Morphological characterization of virus-like particles in coral reef sponges

Pascelli, Cecília; Laffy, Patrick W.; Kupresanin, Marija; Ravasi, Timothy; Webster, Nicole S.

doi:10.7717/peerj.5625

Cited by 31 publications

(32 citation statements)

References 80 publications

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“…The partnership between sponges and their microbial and viral associates represents one of the most ancient examples of interkingdom symbiosis in multicellular life (Hentschel et al ., ). While the sponge microbiome has been intensively studied and reviewed numerous times (Taylor et al ., ; Taylor et al ., ; Webster and Blackall, ; Hentschel et al ., ; Webster and Taylor, ; Webster and Thomas, ; Pita et al ., ), the composition and function of the virome has only recently been elucidated (Laffy et al ., ; Laffy et al ., ; Pascelli et al ., ). Consistent with patterns in the microbiome, the sponge viral community is diverse and host‐species specific, being characterized by an abundance of the dsDNA order Caudovirales , ssDNA family Microviridae and representatives of the Megavirales including the Mimiviridae , Phycodnaviridae and Poxviridae families (Laffy et al ., ; Laffy et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Thermal stress modifies the marine sponge virome

Laffy

Botté

Wood‐Charlson

et al. 2019

Environ Microbiol Rep

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Summary Marine sponges can form stable partnerships with a wide diversity of microbes and viruses, and this high intraspecies symbiont specificity makes them ideal models for exploring how host‐associated viromes respond to changing environmental conditions. Here we exposed the abundant Great Barrier Reef sponge Rhopaloiedes odorabile to elevated seawater temperature for 48 h and utilised a metaviromic approach to assess the response of the associated viral community. An increase in endogenous retro‐transcribing viruses within the Caulimorviridae and Retroviridae families was detected within the first 12 h of exposure to 32 °C, and a 30‐fold increase in retro‐transcribing viruses was evident after 48 h at 32 °C. Thermally stressed sponges also exhibited a complete loss of ssDNA viruses which were prevalent in field samples and sponges from the control temperature treatment. Despite these viromic changes, functional analysis failed to detect any loss or gain of auxiliary metabolic genes, indicating that viral communities are not providing a direct competitive advantage to their host under thermal stress. In contrast, endogenous sponge retro‐transcribing viruses appear to be replicating under thermal stress, and consistent with retroviral infections in other organisms, may be contributing to the previously described rapid decline in host health evident at elevated temperature.

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Section: Introductionmentioning

confidence: 97%

Thermal stress modifies the marine sponge virome

Laffy

Botté

Wood‐Charlson

et al. 2019

Environ Microbiol Rep

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“…Middelboe & Brussaard 2017). Indeed, by filtering enormous volumes of water, sea sponges acquire viruses that infect their cells (Vacelet & Gallissian 1978; Luter et al 2010; Pascelli et al 2018) as well as their bacterial symbionts (Lohr et al 2005). Corals, together with their eukaryotic and prokaryotic symbionts, harbor a variety of viruses too (e.g.…”

Section: Introductionmentioning

confidence: 99%

First evidence of virus-like particles in the bacterial symbionts of Bryozoa

Vishnyakov

Karagodina

Lim-Fong

et al. 2020

Preprint

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23Bacteriophage communities associated with humans and vertebrate animals have been 24 extensively studied, but the data on phages living in invertebrates remain scarce. In 25 fact, they have never been reported for most animal phyla. Our ultrastructural study 26 2 showed for the first time a variety of virus-like particles (VLPs) and supposed virus-27 related structures inside symbiotic bacteria in two marine species from the phylum 28 Bryozoa, the cheilostomes Bugula neritina and Paralicornia sinuosa. We also 29 documented the effect of VLPs on bacterial hosts: we explain different bacterial 30 'ultrastructural types' detected in bryozoan tissues as stages in the gradual destruction 31 of prokaryotic cells caused by viral multiplication during the lytic cycle. We speculate 32 that viruses destroying bacteria regulate symbiont numbers in the bryozoan hosts, a 33 phenomenon known in some insects. We develop two hypotheses explaining exo-and 34 endogenous circulation of the viruses during the life-cycle of B. neritina. Finally, we 35 compare unusual 'sea-urchin'-like structures found in the collapsed bacteria in P. 36 sinuosa with so-called metamorphosis associated complexes (MACs) known to trigger 37 larval metamorphosis in a polychaete worm. 38 39 Importance 40 Complex symbiotic systems, including metazoan hosts, their bacterial symbionts and 41 bacteriophages are widely studied using vertebrate models whereas much less is 42 known about invertebrates. Our ultrastructural research revealed replication of the 43 viruses and/or activation of virus related elements in the bacterial symbionts inhabiting 44 tissues of the marine colonial invertebrates (phylum Bryozoa). The virus activity in the 45 bacterial cells that are believed to be transmitted exclusively vertically is of a special 46 importance. In addition, in the bacterial symbionts of one of the bryozoan hosts we 47 observed the massive replication of the structures seemingly related to the 48 Metamorphosis associated complexes (MAC). To our knowledge, MACs were never 49 reported in the animal prokaryotic symbionts. Our findings indicate that Bryozoa may be 50 new suitable model to study the role of bacteriophages and phage-related structures in 51 the complex symbiotic systems hosted by marine invertebrates.52 3In the marine realm, the large variety of viruses are found across diverse taxa, 78 including protists and various invertebrates such as sponges, cnidarians, flatworms, 79 polychaetes, mollusks, crustaceans and echinoderms (reviewed in Johnson

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“…Electron microscopic studies have identified phage-like particles associated with Lamellodysidea sponge samples [57], but these have not yet been characterized by sequence analysis. In this study, viral scaffold candidates detected by VirSorter [58] in assembled holobiont metagenomes were dominated by GenBank matches to double stranded DNA tailed bacteriophage (Caudovirales) of the Siphoviridae, Myoviridae, and Podoviridae lineages ( Supplementary Figure 9, Additional file 1).…”

Section: Viral Sequences and Phage Defensementioning

confidence: 99%

A genomic view of trophic and metabolic diversity in clade-specific Lamellodysidea sponge microbiomes

Podell

Blanton

Oliver

et al. 2019

Preprint

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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 structures aligned with sponge host subgroup phylogeny in 16 samples from four host clades collected from multiple sites in Guam over a three 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 chemically talented genus Prochloron, a common tunicate symbiont. Two novel Alphaprotobacteria 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.

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Morphological characterization of virus-like particles in coral reef sponges

Cited by 31 publications

References 80 publications

Thermal stress modifies the marine sponge virome

Thermal stress modifies the marine sponge virome

First evidence of virus-like particles in the bacterial symbionts of Bryozoa

A genomic view of trophic and metabolic diversity in clade-specific Lamellodysidea sponge microbiomes

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