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Microbiome Jun 2020Marine sponges and their microbiomes contribute significantly to carbon and nutrient cycling in global reefs, processing and remineralizing dissolved and particulate...
BACKGROUND
Marine sponges and their microbiomes contribute significantly to carbon and nutrient cycling in global reefs, processing and remineralizing dissolved and particulate organic matter. Lamellodysidea herbacea sponges obtain additional energy from abundant photosynthetic Hormoscilla cyanobacterial symbionts, which also produce polybrominated diphenyl ethers (PBDEs) chemically similar to anthropogenic pollutants of environmental concern. Potential contributions of non-Hormoscilla bacteria to Lamellodysidea microbiome metabolism and the synthesis and degradation of additional secondary metabolites are currently unknown.
RESULTS
This study has determined relative abundance, taxonomic novelty, metabolic capacities, and secondary metabolite potential in 21 previously uncharacterized, uncultured Lamellodysidea-associated microbial populations by reconstructing near-complete metagenome-assembled genomes (MAGs) to complement 16S rRNA gene amplicon studies. Microbial community compositions aligned with sponge host subgroup phylogeny in 16 samples from four host clades collected from multiple sites in Guam over a 3-year period, including representatives of Alphaproteobacteria, Gammaproteobacteria, Oligoflexia, and Bacteroidetes as well as Cyanobacteria (Hormoscilla). Unexpectedly, microbiomes from one host clade also included Cyanobacteria from the prolific secondary metabolite-producer genus Prochloron, a common tunicate symbiont. Two novel Alphaproteobacteria MAGs encoded pathways diagnostic for methylotrophic metabolism as well as type III secretion systems, and have been provisionally assigned to a new order, designated Candidatus Methylospongiales. MAGs from other taxonomic groups encoded light-driven energy production pathways using not only chlorophyll, but also bacteriochlorophyll and proteorhodopsin. Diverse heterotrophic capabilities favoring aerobic versus anaerobic conditions included pathways for degrading chitin, eukaryotic extracellular matrix polymers, phosphonates, dimethylsulfoniopropionate, trimethylamine, and benzoate. Genetic evidence identified an aerobic catabolic pathway for halogenated aromatics that may enable endogenous PBDEs to be used as a carbon and energy source.
CONCLUSIONS
The reconstruction of high-quality MAGs from all microbial taxa comprising greater than 0.1% of the sponge microbiome enabled species-specific assignment of unique metabolic features that could not have been predicted from taxonomic data alone. This information will promote more representative models of marine invertebrate microbiome contributions to host bioenergetics, the identification of potential new sponge parasites and pathogens based on conserved metabolic and physiological markers, and a better understanding of biosynthetic and degradative pathways for secondary metabolites and halogenated compounds in sponge-associated microbiota. Video Abstract.
Topics: Animals; Bacteria; Biodiversity; Genomics; Metagenome; Microbiota; Phylogeny; Porifera; RNA, Ribosomal, 16S; Symbiosis
PubMed: 32576248
DOI: 10.1186/s40168-020-00877-y -
The Journal of Antibiotics Aug 2020Marine-derived bacteria are a prolific source of a wide range of structurally diverse natural products. This review, dedicated to Professor William Fenical, begins by... (Review)
Review
Marine-derived bacteria are a prolific source of a wide range of structurally diverse natural products. This review, dedicated to Professor William Fenical, begins by showcasing many seminal discoveries made at the University of California San Diego from marine-derived actinomycetes. Discussed early on is the 20-year journey of discovery and advancement of the seminal actinomycetes natural product salinosporamide A into Phase III anticancer clinical trials. There are many fascinating parallels discussed that were gleaned from the comparative literature of marine sponge, tunicate, and bacteria-derived natural products. Identifying bacterial biosynthetic machinery housed in sponge and tunicate holobionts through both culture-independent and culture-dependent approaches is another important and expanding subject that is analyzed. Work reviewed herein also evaluates the hypotheses that many marine invertebrate-derived natural products are biosynthesised by associated or symbiotic bacteria. The insights and outcomes from metagenomic sequencing and synthetic biology to expand molecule discovery continue to provide exciting outcomes and they are predicted to be the source of the next generation of novel marine natural product chemical scaffolds.
Topics: Animals; Aquatic Organisms; Bacteria; Biological Products; Metagenomics; Porifera; Urochordata
PubMed: 32507851
DOI: 10.1038/s41429-020-0330-5 -
Microbiome Feb 2021Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats. They play an important role in nutrient cycling due to their unrivalled capacity...
BACKGROUND
Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats. They play an important role in nutrient cycling due to their unrivalled capacity for processing both dissolved and particulate organic matter (DOM and POM) and the exceptional metabolic repertoire of their diverse and abundant microbial communities. Functional studies determining the role of host and microbiome in organic nutrient uptake and exchange, however, are limited. Therefore, we coupled pulse-chase isotopic tracer techniques with nanoscale secondary ion mass spectrometry (NanoSIMS) to visualise the uptake and translocation of C- and N-labelled dissolved and particulate organic food at subcellular level in the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Halisarca caerulea.
RESULTS
The two sponge species showed significant enrichment of DOM- and POM-derived C and N into their tissue over time. Microbial symbionts were actively involved in the assimilation of DOM, but host filtering cells (choanocytes) appeared to be the primary site of DOM and POM uptake in both sponge species overall, via pinocytosis and phagocytosis, respectively. Translocation of carbon and nitrogen from choanocytes to microbial symbionts occurred over time, irrespective of microbial abundance, reflecting recycling of host waste products by the microbiome.
CONCLUSIONS
Here, we provide empirical evidence indicating that the prokaryotic communities of a high and a low microbial abundance sponge obtain nutritional benefits from their host-associated lifestyle. The metabolic interaction between the highly efficient filter-feeding host and its microbial symbionts likely provides a competitive advantage to the sponge holobiont in the oligotrophic environments in which they thrive, by retaining and recycling limiting nutrients. Sponges present a unique model to link nutritional symbiotic interactions to holobiont function, and, via cascading effects, ecosystem functioning, in one of the earliest metazoan-microbe symbioses. Video abstract.
Topics: Animals; Carbon; Microbiota; Nitrogen; Nutrients; Porifera; Symbiosis
PubMed: 33583434
DOI: 10.1186/s40168-020-00984-w -
Scientific Reports Apr 2023The potential of sponge-derived chemicals for pharmaceutical applications remains largely unexploited due to limited available biomass. Although many have attempted to...
The potential of sponge-derived chemicals for pharmaceutical applications remains largely unexploited due to limited available biomass. Although many have attempted to culture marine sponge cells in vitro to create a scalable production platform for such biopharmaceuticals, these efforts have been mostly unsuccessful. We recently showed that Geodia barretti sponge cells could divide rapidly in M1 medium. In this study we established the first continuous marine sponge cell line, originating from G. barretti. G. barretti cells cultured in OpM1 medium, a modification of M1, grew more rapidly and to a higher density than in M1. Cells in OpM1 reached 1.74 population doublings after 30 min, more than twofold higher than the already rapid growth rate of 0.74 population doublings in 30 min in M1. The maximum number of population doublings increased from 5 doublings in M1 to at least 98 doublings in OpM1. Subcultured cells could be cryopreserved and used to inoculate new cultures. With these results, we have overcome a major obstacle that has blocked the path to producing biopharmaceuticals with sponge cells at industrial scale for decades.
Topics: Animals; Porifera; Cell Line; Geodia; Cell Culture Techniques
PubMed: 37031251
DOI: 10.1038/s41598-023-32394-x -
International Journal of Systematic and... Mar 2023A novel bacterial strain, designated as PHS-Z21, was isolated from the marine sponge collected from PG Dave's Rock, Philippines. Cells of PHS-Z21 are...
A novel bacterial strain, designated as PHS-Z21, was isolated from the marine sponge collected from PG Dave's Rock, Philippines. Cells of PHS-Z21 are Gram-stain-negative, non-motile, pale-yellow-pigmented, short rods. PHS-Z21 is able to grow at 10-40 ℃ (optimum, 30 ℃), pH 5.5-9.0 (optimum, pH 8.5) and with 3-9 % (w/v) NaCl (optimum, 4 %). Its 16S rRNA gene sequence shows 98.6 % similarity to CGMCC 1.7715, 98.5 % similarity to 022-2-10 and 98.4 % similarity to SW-46, respectively. The phylogenetic tree based on 16S rRNA gene sequences reveals that PHS-Z21 is clustered with SW-46. The total genome of PHS-Z21 is approximately 2 932 896 bp in size with a DNA G+C content of 64.7 %. The average nucleotide identity (ANI) and digital DNA-DNA hybridization (dDDH) values among PHS-Z21 and other type strains are 70.0-77.3 % (ANIb), 83.3-86.8 % (ANIm) and 13.0-26.9 % (dDDH), respectively. The dDDH and ANI values are below the standard cutoff criteria for delineating bacterial species. Percentage of conserved proteins (POCP) values between the genome of strain PHS-Z21 and those of members of the genera , , and were 62.0-74.5 %, 55.8-63.2 %, 60.7-66.9 % and 63.9-66.8%, respectively, while the AAI values were 68.4-74.3 %, 63.8-65.9 %, 66.3-68.3 % and 64.7-66.9%, respectively. The major fatty acids of PHS-Z21 are composed of summed feature 8 (Cω7 and/or Cω6), Cω7 11-methyl, C and summed feature 3 (Cω7 and/or Cω6). The polar lipids of PHS-Z21 mainly consist of diphosphatidylglycerol, glycolipid, phosphatidylcholine, phosphatidylethanolamine, phosphatidylglycerol and glycophospholipid. The respiratory lipoquinone was identified as Q-10. On the basis of the phenotypic and phylogenetic data, strain PHS-Z21 represents a novel species of the genus , for which the name sp. nov. is proposed. The type strain is PHS-Z21 (=MCCC 1K07849=KCTC 92590).
Topics: Animals; Fatty Acids; Phospholipids; Phylogeny; RNA, Ribosomal, 16S; Ubiquinone; Base Composition; Bacterial Typing Techniques; DNA, Bacterial; Sequence Analysis, DNA; Alphaproteobacteria; Porifera
PubMed: 36961875
DOI: 10.1099/ijsem.0.005800 -
Current Opinion in Biotechnology Apr 2022
Review
Topics: Animals; Biotechnology; Petrosia; Phylogeny; Porifera; Symbiosis
PubMed: 34800848
DOI: 10.1016/j.copbio.2021.10.022 -
European Journal of Medicinal Chemistry Aug 2021Marine ecosystem continues to produce a great wealth of molecules endowed with cytotoxic activity towards a large panel of tumor cells. Marine sponges, apparently... (Review)
Review
Marine ecosystem continues to produce a great wealth of molecules endowed with cytotoxic activity towards a large panel of tumor cells. Marine sponges, apparently defenseless organisms are endowed through evolution with a range of cytotoxic metabolites for self protection against predators and space competition. Interestingly, high biodiversity of sponges with Demospongiae and Calcarea species that have yielded numerous bioactive compounds have been accorded in different regions of the Red Sea. This review for the first time provides a comprehensive overview of 123 cytotoxic agents derived from Red Sea sponges with diverse chemical structures covered till mid 2020 showing activities ranging from mildly active to very active against different panels of cancer cell lines. It has been divided according to the different classes of compounds including alkaloids, terpenoids (sesquiterpenes, diterpenes, triterpenes, sesterterpenes, norsesterterpenes), peptides and macrolides, lipids (steroids, fatty acids/amides and glycerides) etc. The enhancement in the cytotoxicity with respect to the molecular structure changes have been described in detail. We have also accounted for the total synthesis of cytotoxic molecules, subereamolline A, aerothionin, asmarine B, norrsolide and latrunculin B showing interesting activity against different cancer cell lines.
Topics: Animals; Antineoplastic Agents; Biological Products; Cell Proliferation; Drug Discovery; Drug Screening Assays, Antitumor; Humans; Molecular Structure; Porifera
PubMed: 33940466
DOI: 10.1016/j.ejmech.2021.113491 -
Zootaxa Jan 2021This paper provides a comprehensive review of the environments where freshwater sponges occur and evaluates the use of sponge spicules as a proxy in paleoenvironmental... (Review)
Review
This paper provides a comprehensive review of the environments where freshwater sponges occur and evaluates the use of sponge spicules as a proxy in paleoenvironmental studies in the Neotropical region. The paper aims to: I) review the information about the ecology of inland sponges to facilitate the use of spicules as a paleoenvironmental tool; and II) identify possible incongruities in the use of this information in paleoenvironmental reconstructions that have been conducted in Neotropical regions. The study compiled data on 77 sponge species, specialist or generalist that occur under certain environmental conditions, such as: substrate type for growth, hydrodynamic types, as well as salinity and acidity concentrations. In addition, it provides a comparison of the paleoenvironmental conditions applied to reconstruction studies that have been carried out within this biogeographic region, highlighting incongruities regarding the current ecology of the sponges.
Topics: Animals; Fresh Water; Porifera
PubMed: 33756551
DOI: 10.11646/zootaxa.4915.4.3 -
Journal of Experimental Zoology. Part... Jan 2020Origin and early evolution of regeneration mechanisms remain among the most pressing questions in animal regeneration biology. Porifera have exceptional regenerative...
Origin and early evolution of regeneration mechanisms remain among the most pressing questions in animal regeneration biology. Porifera have exceptional regenerative capacities and, as early Metazoan lineage, are a promising model for studying evolutionary aspects of regeneration. Here, we focus on reparative regeneration of the body wall in the Mediterranean demosponge Aplysina cavernicola. The epithelialization of the wound surface is completed within 2 days, and the wound is completely healed within 2 weeks. The regeneration is accompanied with the formation of a mass of undifferentiated cells (blastema), which consists of archaeocytes, dedifferentiated choanocytes, anucleated amoebocytes, and differentiated spherulous cells. The main mechanisms of A. cavernicola regeneration are cell dedifferentiation with active migration and subsequent redifferentiation or transdifferentiation of polypotent cells through the mesenchymal-to-epithelial transformation. The main cell sources of the regeneration are archaeocytes and choanocytes. At early stages of the regeneration, the blastema almost devoid of cell proliferation, but after 24 hr postoperation (hpo) and up to 72 hpo numerous DNA-synthesizing cells appear there. In contrast to intact tissues, where vast majority of DNA-synthesizing cells are choanocytes, all 5-ethynyl-2'-deoxyuridine-labeled cells in the blastema are mesohyl cells. Intact tissues, distant from the wound, retains intact level of cell proliferation during whole regeneration process. For the first time, the apoptosis was studied during the regeneration of sponges. Two waves of apoptosis were detected during A. cavernicola regeneration: The first wave at 6-12 hpo and the second wave at 48-72 hpo.
Topics: Animals; Cell Differentiation; Cell Transdifferentiation; Porifera; Regeneration
PubMed: 31725194
DOI: 10.1002/jez.b.22919 -
International Journal of Molecular... Sep 2022Metabolomics represent the set of small organic molecules generally called metabolites, which are located within cells, tissues or organisms. This new "omic" technology,... (Review)
Review
Metabolomics represent the set of small organic molecules generally called metabolites, which are located within cells, tissues or organisms. This new "omic" technology, together with other similar technologies (genomics, transcriptomics and proteomics) is becoming a widely used tool in cancer research, aiming at the understanding of global biology systems in their physiologic or altered conditions. Cancer is among the most alarming human diseases and it causes a considerable number of deaths each year. Cancer research is one of the most important fields in life sciences. In fact, several scientific advances have been made in recent years, aiming to illuminate the metabolism of cancer cells, which is different from that of healthy cells, as suggested by Otto Warburg in the 1950s. Studies on sponges and algae revealed that these organisms are the main sources of the marine bioactive compounds involved in drug discovery for cancer treatment and prevention. In this review, we analyzed these two promising groups of marine organisms to focus on new metabolomics approaches for the study of metabolic changes in cancer cell lines treated with chemical extracts from sponges and algae, and for the classification of the chemical structures of bioactive compounds that may potentially prove useful for specific biotechnological applications.
Topics: Animals; Aquatic Organisms; Biotechnology; Humans; Metabolome; Neoplasms; Plant Extracts; Porifera
PubMed: 36142592
DOI: 10.3390/ijms231810680