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MBio Apr 2016A paradigm shift has recently transformed the field of biological science; molecular advances have revealed how fundamentally important microorganisms are to many... (Review)
Review
A paradigm shift has recently transformed the field of biological science; molecular advances have revealed how fundamentally important microorganisms are to many aspects of a host's phenotype and evolution. In the process, an era of "holobiont" research has emerged to investigate the intricate network of interactions between a host and its symbiotic microbial consortia. Marine sponges are early-diverging metazoa known for hosting dense, specific, and often highly diverse microbial communities. Here we synthesize current thoughts about the environmental and evolutionary forces that influence the diversity, specificity, and distribution of microbial symbionts within the sponge holobiont, explore the physiological pathways that contribute to holobiont function, and describe the molecular mechanisms that underpin the establishment and maintenance of these symbiotic partnerships. The collective genomes of the sponge holobiont form the sponge hologenome, and we highlight how the forces that define a sponge's phenotype in fact act on the genomic interplay between the different components of the holobiont.
Topics: Animals; Bacteria; Bacterial Physiological Phenomena; Genome, Bacterial; Microbial Consortia; Porifera; Symbiosis
PubMed: 27103626
DOI: 10.1128/mBio.00135-16 -
Marine Drugs Mar 2018The biosynthesis, structural diversity, and functionality of collagens of sponge origin are still paradigms and causes of scientific controversy. This review has the... (Review)
Review
The biosynthesis, structural diversity, and functionality of collagens of sponge origin are still paradigms and causes of scientific controversy. This review has the ambitious goal of providing thorough and comprehensive coverage of poriferan collagens as a multifaceted topic with intriguing hypotheses and numerous challenging open questions. The structural diversity, chemistry, and biochemistry of collagens in sponges are analyzed and discussed here. Special attention is paid to spongins, collagen IV-related proteins, fibrillar collagens from demosponges, and collagens from glass sponge skeletal structures. The review also focuses on prospects and trends in applications of sponge collagens for technology, materials science and biomedicine.
Topics: Animals; Biological Products; Collagen; Microscopy, Electron, Scanning; Porifera; Tissue Scaffolds
PubMed: 29510493
DOI: 10.3390/md16030079 -
Microbiology Spectrum Jun 2022Sponge microbiomes are typically profiled by analyzing the community DNA of whole tissues, which does not distinguish the taxa residing within sponge cells from...
Sponge microbiomes are typically profiled by analyzing the community DNA of whole tissues, which does not distinguish the taxa residing within sponge cells from extracellular microbes. To uncover the endosymbiotic microbiome, we separated the sponge cells to enrich the intracellular microbes. The intracellular bacterial community of sponge was initially assessed by amplicon sequencing, which indicated that it hosts three unique phyla not found in the extracellular and bulk tissue microbiomes. These three phyla account for 66% of the taxonomically known genera in the intracellular microbiome. The shotgun metagenomic analysis extended the taxonomic coverage to viruses and eukaryotes, revealing the most abundant signature taxa specific to the intracellular microbiome. Functional KEGG pathway annotation demonstrated that the endosymbiotic microbiome hosted the greatest number of unique gene orthologs. The pathway profiles distinguished the intra- and extracellular microbiomes from the tissue and seawater microbiomes. Carbohydrate-active enzyme analysis further discriminated each microbiome based on their representative and dominant enzyme families. One pathway involved in digestion system and family esterase had a consistently higher level in intracellular microbiome and could statistically differentiate the intracellular microbiome from the others, suggesting that triacylglycerol lipases could be the key functional component peculiar to the endosymbionts. The identified higher abundance of lipase-related eggNOG categories further supported the lipid-hydrolyzing metabolism of endosymbiotic microbiota. Pseudomonas members, reported as lipase-producing bacteria, were only in the endosymbiotic microbiome, meanwhile Pseudomonas also showed a greater abundance intracellularly. Our study aided a comprehensive sponge microbiome that demonstrated the taxonomic and functional specificity of endosymbiotic microbiota. Sponges host abundant microbial symbionts that can produce an impressive number of novel bioactive metabolites. However, knowledge on intracellular (endosymbiotic) microbiota is scarce. We characterize the composition and function of the endosymbiotic microbiome by separation of sponge cells and enrichment of intracellular microbes. We uncover a noteworthy number of taxa exclusively in the endosymbiotic microbiome. We unlock the unique pathways and enzymes of endosymbiotic taxa. This study achieves a more comprehensive sponge microbial community profile, which demonstrates the structural and functional specificity of the endosymbiotic microbiome. Our findings not only open the possibility to reveal the low abundant and the likely missed microbiota when directly sequencing the sponge bulk tissues, but also warrant future in-depth exploration within single sponge cells.
Topics: Animals; Lipase; Microbiota; Phylogeny; Porifera; RNA, Ribosomal, 16S
PubMed: 35499324
DOI: 10.1128/spectrum.02296-21 -
Genome Biology and Evolution Apr 2019Addressing the origin of axial-patterning machinery is essential for understanding the evolution of animal form. Historically, sponges, a lineage that branched off early...
Addressing the origin of axial-patterning machinery is essential for understanding the evolution of animal form. Historically, sponges, a lineage that branched off early in animal evolution, were thought to lack Hox and ParaHox genes, suggesting that these critical axial-patterning genes arose after sponges diverged. However, a recent study has challenged this long-held doctrine by claiming to identify ParaHox genes (Cdx family) in two calcareous sponge species, Sycon ciliatum and Leucosolenia complicata. We reanalyzed the main data sets in this paper and analyzed an additional data set that expanded the number of bilaterians represented and removed outgroup homeodomains. As in the previous study, our Neighbor-Joining analyses of the original data sets recovered a clade that included sponge and Cdx genes, whereas Bayesian analyses placed these sponge genes within the NKL subclass of homeodomains. Unlike the original study, only one of our two maximum-likelihood analyses was congruent with Cdx genes in sponges. Our analyses of our additional data set led to the sponge genes consistently being placed within the NKL subclass of homeodomains regardless of method or model. Our results show more support for these sponge genes belonging to the NKL subclass, and therefore imply that Hox and ParaHox genes arose after Porifera diverged from the rest of animals.
Topics: Animals; Homeodomain Proteins; Models, Genetic; Porifera
PubMed: 30859199
DOI: 10.1093/gbe/evz052 -
Microbiome Mar 2018The recognition that all macroorganisms live in symbiotic association with microbial communities has opened up a new field in biology. Animals, plants, and algae are now... (Review)
Review
The recognition that all macroorganisms live in symbiotic association with microbial communities has opened up a new field in biology. Animals, plants, and algae are now considered holobionts, complex ecosystems consisting of the host, the microbiota, and the interactions among them. Accordingly, ecological concepts can be applied to understand the host-derived and microbial processes that govern the dynamics of the interactive networks within the holobiont. In marine systems, holobionts are further integrated into larger and more complex communities and ecosystems, a concept referred to as "nested ecosystems." In this review, we discuss the concept of holobionts as dynamic ecosystems that interact at multiple scales and respond to environmental change. We focus on the symbiosis of sponges with their microbial communities-a symbiosis that has resulted in one of the most diverse and complex holobionts in the marine environment. In recent years, the field of sponge microbiology has remarkably advanced in terms of curated databases, standardized protocols, and information on the functions of the microbiota. Like a Russian doll, these microbial processes are translated into sponge holobiont functions that impact the surrounding ecosystem. For example, the sponge-associated microbial metabolisms, fueled by the high filtering capacity of the sponge host, substantially affect the biogeochemical cycling of key nutrients like carbon, nitrogen, and phosphorous. Since sponge holobionts are increasingly threatened by anthropogenic stressors that jeopardize the stability of the holobiont ecosystem, we discuss the link between environmental perturbations, dysbiosis, and sponge diseases. Experimental studies suggest that the microbial community composition is tightly linked to holobiont health, but whether dysbiosis is a cause or a consequence of holobiont collapse remains unresolved. Moreover, the potential role of the microbiome in mediating the capacity for holobionts to acclimate and adapt to environmental change is unknown. Future studies should aim to identify the mechanisms underlying holobiont dynamics at multiple scales, from the microbiome to the ecosystem, and develop management strategies to preserve the key functions provided by the sponge holobiont in our present and future oceans.
Topics: Animals; Aquatic Organisms; Bacteria; Carbon; Climate Change; Dysbiosis; Ecosystem; Microbiota; Nitrogen; Oceans and Seas; Phosphorus; Porifera; Symbiosis
PubMed: 29523192
DOI: 10.1186/s40168-018-0428-1 -
Proceedings of the National Academy of... Feb 2023Sea sponges are the largest marine source of small-molecule natural products described to date. Sponge-derived molecules, such as the chemotherapeutic eribulin, the...
Sea sponges are the largest marine source of small-molecule natural products described to date. Sponge-derived molecules, such as the chemotherapeutic eribulin, the calcium-channel blocker manoalide, and antimalarial compound kalihinol A, are renowned for their impressive medicinal, chemical, and biological properties. Sponges contain microbiomes that control the production of many natural products isolated from these marine invertebrates. In fact, all genomic studies to date investigating the metabolic origins of sponge-derived small molecules concluded that microbes-not the sponge animal host-are the biosynthetic producers. However, early cell-sorting studies suggested the sponge animal host may play a role particularly in the production of terpenoid molecules. To investigate the genetic underpinnings of sponge terpenoid biosynthesis, we sequenced the metagenome and transcriptome of an isonitrile sesquiterpenoid-containing sponge of the order Bubarida. Using bioinformatic searches and biochemical validation, we identified a group of type I terpene synthases (TSs) from this sponge and multiple other species, the first of this enzyme class characterized from the sponge holobiome. The Bubarida TS-associated contigs consist of intron-containing genes homologous to sponge genes and feature GC percentage and coverage consistent with other eukaryotic sequences. We identified and characterized TS homologs from five different sponge species isolated from geographically distant locations, thereby suggesting a broad distribution amongst sponges. This work sheds light on the role of sponges in secondary metabolite production and speaks to the possibility that other sponge-specific molecules originate from the animal host.
Topics: Animals; Porifera; Aquatic Organisms; Microbiota; Metagenome; Biological Products; Phylogeny
PubMed: 36802428
DOI: 10.1073/pnas.2220934120 -
GigaScience Oct 2017Marine sponges (phylum Porifera) are a diverse, phylogenetically deep-branching clade known for forming intimate partnerships with complex communities of microorganisms....
Marine sponges (phylum Porifera) are a diverse, phylogenetically deep-branching clade known for forming intimate partnerships with complex communities of microorganisms. To date, 16S rRNA gene sequencing studies have largely utilised different extraction and amplification methodologies to target the microbial communities of a limited number of sponge species, severely limiting comparative analyses of sponge microbial diversity and structure. Here, we provide an extensive and standardised dataset that will facilitate sponge microbiome comparisons across large spatial, temporal, and environmental scales. Samples from marine sponges (n = 3569 specimens), seawater (n = 370), marine sediments (n = 65) and other environments (n = 29) were collected from different locations across the globe. This dataset incorporates at least 268 different sponge species, including several yet unidentified taxa. The V4 region of the 16S rRNA gene was amplified and sequenced from extracted DNA using standardised procedures. Raw sequences (total of 1.1 billion sequences) were processed and clustered with (i) a standard protocol using QIIME closed-reference picking resulting in 39 543 operational taxonomic units (OTU) at 97% sequence identity, (ii) a de novo clustering using Mothur resulting in 518 246 OTUs, and (iii) a new high-resolution Deblur protocol resulting in 83 908 unique bacterial sequences. Abundance tables, representative sequences, taxonomic classifications, and metadata are provided. This dataset represents a comprehensive resource of sponge-associated microbial communities based on 16S rRNA gene sequences that can be used to address overarching hypotheses regarding host-associated prokaryotes, including host specificity, convergent evolution, environmental drivers of microbiome structure, and the sponge-associated rare biosphere.
Topics: Animals; Microbiota; Porifera; RNA, Ribosomal, 16S; Sequence Analysis, DNA
PubMed: 29020741
DOI: 10.1093/gigascience/gix077 -
Microbiome Oct 2020Viruses directly affect the most important biological processes in the ocean via their regulation of prokaryotic and eukaryotic populations. Marine sponges form stable...
BACKGROUND
Viruses 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.
RESULTS
Viromic 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.
CONCLUSIONS
Our 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. Video Abstract.
Topics: Animals; Genome, Viral; Genomics; Microbiota; Phylogeny; Porifera; Symbiosis; Viruses
PubMed: 33008461
DOI: 10.1186/s40168-020-00919-5 -
BMC Genomics Sep 2022Sponge holobionts (i.e., the host and its associated microbiota) play a key role in the cycling of dissolved organic matter (DOM) in marine ecosystems. On coral reefs,...
BACKGROUND
Sponge holobionts (i.e., the host and its associated microbiota) play a key role in the cycling of dissolved organic matter (DOM) in marine ecosystems. On coral reefs, an ecological shift from coral-dominated to algal-dominated ecosystems is currently occurring. Given that benthic corals and macroalgae release different types of DOM, in different abundances and with different bioavailability to sponge holobionts, it is important to understand how the metabolic activity of the host and associated microbiota change in response to the exposure to both DOM sources. Here, we look at the differential gene expression of two sponge holobionts 6 hours after feeding on naturally sourced coral- and macroalgal-DOM using RNA sequencing and meta-transcriptomic analysis.
RESULTS
We found a slight, but significant differential gene expression in the comparison between the coral- and macroalgal-DOM treatments in both the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Haliclona vansoesti. In the hosts, processes that regulate immune response, signal transduction, and metabolic pathways related to cell proliferation were elicited. In the associated microbiota carbohydrate metabolism was upregulated in both treatments, but coral-DOM induced further lipid and amino acids biosynthesis, while macroalgal-DOM caused a stress response. These differences could be driven by the presence of distinct organic macronutrients in the two DOM sources and of small pathogens or bacterial virulence factors in the macroalgal-DOM.
CONCLUSIONS
This work provides two new sponge meta-transcriptomes and a database of putative genes and genetic pathways that are involved in the differential processing of coral- versus macroalgal-DOM as food source to sponges with high and low abundances of associated microbes. These pathways include carbohydrate metabolism, signaling pathways, and immune responses. However, the differences in the meta-transcriptomic responses of the sponge holobionts after 6 hours of feeding on the two DOM sources were small. Longer-term responses to both DOM sources should be assessed to evaluate how the metabolism and the ecological function of sponges will be affected when reefs shift from coral towards algal dominance.
Topics: Amino Acids; Animals; Anthozoa; Coral Reefs; Dissolved Organic Matter; Lipids; Microbiota; Porifera; Transcriptome
PubMed: 36175840
DOI: 10.1186/s12864-022-08893-y -
Molecular Ecology Oct 2022Understanding the maintenance and origin of beta diversity is a central topic in ecology. However, the factors that drive diversity patterns and underlying processes...
Understanding the maintenance and origin of beta diversity is a central topic in ecology. However, the factors that drive diversity patterns and underlying processes remain unclear, particularly for host-prokaryotic associations. Here, beta diversity patterns were studied in five prokaryotic biotopes, namely, two high microbial abundance (HMA) sponge taxa (Xestospongia spp. and Hyrtios erectus), one low microbial abundance (LMA) sponge taxon (Stylissa carteri), sediment and seawater sampled across thousands of kilometres. Using multiple regression on distance matrices (MRM), spatial (geographic distance) and environmental (sea surface temperature and chlorophyll α concentrations) variables proved significant predictors of beta diversity in all five biotopes and together explained from 54% to 82% of variation in dissimilarity of both HMA species, 27% to 43% of variation in sediment and seawater, but only 20% of variation of the LMA S. carteri. Variance partitioning was subsequently used to partition the variation into purely spatial, purely environmental and spatially-structured environmental components. The amount of variation in dissimilarity explained by the purely spatial component was lowest for S. carteri at 11% and highest for H. erectus at 55%. The purely environmental component, in turn, only explained from 0.15% to 2.83% of variation in all biotopes. In addition to spatial and environmental variables, a matrix of genetic differences between pairs of sponge individuals also proved a significant predictor of variation in prokaryotic dissimilarity of the Xestospongia species complex. We discuss the implications of these results for the HMA-LMA dichotomy and compare the MRM results with results obtained using constrained ordination and zeta diversity.
Topics: Animals; Bacteria; Biodiversity; Chlorophyll; Humans; Phylogeny; Porifera; RNA, Ribosomal, 16S; Seawater
PubMed: 35881675
DOI: 10.1111/mec.16631