Authors: Jacob M Musser, Klaske J Schippers, Michael Nickel...

The evolutionary origin of metazoan cell types such as neurons and muscles is not known. Using whole-body single-cell RNA sequencing in a sponge, an animal without nervous system and musculature, we identified 18 distinct cell types. These include nitric oxide–sensitive contractile pinacocytes, amoeboid phagocytes, and secretory neuroid cells that reside in close contact with digestive choanocytes that express scaffolding and receptor proteins. Visualizing neuroid cells by correlative x-ray and electron microscopy revealed secretory vesicles and cellular projections enwrapping choanocyte microvilli and cilia. Our data show a communication system that is organized around sponge digestive chambers, using conserved modules that became incorporated into the pre- and postsynapse in the nervous systems of other animals.

Topics: Animals; Biological Evolution; Cell Communication; Cell Surface Extensions; Cilia; Digestive System; Mesoderm; Nervous System; Nervous System Physiological Phenomena; Nitric Oxide; Porifera; RNA-Seq; Secretory Vesicles; Signal Transduction; Single-Cell Analysis; Transcriptome

PubMed: 34735222
DOI: 10.1126/science.abj2949

Review

Authors: Nicole S Webster, Torsten Thomas

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

Authors: Todd A Anzelon, Saikat Chowdhury, Siobhan M Hughes...

PIWI proteins use PIWI-interacting RNAs (piRNAs) to identify and silence transposable elements and thereby maintain genome integrity between metazoan generations. The targeting of transposable elements by PIWI has been compared to mRNA target recognition by Argonaute proteins, which use microRNA (miRNA) guides, but the extent to which piRNAs resemble miRNAs is not known. Here we present cryo-electron microscopy structures of a PIWI-piRNA complex from the sponge Ephydatia fluviatilis with and without target RNAs, and a biochemical analysis of target recognition. Mirroring Argonaute, PIWI identifies targets using the piRNA seed region. However, PIWI creates a much weaker seed so that stable target association requires further piRNA-target pairing, making piRNAs less promiscuous than miRNAs. Beyond the seed, the structure of PIWI facilitates piRNA-target pairing in a manner that is tolerant of mismatches, leading to long-lived PIWI-piRNA-target interactions that may accumulate on transposable-element transcripts. PIWI ensures targeting fidelity by physically blocking the propagation of piRNA-target interactions in the absence of faithful seed pairing, and by requiring an extended piRNA-target duplex to reach an endonucleolytically active conformation. PIWI proteins thereby minimize off-targeting cellular mRNAs while defending against evolving genomic threats.

Topics: Animals; Argonaute Proteins; Cryoelectron Microscopy; Models, Molecular; Nucleic Acid Conformation; Porifera; RNA, Small Interfering; Substrate Specificity

PubMed: 34471284
DOI: 10.1038/s41586-021-03856-x

Review

Authors: Sally P Leys, Daniel S Rohksar, Bernard M Degnan...

Topics: Animals; Biological Evolution; Genome; Porifera

PubMed: 15723776
DOI: 10.1016/j.cub.2005.02.005

Review

Authors: Hermann Ehrlich, Marcin Wysokowski, Sonia Żółtowska-Aksamitowska...

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

Review

Authors: Taitusi Taufa, Ramesh Subramani, Peter T Northcote...

The islands of the South Pacific Ocean have been in the limelight for natural product biodiscovery, due to their unique and pristine tropical waters and environment. The Kingdom of Tonga is an archipelago in the central Indo-Pacific Ocean, consisting of 176 islands, 36 of which are inhabited, flourishing with a rich diversity of flora and fauna. Many unique natural products with interesting bioactivities have been reported from Indo-Pacific marine sponges and other invertebrate phyla; however, there have not been any reviews published to date specifically regarding natural products from Tongan marine organisms. This review covers both known and new/novel Marine Natural Products (MNPs) and their biological activities reported from organisms collected within Tongan territorial waters up to December 2020, and includes 109 MNPs in total, the majority from the phylum Porifera. The significant biological activity of these metabolites was dominated by cytotoxicity and, by reviewing these natural products, it is apparent that the bulk of the new and interesting biologically active compounds were from organisms collected from one particular island, emphasizing the geographic variability in the chemistry between these organisms collected at different locations.

Topics: Animals; Aquatic Organisms; Biodiversity; Biological Products; Drug Discovery; Pacific Ocean; Porifera; Secondary Metabolism; Tonga; Tropical Climate

PubMed: 34361690
DOI: 10.3390/molecules26154534

Review

Authors: Tadeusz F Molinski

This review discusses the chemistry of cyclic azole-homologated peptides (AHPs) from the marine sponges, Theonella swinhoei, other Theonella species, Calyx spp. and Plakina jamaicensis. The origin, distribution of AHPs and molecular structure elucidations of AHPs are described followed by their biosynthesis, bioactivity, and synthetic efforts towards their total synthesis. Reports of partial and total synthesis of AHPs extend beyond peptide coupling reactions and include creative construction of the non-proteinogenic amino acid components, mainly the homologated heteroaromatic and α-keto-β-amino acids. A useful conclusion is drawn regarding AHPs: despite their rarity, exotic structures and the potent protease inhibitory properties of some members, their synthesis is under-developed and beckons solutions for outstanding problems towards their efficient assembly.

Topics: Animals; Azoles; Molecular Conformation; Peptides; Porifera

PubMed: 29210421
DOI: 10.1039/c7ob02628e

Authors: Nikki Traylor-Knowles, William E Browne, Laura D Mydlarz...

Topics: Animals; Cnidaria; Immunity, Innate; Porifera

PubMed: 35173730
DOI: 10.3389/fimmu.2022.816550

Review

Authors: Casey W Dunn, Sally P Leys, Steven H D Haddock...

Animal evolution is often presented as a march toward complexity, with different living animal groups each representing grades of organization that arose through the progressive acquisition of complex traits. There are now many reasons to reject this classical hypothesis. Not only is it incompatible with recent phylogenetic analyses, but it is also an artifact of 'hidden biology', that is, blind spots to complex traits in non-model species. A new hypothesis of animal evolution, where many complex traits have been repeatedly gained and lost, is emerging. As we discuss here, key details of this new model hinge on a better understanding of the Porifera and Ctenophora, which have each been hypothesized to be sister to all other animals, but are poorly studied and often misrepresented.

Topics: Animals; Biological Evolution; Ctenophora; Phylogeny; Porifera

PubMed: 25840473
DOI: 10.1016/j.tree.2015.03.003

Review

Authors: Valentin A Stonik, Sophia A Kolesnikova

In this review, we discuss structural diversity, taxonomic distribution, biological activities, biogenesis, and synthesis of a rare group of terpenoids, the so-called malabaricane and isomalabaricane triterpenoids, as well as some compounds derived from them. Representatives of these groups were found in some higher and lower terrestrial plants, as well as in some fungi, and in a relatively small group of marine sponges. The skeletal systems of malabaricanes and isomalabaricanes are similar to each other, but differ principally in the stereochemistry of their tricyclic core fragments, consisting of two six-membered and one five-membered rings. Evolution of these triterpenoids provides variety of rearranged, oxidized, and glycoconjugated products. These natural compounds have attracted a lot of attention for their biosynthetic origin and biological activity, especially for their extremely high cytotoxicity against tumor cells as well as promising neuroprotective properties in nanomolar concentrations.

Topics: Animals; Biosynthetic Pathways; Fungi; Glycoconjugates; Plants; Porifera; Triterpenes

PubMed: 34198756
DOI: 10.3390/md19060327