melanoma cells (A2058), in order to screen for antiproliferative or cytotoxic activity. Two different chemical classes of compounds, belonging to mycalols and suberitenones, were identified in the active fractions. Mycalols were the most active compounds, and their mechanism of action was also investigated at the gene and protein levels in HepG2 cells. Of the differentially expressed genes, ULK1 and GALNT5 were the most down-regulated genes, while MAPK8 was one of the most up-regulated genes. These genes were previously associated with ferroptosis, a programmed cell death triggered by iron-dependent lipid peroxidation, confirmed at the protein level by the down-regulation of GPX4, a key regulator of ferroptosis, and the up-regulation of NCOA4, involved in iron homeostasis. These data suggest, for the first time, that mycalols act by triggering ferroptosis in HepG2 cells.

A Metataxonomic Approach Reveals Diversified Bacterial Communities in Antarctic Sponges

Marine sponges commonly host a repertoire of bacterial-associated organisms, which significantly contribute to their health and survival by producing several anti-predatory molecules. Many of these compounds are produced by sponge-associated bacteria and represent an incredible source of novel bioactive metabolites with biotechnological relevance. Although most investigations are focused on tropical and temperate species, to date, few studies have described the composition of microbiota hosted by Antarctic sponges and the secondary metabolites that they produce. The investigation was conducted on four sponges collected from two different sites in the framework of the XXXIV Italian National Antarctic Research Program (PNRA) in November–December 2018. Collected species were characterized as Mycale (Oxymycale) acerata, Haliclona (Rhizoniera) dancoi, Hemigellius pilosus and Microxina sarai by morphological analysis of spicules and amplification of four molecular markers. Metataxonomic analysis of these four Antarctic sponges revealed a considerable abundance of Amplicon Sequence Variants (ASVs) belonging to the phyla Proteobacteria, Bacteroidetes, Actinobacteria and Verrucomicrobia. In particular, M. (Oxymycale) acerata, displayed several genera of great interest, such as Endozoicomonas, Rubritalea, Ulvibacter, Fulvivirga and Colwellia. On the other hand, the sponges H. pilosus and H. (Rhizoniera) dancoi hosted bacteria belonging to the genera Pseudhongella, Roseobacter and Bdellovibrio, whereas M. sarai was the sole species showing some strains affiliated to the genus Polaribacter. Considering that most of the bacteria identified in the present study are known to produce valuable secondary metabolites, the four Antarctic sponges could be proposed as potential tools for the discovery of novel pharmacologically active compounds.

Recycling resources: silica of diatom frustules as a source for spicule building in Antarctic siliceous demosponges

Dissolved silicon (DSi) is biologically processed to produce siliceous skeletons by a variety of organisms including radiolarians, silicoflagellates, choanoflagellates, plants, diatoms and some animals. In the photic ocean, diatoms are dominant consumers over competing other silicifiers. In Antarctica, where DSi is not particularly limiting, diatoms and sponges coexist in high abundances. Interestingly, diatom ingestion by sponges is a regular feeding strategy there. Although it was known that the diatom organic nutrients are readily metabolized by the sponges, what happened to the inorganic diatom silica skeleton remained unexplored. Here, we have conducted a multi-analytical approach to investigate the processing of diatom silica and whether it is reconverted into sponge silica. We have documented widespread diatom consumption by several demosponges, identifying storage vesicles for the diatom-derived silica by electron microscopy and microanalysis. Diatom-consuming sponges showed upregulation of silicatein and silicase genes, which in addition to the δ 30Si values of their silica, supports that the sponges are converting the ingested diatom silica into sponge silica without much further Si fractionation. Our multidisciplinary approach suggests that the reutilization of diatom silica by sponges is a common feature among Antarctic sponges, which should be further investigated in other latitudes and in other silicifiers.

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

The microbiota of four Antarctic sponges, Dendrilla antarctica, Sphaerotylus antarcticus, Mycale acerata, and Hemigellius pilosus, collected at two South Shetland Islands and at two locations in the Antarctic Peninsula separated by ca. 670 km, were analyzed together with surrounding seawater. We used high throughput sequencing of the V4 region of the 16S rRNA gene common to Bacteria and Archaea to investigate the microbial diversity and community composition. Our study reveals that sponge-associated prokaryote communities are consistently detected within a particular sponge species regardless of the collection site. Their community structure and composition are typical of low microbial abundance (LMA) sponges. We conclude that prokaryote communities from Antarctic sponges are less diverse and differ in their composition compared to those in the water column. Microbiome analysis indicates that Antarctic sponges harbor a strict core consisting of seven OTUs, and a small variable community comprising several tens of OTUs. Two abundant prokaryotes from the variable microbiota that are affiliated to the archaeal and bacterial phyla Thaumarchaeota and Nitrospirae may be involved in the sponge nitrification process and might be relevant components of the nitrogen cycling in Antarctica. The likely generalist nature of dominant microbes and the host-specific structure of symbiont communities suggest that these Antarctic sponges represent different ecological niches for particular microbial enrichments.

Sponges from Doumer Island, Antarctic Peninsula, with description of new species of Clathria (Axosuberites) Topsent, 1893 and Hymeniacidon Bowerbank, 1858, and a re-description of H. torquata Topsent, 1916

Antarctic sponges were mainly studied from trawling or dredging (shallow and deep water) during pioneering oceanographic expeditions carried out since the late 19th century. More recently, sponge collections by SCUBA diving have allowed the detection of species in more cryptic habitats such as rocky walls. In this study, we analyzed Antarctic sponges collected by SCUBA (in 2016 to 2018; shallower than 25 m) around Doumer Island (Palmer Archipelago, Western Antarctic Peninsula—WAP), where only five sponge species have been known. We gathered over 215 specimens, most part identified; 18 known species and one new species. Clathria (Axosuberites) retamalesi sp. nov., is set apart from its congeners on account of the combination of its habit, categories and dimensions of spicules. The East Antarctic material named as Hymeniacidon spec. (3397 m depth) from the Gauss scientific collection has been related to the shallow species H. torquata Topsent, 1916. We described H. torquata based in several specimens (n= 51) from Doumer Island (WAP), only ca. 41 km from Petermann Island (the type locality). Spicules of H. torquata are smaller than the ones present in the Hymeniacidon spec. material, which is here named Hymeniacidon hentscheli sp. nov., since it does not fit into any known cold water species of Hymeniacidon from Antarctica or the Southern Hemisphere, due to a combination of habit, oscula shape, and spicule dimensions. Only five sponge species were previously known from Doumer Island, also collected by SCUBA. Our findings suggest that the ongoing study of collections of sponges assembled at Doumer Island will still yield new taxonomic findings.