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

A.E. Vishnyakov, N.P. Karagodina, G. Lim-Fong, P.A. Ivanov, T.F. Schwaha, A.V. Letarov, A.N. Ostrovsky
doi: https://doi.org/10.1101/2020.04.16.045880
A.E. Vishnyakov
1Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaja nab. 7/9, 199034, Saint Petersburg, Russia
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N.P. Karagodina
1Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaja nab. 7/9, 199034, Saint Petersburg, Russia
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G. Lim-Fong
2Department of Biology, Randolph-Macon College, 304 Caroline Street, Ashland, Virginia, USA
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P.A. Ivanov
3Winogradsky Institute of Microbiology, Research Centre of Biotechnology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7 bld. 2, 117312 Moscow, Russia
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T.F. Schwaha
4Department of Evolutionary Biology, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria
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A.V. Letarov
3Winogradsky Institute of Microbiology, Research Centre of Biotechnology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7 bld. 2, 117312 Moscow, Russia
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  • For correspondence: a.ostrovsky@spbu.ru letarov@gmail.com
A.N. Ostrovsky
1Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaja nab. 7/9, 199034, Saint Petersburg, Russia
5Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, Geozentrum, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria
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  • For correspondence: a.ostrovsky@spbu.ru letarov@gmail.com
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ABSTRACT

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 complexes (MACs) known to trigger larval metamorphosis in a polychaete worm.

Importance Complex symbiotic systems, including metazoan hosts, their bacterial symbionts and bacteriophages are widely studied using vertebrate models whereas much less is known about invertebrates. Our ultrastructural research revealed replication of the viruses and/or activation of virus related elements in the bacterial symbionts inhabiting tissues of the marine colonial invertebrates (phylum Bryozoa). The virus activity in the bacterial cells that are believed to be transmitted exclusively vertically is of a special importance. In addition, in the bacterial symbionts of one of the bryozoan hosts we observed the massive replication of the structures seemingly related to the Metamorphosis associated complexes (MAC). To our knowledge, MACs were never reported in the animal prokaryotic symbionts. Our findings indicate that Bryozoa may be new suitable model to study the role of bacteriophages and phage-related structures in the complex symbiotic systems hosted by marine invertebrates.

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Posted April 18, 2020.
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First evidence of virus-like particles in the bacterial symbionts of Bryozoa
A.E. Vishnyakov, N.P. Karagodina, G. Lim-Fong, P.A. Ivanov, T.F. Schwaha, A.V. Letarov, A.N. Ostrovsky
bioRxiv 2020.04.16.045880; doi: https://doi.org/10.1101/2020.04.16.045880
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First evidence of virus-like particles in the bacterial symbionts of Bryozoa
A.E. Vishnyakov, N.P. Karagodina, G. Lim-Fong, P.A. Ivanov, T.F. Schwaha, A.V. Letarov, A.N. Ostrovsky
bioRxiv 2020.04.16.045880; doi: https://doi.org/10.1101/2020.04.16.045880

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