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Scientific Reports Mar 2024Marine sponges host diverse microbial communities. Although we know many of its ecological patterns, a deeper understanding of the polar sponge holobiont is still...
Marine sponges host diverse microbial communities. Although we know many of its ecological patterns, a deeper understanding of the polar sponge holobiont is still needed. We combine high-throughput sequencing of ribosomal genes, including the largest taxonomic repertoire of Antarctic sponge species analyzed to date, functional metagenomics, and metagenome-assembled genomes (MAGs). Our findings show that sponges harbor more exclusive bacterial and archaeal communities than seawater, while microbial eukaryotes are mostly shared. Furthermore, bacteria in Antarctic sponge holobionts establish more cooperative interactions than in sponge holobionts from other environments. The bacterial classes that established more positive relations were Bacteroidia, Gamma- and Alphaproteobacteria. Antarctic sponge microbiomes contain microbial guilds that encompass ammonia-oxidizing archaea, ammonia-oxidizing bacteria, nitrite-oxidizing bacteria, and sulfur-oxidizing bacteria. The retrieved MAGs showed a high level of novelty and streamlining signals and belong to the most abundant members of the main microbial guilds in the Antarctic sponge holobiont. Moreover, the genomes of these symbiotic bacteria contain highly abundant functions related to their adaptation to the cold environment, vitamin production, and symbiotic lifestyle, helping the holobiont survive in this extreme environment.
Topics: Animals; Porifera; Antarctic Regions; Ammonia; Archaea; Bacteria; Microbiota; Phylogeny; RNA, Ribosomal, 16S
PubMed: 38493232
DOI: 10.1038/s41598-024-56480-w -
Antonie Van Leeuwenhoek Mar 2024A new member of the family Flavobacteriaceae (termed Hal144) was isolated from the marine breadcrumb sponge Halichondria panicea. Sponge material was collected in 2018...
A new member of the family Flavobacteriaceae (termed Hal144) was isolated from the marine breadcrumb sponge Halichondria panicea. Sponge material was collected in 2018 at Schilksee which is located in the Kiel Fjord (Baltic Sea, Germany). Phylogenetic analysis of the full-length Hal144 16S rRNA gene sequence revealed similarities from 94.3 to 96.6% to the nearest type strains of the genus Maribacter. The phylogenetic tree of the 16S rRNA gene sequences depicted a cluster of strain Hal144 with its closest relatives Maribacter aestuarii GY20 (96.6%) and Maribacter thermophilus HT7-2 (96.3%). Genome phylogeny showed that Maribacter halichondriae Hal144 branched from a cluster consisting of Maribacter arenosus, Maribacter luteus, and Maribacter polysiphoniae. Genome comparisons of strain Maribacter halichondriae Hal144 with Maribacter sp. type strains exhibited average nucleotide identities in the range of 75-76% and digital DNA-DNA hybridisation values in the range of 13.1-13.4%. Compared to the next related type strains, strain Hal144 revealed unique genomic features such as phosphoenolpyruvate-dependent phosphotransferase system pathway, serine-glyoxylate cycle, lipid A 3-O-deacylase, 3-hexulose-6-phosphate synthase, enrichment of pseudogenes and of genes involved in cell wall and envelope biogenesis, indicating an adaptation to the host. Strain Hal144 was determined to be Gram-negative, mesophilic, strictly aerobic, flexirubin positive, resistant to aminoglycoside antibiotics, and able to utilize N-acetyl-β-D-glucosamine. Optimal growth occurred at 25-30 °C, within a salinity range of 2-6% sea salt, and a pH range between 5 and 8. The major fatty acids identified were C 3-OH, iso-C, and iso-C G. The DNA G + C content of strain Hal144 was 41.4 mol%. Based on the polyphasic approach, strain Hal144 represents a novel species of the genus Maribacter, and we propose the name Maribacter halichondriae sp. nov. The type strain is Hal144 (= DSM 114563 = LMG 32744).
Topics: Animals; Seawater; Phosphatidylethanolamines; Phylogeny; RNA, Ribosomal, 16S; Porifera; DNA, Bacterial; Sequence Analysis, DNA; Bacterial Typing Techniques; Vitamin K 2; Fatty Acids; Flavobacteriaceae
PubMed: 38489089
DOI: 10.1007/s10482-024-01950-4 -
Frontiers in Microbiology 2024Metaorganism research contributes substantially to our understanding of the interaction between microbes and their hosts, as well as their co-evolution. Most research is...
Metaorganism research contributes substantially to our understanding of the interaction between microbes and their hosts, as well as their co-evolution. Most research is currently focused on the bacterial community, while archaea often remain at the sidelines of metaorganism-related research. Here, we describe the archaeome of a total of eleven classical and emerging multicellular model organisms across the phylogenetic tree of life. To determine the microbial community composition of each host, we utilized a combination of archaea and bacteria-specific 16S rRNA gene amplicons. Members of the two prokaryotic domains were described regarding their community composition, diversity, and richness in each multicellular host. Moreover, association with specific hosts and possible interaction partners between the bacterial and archaeal communities were determined for the marine models. Our data show that the archaeome in marine hosts predominantly consists of and , which represent keystone taxa among the porifera. The presence of an archaeome in the terrestrial hosts varies substantially. With respect to abundant archaeal taxa, they harbor a higher proportion of methanoarchaea over the aquatic environment. We find that the archaeal community is much less diverse than its bacterial counterpart. Archaeal amplicon sequence variants are usually host-specific, suggesting adaptation through co-evolution with the host. While bacterial richness was higher in the aquatic than the terrestrial hosts, a significant difference in diversity and richness between these groups could not be observed in the archaeal dataset. Our data show a large proportion of unclassifiable archaeal taxa, highlighting the need for improved cultivation efforts and expanded databases.
PubMed: 38476944
DOI: 10.3389/fmicb.2024.1347422 -
Environmental Microbiome Mar 2024Poriferans (sponges) are highly adaptable organisms that can thrive in diverse marine and freshwater environments due, in part, to their close associations with internal...
BACKGROUND
Poriferans (sponges) are highly adaptable organisms that can thrive in diverse marine and freshwater environments due, in part, to their close associations with internal microbial communities. This sponge microbiome can be acquired from the surrounding environment (horizontal acquisition) or obtained from the parents during the reproductive process through a variety of mechanisms (vertical transfer), typically resulting in the presence of symbiotic microbes throughout all stages of sponge development. How and to what extent the different components of the microbiome are transferred to the developmental stages remain poorly understood. Here, we investigated the microbiome composition of a common, low-microbial-abundance, Atlantic-Mediterranean sponge, Crambe crambe, throughout its ontogeny, including adult individuals, brooded larvae, lecithotrophic free-swimming larvae, newly settled juveniles still lacking osculum, and juveniles with a functional osculum for filter feeding.
RESULTS
Using 16S rRNA gene analysis, we detected distinct microbiome compositions in each ontogenetic stage, with variations in composition, relative abundance, and diversity of microbial species. However, a particular dominant symbiont, Candidatus Beroebacter blanensis, previously described as the main symbiont of C. crambe, consistently occurred throughout all stages, an omnipresence that suggests vertical transmission from parents to offspring. This symbiont fluctuated in relative abundance across developmental stages, with pronounced prevalence in lecithotrophic stages. A major shift in microbial composition occurred as new settlers completed osculum formation and acquired filter-feeding capacity. Candidatus Beroebacter blanensis decreased significatively at this point. Microbial diversity peaked in filter-feeding stages, contrasting with the lower diversity of lecithotrophic stages. Furthermore, individual specific transmission patterns were detected, with greater microbial similarity between larvae and their respective parents compared to non-parental conspecifics.
CONCLUSIONS
These findings suggest a putative vertical transmission of the dominant symbiont, which could provide some metabolic advantage to non-filtering developmental stages of C. crambe. The increase in microbiome diversity with the onset of filter-feeding stages likely reflects enhanced interaction with environmental microbes, facilitating horizontal transmission. Conversely, lower microbiome diversity in lecithotrophic stages, prior to filter feeding, suggests incomplete symbiont transfer or potential symbiont digestion. This research provides novel information on the dynamics of the microbiome through sponge ontogeny, on the strategies for symbiont acquisition at each ontogenetic stage, and on the potential importance of symbionts during larval development.
PubMed: 38468324
DOI: 10.1186/s40793-024-00556-7 -
Data in Brief Apr 2024Biodiversity information in the form of species occurrence records is key for monitoring and predicting current and future biodiversity patterns, as well as for guiding...
Biodiversity information in the form of species occurrence records is key for monitoring and predicting current and future biodiversity patterns, as well as for guiding conservation and management strategies. However, the reliability and accuracy of this information are frequently undermined by taxonomic and spatial errors. Additionally, biodiversity information facilities often share data in diverse incompatible formats, precluding seamless integration and interoperability. We provide a comprehensive quality-controlled dataset of occurrence records of the Class Demospongiae, which comprises 81% of the entire Porifera phylum. Demosponges are ecologically significant as they structure rich habitats and play a key role in nutrient cycling within marine benthic communities. The dataset aggregates occurrence records from multiple sources, employs dereplication and taxonomic curation techniques, and is flagged for potentially incorrect records based on expert knowledge regarding each species' bathymetric and geographic distributions. It yields 417,626 records of 1,816 accepted demosponge species (of which 321,660 records of 1,495 species are flagged as potentially correct), which are provided under the FAIR principle of Findability, Accessibility, Interoperability and Reusability in the Darwin Core Standard. This dataset constitutes the most up-to-date baseline for studying demosponge diversity at the global scale, enabling researchers to examine biodiversity patterns (e.g., species richness and endemicity), and forecast potential distributional shifts under future scenarios of climate change.
PubMed: 38435734
DOI: 10.1016/j.dib.2024.110200 -
PeerJ 2024Coral reefs are biodiverse ecosystems that rely on trophodynamic transfers from primary producers to consumers through the detrital pathway. The sponge loop hypothesis...
Coral reefs are biodiverse ecosystems that rely on trophodynamic transfers from primary producers to consumers through the detrital pathway. The sponge loop hypothesis proposes that sponges consume dissolved organic carbon (DOC) and produce large quantities of detritus on coral reefs, with this turn-over approaching the daily gross primary production of the reef ecosystem. In this study, we collected samples of detritus in the epilithic algal matrix (EAM) and samples from potential sources of detritus over two seasons from the forereef at Carrie Bow Cay, Belize. We chose this location to maximize the likelihood of finding support for the sponge loop hypothesis because Caribbean reefs have higher sponge abundances than other tropical reefs worldwide and the Mesoamerican barrier reef is an archetypal coral reef ecosystem. We used stable isotope analyses and eDNA metabarcoding to determine the composition of the detritus. We determined that the EAM detritus was derived from a variety of benthic and pelagic sources, with primary producers (micro- and macroalgae) as major contributors and metazoans (Arthropoda, Porifera, Cnidaria, Mollusca) as minor contributors. None of the sponge species that reportedly produce detritus were present in EAM detritus. The cnidarian signature in EAM detritus was dominated by octocorals, with a scarcity of hard corals. The composition of detritus also varied seasonally. The negligible contribution of sponges to reef detritus contrasts with the detrital pathway originally proposed in the sponge loop hypothesis. The findings indicate a mix of pelagic and benthic sources in the calmer summer and primarily benthic sources in the more turbulent spring.
Topics: Animals; Ecosystem; Coral Reefs; Anthozoa; Caribbean Region; Isotopes
PubMed: 38410802
DOI: 10.7717/peerj.16970 -
Frontiers in Microbiology 2024Antarctic Porifera have gained increasing interest as hosts of diversified associated microbial communities that could provide interesting insights on the holobiome...
INTRODUCTION
Antarctic Porifera have gained increasing interest as hosts of diversified associated microbial communities that could provide interesting insights on the holobiome system and its relation with environmental parameters.
METHODS
The Antarctic demosponge species and were targeted for the determination of persistent organic pollutant (i. e., polychlorobiphenyls, PCBs, and polycyclic aromatic hydrocarbons, PAHs) and trace metal concentrations, along with the characterization of the associated prokaryotic communities by the 16S rRNA next generation sequencing, to evaluate possible relationships between pollutant accumulation (e.g., as a stress factor) and prokaryotic community composition in Antarctic sponges. To the best of our knowledge, this approach has been never applied before.
RESULTS
Notably, both chemical and microbiological data on (a quite rare species in the Ross Sea) are here reported for the first time, as well as the determination of PAHs in Antarctic Porifera. Both sponge species generally contained higher amounts of pollutants than the surrounding sediment and seawater, thus demonstrating their accumulation capability. The structure of the associated prokaryotic communities, even if differing at order and genus levels between the two sponge species, was dominated by and (with abundances that were negligible) and appeared in sharp contrast to communities inhabiting the bulk environment.
DISCUSSIONS
Results suggested that some bacterial groups associated with and were significantly (positively or negatively) correlated to the occurrence of certain contaminants.
PubMed: 38404594
DOI: 10.3389/fmicb.2024.1341641 -
Marine Drugs Jan 2024is a collagen-rich marine sponge that is considered a sustainable and viable option for producing an alternative to mammalian-origin collagens. However, there is a lack...
is a collagen-rich marine sponge that is considered a sustainable and viable option for producing an alternative to mammalian-origin collagens. However, there is a lack of knowledge regarding the properties of collagen isolated from different sponge parts, namely the outer region, or cortex, (ectosome) and the inner region (choanosome), and how it affects the development of biomaterials. In this study, a brief histological analysis focusing on collagen spatial distribution and a comprehensive comparative analysis between collagen isolated from ectosome and choanosome are presented. The isolated collagen characterization was based on isolation yield, Fourier-transformed infrared spectroscopy (FTIR), circular dichroism (CD), SDS-PAGE, dot blot, and amino acid composition, as well as their cytocompatibility envisaging the development of future biomedical applications. An isolation yield of approximately 20% was similar for both sponge parts, as well as the FTIR, CD, and SDS-PAGE profiles, which demonstrated that both isolated collagens presented a high purity degree and preserved their triple helix and fibrillar conformation. Ectosome collagen had a higher OHpro content and possessed collagen type I and IV, while the choanosome was predominately constituted by collagen type IV. In vitro cytotoxicity assays using the L929 fibroblast cell line displayed a significant cytotoxic effect of choanosome collagen at 2 mg/mL, while ectosome collagen enhanced cell metabolism and proliferation, thus indicating the latter as being more suitable for the development of biomaterials. This research represents a unique comparative study of body parts, serving as a support for further establishing this marine sponge as a promising alternative collagen source for the future development of biomedical applications.
Topics: Animals; Cell-Derived Microparticles; Biocompatible Materials; Porifera; Collagen; Collagen Type I; Mammals
PubMed: 38393026
DOI: 10.3390/md22020055 -
Marine Drugs Jan 2024Mycalin A (MA) is a polybrominated C-15 acetogenin isolated from the marine sponge . Since this substance displays a strong antiproliferative bioactivity towards some...
Mycalin A (MA) is a polybrominated C-15 acetogenin isolated from the marine sponge . Since this substance displays a strong antiproliferative bioactivity towards some tumour cells, we have now directed our studies towards the elucidation of the MA interactome through functional proteomic approaches, (DARTS and t-LIP-MS). DARTS experiments were performed on Hela cell lysates with the purpose of identifying MA main target protein(s); t-LiP-MS was then applied for an in-depth investigation of the MA-target protein interaction. Both these techniques exploit limited proteolysis coupled with MS analysis. To corroborate LiP data, molecular docking studies were performed on the complexes. Finally, biological and SPR analysis were conducted to explore the effect of the binding. Mortalin (GRP75) was identified as the MA's main interactor. This protein belongs to the Hsp70 family and has garnered significant attention due to its involvement in certain forms of cancer. Specifically, its overexpression in cancer cells appears to hinder the pro-apoptotic function of p53, one of its client proteins, because it becomes sequestered in the cytoplasm. Our research, therefore, has been focused on the possibility that MA might prevent this sequestration, promoting the re-localization of p53 to the nucleus and facilitating the apoptosis of tumor cells.
Topics: Animals; Humans; Acetogenins; Porifera; Molecular Docking Simulation; HeLa Cells; Proteomics; Tumor Suppressor Protein p53; HSP70 Heat-Shock Proteins
PubMed: 38393023
DOI: 10.3390/md22020052 -
Cellular & Molecular Biology Letters Feb 2024The R-RAS2 is a small GTPase highly similar to classical RAS proteins at the regulatory and signaling levels. The high evolutionary conservation of R-RAS2, its links to...
BACKGROUND
The R-RAS2 is a small GTPase highly similar to classical RAS proteins at the regulatory and signaling levels. The high evolutionary conservation of R-RAS2, its links to basic cellular processes and its role in cancer, make R-RAS2 an interesting research topic. To elucidate the evolutionary history of R-RAS proteins, we investigated and compared structural and functional properties of ancestral type R-RAS protein with human R-RAS2.
METHODS
Bioinformatics analysis were used to elucidate the evolution of R-RAS proteins. Intrinsic GTPase activity of purified human and sponge proteins was analyzed with GTPase-Glo Assay kit. The cell model consisted of human breast cancer cell lines MCF-7 and MDA-MB-231 transiently transfected with EsuRRAS2-like or HsaRRAS2. Biological characterization of R-RAS2 proteins was performed by Western blot on whole cell lysates or cell adhesion protein isolates, immunofluorescence and confocal microscopy, MTT test, colony formation assay, wound healing and Boyden chamber migration assays.
RESULTS
We found that the single sponge R-RAS2-like gene/protein probably reflects the properties of the ancestral R-RAS protein that existed prior to duplications during the transition to Bilateria, and to Vertebrata. Biochemical characterization of sponge and human R-RAS2 showed that they have the same intrinsic GTPase activity and RNA binding properties. By testing cell proliferation, migration and colony forming efficiency in MDA-MB-231 human breast cancer cells, we showed that the ancestral type of the R-RAS protein, sponge R-RAS2-like, enhances their oncogenic potential, similar to human R-RAS2. In addition, sponge and human R-RAS2 were not found in focal adhesions, but both homologs play a role in their regulation by increasing talin1 and vinculin.
CONCLUSIONS
This study suggests that the ancestor of all animals possessed an R-RAS2-like protein with oncogenic properties similar to evolutionarily more recent versions of the protein, even before the appearance of true tissue and the origin of tumors. Therefore, we have unraveled the evolutionary history of R-RAS2 in metazoans and improved our knowledge of R-RAS2 properties, including its structure, regulation and function.
Topics: Animals; Female; Humans; Breast Neoplasms; Cell Proliferation; Monomeric GTP-Binding Proteins; ras Proteins; Signal Transduction
PubMed: 38383288
DOI: 10.1186/s11658-024-00546-0