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BMC Biology May 2022Marine sponges (phylum Porifera) form symbioses with diverse microbial communities that can be transmitted between generations through their developmental stages. Here,... (Review)
Review
Marine sponges (phylum Porifera) form symbioses with diverse microbial communities that can be transmitted between generations through their developmental stages. Here, we integrate embryology and microbiology to review how symbiotic microorganisms are transmitted in this early-diverging lineage. We describe that vertical transmission is widespread but not universal, that microbes are vertically transmitted during a select developmental window, and that properties of the developmental microbiome depends on whether a species is a high or low microbial abundance sponge. Reproduction, development, and symbiosis are thus deeply rooted, but why these partnerships form remains the central and elusive tenet of these developmental symbioses.
Topics: Animals; Microbiota; Phylogeny; Porifera; RNA, Ribosomal, 16S; Reproduction; Symbiosis
PubMed: 35524305
DOI: 10.1186/s12915-022-01291-6 -
Zootaxa Apr 2023This study describes 81 specimens belonging to Suberitida, collected during the projects Esponjas del Perú (ESPER), Esponjas da América do Sul (EsponjAS) and Semilla...
This study describes 81 specimens belonging to Suberitida, collected during the projects Esponjas del Perú (ESPER), Esponjas da América do Sul (EsponjAS) and Semilla UCSUR 2019 (Demospongiae) along the coast of Peru, down to 30 m depth. Using morphological analyses, eight species were identified, one of which is new to science: Halichondria (H.) cristata, H. (H.) prostrata, Hymeniacidon perlevis, Johannesia reticulosa, Plicatellopsis expansa, Suberites aff. latus, Terpios cf. granulosus and Suberites inti sp. nov. Halichondria (H.) cristata, originally from Tierra del Fuego (SW Atlantic), was found widely distributed along the coast of Peru (06° S-14° S). The Magellanican H. (H.) prostrata and the formerly Chilean endemic P. expansa are extended up to Central Peru (12° S). Hymeniacidon perlevis, which presents a highly variable morphology (colour, shape, and spicule size), is firstly reported from the SE Pacific and its continuous occurrence in Peru (04° S-17° S) should be monitored given its supposed invasive potential. Johannesia reticulosa, previously known from Chile (20° S) and southern Peru (13° S), was found further north (11° S). Suberites latus and T. granulosus were originally recorded far-off from the Peruvian coast, in British Columbia and Hawaii, respectively. Thus, the occurrences of Suberites aff. latus and Terpios cf. granulosus are unexpected and should receive special attention in future molecular studies assessing their taxonomical status. Suberites inti sp. nov. characterised by its skeleton with ectosomal bouquets and multispicular choanosomal tracts, and two categories of straight tylostyles, is provisionally endemic to Paracas (13° S). With these results, the number of shallow Suberitida from Peru increases from 2 to 9. However, this number might rise as sampling in deeper environments could bring descriptions of new records.
Topics: Animals; Peru; Suberites; Porifera
PubMed: 37518036
DOI: 10.11646/zootaxa.5264.4.1 -
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 -
Photochemistry and Photobiology Jan 2017The photolyase/cryptochrome (PHR/CRY) family is a large group of proteins with similar structure but very diverge functions such as DNA repair, circadian clock resetting... (Review)
Review
The photolyase/cryptochrome (PHR/CRY) family is a large group of proteins with similar structure but very diverge functions such as DNA repair, circadian clock resetting and regulation of transcription. As a result of advances in the biochemistry of the CRY/PHR family and identification of new members, several adjustments have been made to the classification of this protein family. For example, a new class of PHRs, Class III, has been proposed. Furthermore, CRYs have been suggested to function as photosensory proteins in the primordial eye of sponge larvae. Additionally, a magnetosensory function has been attributed to certain CRYs. Recent advances in the field enabled us to propose a comprehensive classification scheme and nomenclatural system for this family. This review focuses on the computational and biochemical classifications of the PHR/CRY family. Several examples show that computational analysis can give a hinge about the function of newly discovered members before performing any biochemical study.
Topics: Animals; Circadian Rhythm; Cryptochromes; Deoxyribodipyrimidine Photo-Lyase; Larva; Phylogeny; Porifera
PubMed: 27864885
DOI: 10.1111/php.12676 -
MBio Dec 2022Chemists have studied marine animals for the better part of a century because they contain a diverse array of bioactive compounds. Tens of thousands of compounds have...
Chemists have studied marine animals for the better part of a century because they contain a diverse array of bioactive compounds. Tens of thousands of compounds have been reported, many with elaborate structural motifs and biological mechanisms of action found nowhere else. The challenge holding back the field has long been that of supply. Compounds are sometimes obtained by cultivating marine animals or by wild harvest, but this often presents logistical and environmental challenges. Some of the most medically important marine animal compounds are supplied by synthesis, often through multistep procedures that delay drug development. A relatively small number of such agents have been approved by the U.S. Food and Drug Administration, often after a heroic effort. In a recent paper, Uppal and coworkers (https://doi.org/10.1128/mBio.01524-22) address key hurdles underlying the supply issue, discovering an uncultivated new bacterial genus from a marine sponge and reconstituting the biosynthetic pathway for expression.
Topics: Animals; Porifera; Bacteria; Drug Development; Drug Discovery; Biological Products
PubMed: 36314838
DOI: 10.1128/mbio.02499-22 -
Integrative and Comparative Biology Oct 2019The chemical ecology and chemical defenses of sponges have been investigated for decades; consequently, sponges are among the best understood marine organisms in terms... (Review)
Review
The chemical ecology and chemical defenses of sponges have been investigated for decades; consequently, sponges are among the best understood marine organisms in terms of their chemical ecology, from the level of molecules to ecosystems. Thousands of natural products have been isolated and characterized from sponges, and although relatively few of these compounds have been studied for their ecological functions, some are known to serve as chemical defenses against predators, microorganisms, fouling organisms, and other competitors. Sponges are hosts to an exceptional diversity of microorganisms, with almost 40 microbial phyla found in these associations to date. Microbial community composition and abundance are highly variable across host taxa, with a continuum from diverse assemblages of many microbial taxa to those that are dominated by a single microbial group. Microbial communities expand the nutritional repertoire of their hosts by providing access to inorganic and dissolved sources of nutrients. Not only does this continuum of microorganism-sponge associations lead to divergent nutritional characteristics in sponges, these associated microorganisms and symbionts have long been suspected, and are now known, to biosynthesize some of the natural products found in sponges. Modern "omics" tools provide ways to study these sponge-microbe associations that would have been difficult even a decade ago. Metabolomics facilitate comparisons of sponge compounds produced within and among taxa, and metagenomics and metatranscriptomics provide tools to understand the biology of host-microbe associations and the biosynthesis of ecologically relevant natural products. These combinations of ecological, microbiological, metabolomic and genomics tools, and techniques provide unprecedented opportunities to advance sponge biology and chemical ecology across many marine ecosystems.
Topics: Animals; Aquatic Organisms; Genome; Host Microbial Interactions; Microbiota; Porifera; Transcriptome
PubMed: 30942859
DOI: 10.1093/icb/icz014 -
Environmental Microbiology Reports Dec 2020Sponges have co-evolved for millions of years alongside several types of microorganisms, which aside from participating in the animal's diet, are mostly symbionts. Since... (Review)
Review
Sponges have co-evolved for millions of years alongside several types of microorganisms, which aside from participating in the animal's diet, are mostly symbionts. Since most of the genetic repertoire in the holobiont genome is provided by microbes, it is expected that the host-associated microbiome will be at least partially heritable. Sponges can therefore acquire their symbionts in different ways. Both vertical transmission (VT) and horizontal transmission (HT) have different advantages and disadvantages in the life cycle of these invertebrates. However, a third mode of transmission, called leaky vertical transmission or mixed mode of transmission (MMT), which incorporates both VT and HT modes, has gained relevance and seems to be the most robust model. In that regard, the aim of this review is to present the evolving knowledge on these main modes of transmission of the sponge microbiome. Our conclusions lead us to suggest that MMT may be more common for all sponges, with its frequency varying across the transmission spectrum between species and the environment. This hybrid model supports the stable and specific transmission of these microbial partners and reinforces their assistance in the resilience of sponges over the years.
Topics: Animals; Bacteria; Bacterial Physiological Phenomena; Microbiota; Models, Biological; Phylogeny; Porifera; Symbiosis
PubMed: 33048474
DOI: 10.1111/1758-2229.12896 -
Philosophical Transactions of the Royal... Dec 2015Recent phylogenomic evidence suggests that ctenophores may be the sister group to the rest of animals. This phylogenetic arrangement opens the possibility that sponges... (Review)
Review
Recent phylogenomic evidence suggests that ctenophores may be the sister group to the rest of animals. This phylogenetic arrangement opens the possibility that sponges and placozoans could have lost neural cell types or that the ctenophore nervous system evolved independently. We critically review evidence to date that has been put forth in support of independent evolution of neural cell types in ctenophores. We observe a reluctance in the literature to consider a lost nervous system in sponges and placozoans and suggest that this may be due to historical bias and the commonly misconstrued concept of animal complexity. In support of the idea of loss (or modification beyond recognition), we provide hypothetical scenarios to show how sponges and placozoans may have benefitted from the loss and/or modification of their neural cell types.
Topics: Animals; Biological Evolution; Nervous System; Neurons; Placozoa; Porifera
PubMed: 26554046
DOI: 10.1098/rstb.2015.0059 -
Molecules (Basel, Switzerland) Jan 2021Glycan-to-glycan binding was shown by biochemical and biophysical measurements to mediate xenogeneic self-recognition and adhesion in sponges, stage-specific cell... (Review)
Review
Glycan-to-glycan binding was shown by biochemical and biophysical measurements to mediate xenogeneic self-recognition and adhesion in sponges, stage-specific cell compaction in mice embryos, and in vitro tumor cell adhesion in mammals. This intermolecular recognition process is accepted as the new paradigm accompanying high-affinity and low valent protein-to-protein and protein-to-glycan binding in cellular interactions. Glycan structures in sponges have novel species-specific sequences. Their common features are the large size >100 kD, polyvalency >100 repeats of the specific self-binding oligosaccharide, the presence of fucose, and sulfated and/or pyruvylated hexoses. These structural and functional properties, different from glycosaminoglycans, inspired their classification under the glyconectin name. The molecular mechanism underlying homophilic glyconectin-to-glyconectin binding relies on highly polyvalent, strong, and structure-specific interactions of small oligosaccharide motifs, possessing ultra-weak self-binding strength and affinity. Glyconectin localization at the glycocalyx outermost cell surface layer suggests their role in the initial recognition and adhesion event during the complex and multistep process. In mammals, Le-to-Le homophilic binding is structure-specific and has ultra-weak affinity. Cell adhesion is achieved through highly polyvalent interactions, enabled by clustering of small low valent structure in plasma membranes.
Topics: Animals; Binding Sites; Cell Adhesion; Particle Size; Polymers; Polysaccharides; Porifera
PubMed: 33451117
DOI: 10.3390/molecules26020397 -
Journal of Natural Products May 2022Investigation of the marine sponge MeOH fractions using feature-based molecular networking, dereplication, and isolation led to the discovery of new... (Review)
Review
Investigation of the marine sponge MeOH fractions using feature-based molecular networking, dereplication, and isolation led to the discovery of new bromopyrrole-derived metabolites. An in-house library of bromopyrrole alkaloids previously isolated from and sp. was utilized, along with the investigation of an MS/MS fragmentation of these compounds. Our strategy led to the isolation and identification of the disparamides A-C (-), with a novel carbon skeleton. Additionally, new dispyrins B-F (-) and nagelamides H2 and H3 ( and ) and known nagelamide H (), citrinamine B (), ageliferin (), bromoageliferin (), and dibromoageliferin () were also isolated and identified by analysis of spectroscopic data. Analysis of MS/MS fragmentation data and molecular networking analysis indicated the presence of hymenidin (), oroidin (), dispacamide (), monobromodispacamide (), keramadine (), longamide B (), methyl ester of longamide B (), hanishin (), methyl ester of 3-debromolongamide B (), and 3-debromohanishin (). Antibacterial activity of ageliferin (), bromoageliferin (), and dibromoageliferin () was evaluated against susceptible and multi-drug-resistant ESKAPE pathogenic bacteria , , , , , and . Dibromoageliferin () displayed the most potent antimicrobial activity against all tested susceptible and MDR strains. Compounds - presented no significant hemolytic activity up to 100 μM.
Topics: Agelas; Alkaloids; Animals; Anti-Bacterial Agents; Escherichia coli; Esters; Molecular Structure; Porifera; Pyrroles; Tandem Mass Spectrometry
PubMed: 35427139
DOI: 10.1021/acs.jnatprod.2c00094