Ultrastructural evidence for nutritional relationships between a marine colonial invertebrate (Bryozoa) and its bacterial symbionts

Karagodina, N. P.; Vishnyakov, Andrey E.; Kotenko, Olga N.; Maltseva, Arina L.; Ostrovsky, Andrew N.

doi:10.1007/s13199-017-0516-1

Cited by 16 publications

(23 citation statements)

References 51 publications

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“…Zooidal budding then results in colony formation and the spread of the symbionts through it. Occupying the transport funicular system and utilizing the nutrients from it, the symbionts multiply, triggering the formation of the funicular bodies that was recently shown in another cheilostome bryozoan 62 . Bacteria partly stay in these bodies and partly move to the ooecial vesicle of the brood chamber by an unknown mechanism.…”

Section: Discussionmentioning

confidence: 89%

“…Although viruses were never reported from bryozoans before, symbiotic associations with bacteria are known in species from several families of the order Cheilostomata, the largest bryozoan group (e.g. 55 – 61 , reviewed in 62 ). The symbionts are reportedly vertically transmitted via the larval stage ( 63 – 69 and references therein).…”

Section: Introductionmentioning

confidence: 99%

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

Vishnyakov

Karagodina

Lim-Fong

et al. 2021

Sci Rep

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Bacteriophage communities associated with humans and vertebrate animals have been extensively studied, but the data on phages living in invertebrates remain scarce. In fact, they have never been reported for most animal phyla. Our ultrastructural study showed for the first time a variety of virus-like particles (VLPs) and supposed virus-related structures inside symbiotic bacteria in two marine species from the phylum Bryozoa, the cheilostomes Bugula neritina and Paralicornia sinuosa. We also documented the effect of VLPs on bacterial hosts: we explain different bacterial ‘ultrastructural types’ detected in bryozoan tissues as stages in the gradual destruction of prokaryotic cells caused by viral multiplication during the lytic cycle. We speculate that viruses destroying bacteria regulate symbiont numbers in the bryozoan hosts, a phenomenon known in some insects. We develop two hypotheses explaining exo- and endogenous circulation of the viruses during the life-cycle of B. neritina. Finally, we compare unusual ‘sea-urchin’-like structures found in the collapsed bacteria in P. sinuosa with so-called metamorphosis associated contractile structures (MACs) formed in the cells of the marine bacterium Pseudoalteromonas luteoviolacea which are known to trigger larval metamorphosis in a polychaete worm.

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Section: Discussionmentioning

confidence: 89%

“…Although viruses were never reported from bryozoans before, symbiotic associations with bacteria are known in species from several families of the order Cheilostomata, the largest bryozoan group (e.g. 55 – 61 , reviewed in 62 ). The symbionts are reportedly vertically transmitted via the larval stage ( 63 – 69 and references therein).…”

Section: Introductionmentioning

confidence: 99%

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

Vishnyakov

Karagodina

Lim-Fong

et al. 2021

Sci Rep

Self Cite

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“…Zooidal budding then results in colony formation and the spread of the symbionts through it. Occupying the transport funicular system and utilizing the nutrients from it, the symbionts multiply, triggering the formation of the funicular bodies (Karagodina et al 2018). Bacteria partly stay in these bodies and partly move to the ooecial vesicle of the brood chamber by an unknown mechanism.…”

Section: Discussionmentioning

confidence: 99%

“…Although viruses were never reported from bryozoans before, symbiotic associations with bacteria are known in species from several families of the order Cheilostomata, the largest bryozoan group (e.g. Lutaud 1965, 1969, 1986; Woollacott & Zimmer 1975; Dyrynda & King 1982; Moosbrugger et al 2012; Mathew et al 2018, reviewed in Karagodina et al 2018). The symbionts are vertically transmitted via the larval stage (Woollacott 1981; Zimmer & Woollacott 1983, 1989; Boyle et al 1987; Lim & Haygood 2004; Sharp et al 2007a; Lim-Fong et al 2008, and references therein).…”

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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“…These strands emanate from the peritoneal lining of the gut and run to pore‐cell complexes of the communication pores in the interzooidal walls or to the lateral funicular strands in the vicinity of the body wall. In some species the funicular tissue contains bacterial symbionts in so‐called ‘funicular bodies’ (Lutaud, ; Mathew et al ., ; Shunatova & Tamberg, ; Karagodina et al ., ).…”

Section: Character Evolutionmentioning

confidence: 97%

Key novelties in the evolution of the aquatic colonial phylum Bryozoa: evidence from soft body morphology

2020

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Molecular techniques are currently the leading tools for reconstructing phylogenetic relationships, but our understanding of ancestral, plesiomorphic and apomorphic characters requires the study of the morphology of extant forms for testing these phylogenies and for reconstructing character evolution. This review highlights the potential of soft body morphology for inferring the evolution and phylogeny of the lophotrochozoan phylum Bryozoa. This colonial taxon comprises aquatic coelomate filter-feeders that dominate many benthic communities, both marine and freshwater. Despite having a similar bauplan, bryozoans are morphologically highly diverse and are represented by three major taxa: Phylactolaemata, Stenolaemata and Gymnolaemata. Recent molecular studies resulted in a comprehensive phylogenetic tree with the Phylactolaemata sister to the remaining two taxa, and Stenolaemata (Cyclostomata) sister to Gymnolaemata. We plotted data of soft tissue morphology onto this phylogeny in order to gain further insights into the origin of morphological novelties and character evolution in the phylum. All three larger clades have morphological apomorphies assignable to the latest molecular phylogeny. Stenolaemata (Cyclostomata) and Gymnolaemata were united as monophyletic Myolaemata because of the apomorphic myoepithelial and triradiate pharynx. One of the main evolutionary changes in bryozoans is a change from a body wall with two well-developed muscular layers and numerous retractor muscles in Phylactolaemata to a body wall with few specialized muscles and few retractors in the remaining bryozoans. Such a shift probably pre-dated a body wall calcification that evolved independently at least twice in Bryozoa and resulted in the evolution of various hydrostatic mechanisms for polypide protrusion. In Cyclostomata, body wall calcification was accompanied by a unique detachment of the peritoneum from the epidermis to form the hydrostatic membraneous sac. The digestive tract of the Myolaemata differs from the phylactolaemate condition by a distinct ciliated pylorus not present in phylactolaemates. All bryozoans have a mesodermal funiculus, which is duplicated in Gymnolaemata. A colonial system of integration (CSI) of additional, sometimes branching, funicular cords connecting neighbouring zooids via pores with pore-cell complexes evolved at least twice in Gymnolaemata. The nervous system in all bryozoans is subepithelial and concentrated at the lophophoral base and the tentacles. Tentacular nerves emerge intertentacularly in Phylactolaemata whereas they partially emanate directly from the cerebral ganglion or the circum-oral nerve ring in myolaemates. Overall, morphological evidence shows that ancestral forms were small, colonial coelomates with a muscular body wall and a U-shaped gut with ciliary tentacle crown, and were capable of asexual budding. Coloniality resulted in many novelties including the origin of zooidal polymorphism, an apomorphic landmark trait of the Myolaemata.Biological Reviews 95 (2020) 696-729

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Ultrastructural evidence for nutritional relationships between a marine colonial invertebrate (Bryozoa) and its bacterial symbionts

Cited by 16 publications

References 51 publications

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

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

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

Key novelties in the evolution of the aquatic colonial phylum Bryozoa: evidence from soft body morphology

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