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

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 contractile structures (MACs) formed in the cells of the marine bacterium Pseudoalteromonas luteoviolacea which are known to trigger larval metamorphosis in a polychaete worm.

Seasonal dynamics of a complex cheilostome bryozoan symbiosis: vertical transfer challenged

“…In the latter case, FBs are considered to be modified expanded parts of the funicular system. This is consistent with experiments by Sharp and co-authors 40 , who detected groups of labeled bacteria in the funicular cords of Bugula neritina , and also multiple bacteria developing inside enlarged funicular cords (in fact, very large FBs) in the related Paralicornia sinuosa 20 .…”

“…FBs with symbiotic bacteria have been found in several bryozoan species from four different families 20 , 25 , 47 , 49 , 51 (our data). Remarkably, all these families (Bugulidae, Beaniidae, Candidae, Epistomiidae) belong to the clade Buguloidea.…”

“…The marine realm encompasses a plethora of symbiotic associations between various protists 8 , 9 , metazoans 10 – 12 , metazoans and protists 13 , 14 , protists and prokaryotes 15 , 16 , and metazoans and procaryotes 17 – 19 . Some symbioses also involve viruses 20 . While certain associations (e.g., corals-zooxanthellae, sponges-bacteria) became model study objects 21 – 24 , most symbiotic relationships still await exploration.…”

“…In species of four bryozoan families (Bugulidae, Candidae, Beaniidae, Epistomiidae), the bacteria are located inside the so-called funicular bodies (abbreviated as FBs here and elsewhere)—‘capsules’ that have a wall of somatic cells associated with the funicular cords 20 , 25 , 47 , 49 , 51 . It was suggested that these structures serve as sites for incubation and multiplication of bacteria 25 , which can later move to the funicular cords and travel inside them towards incubation chambers containing a larva, thereby corroborating the idea of their vertical transfer 47 .…”

“…It was suggested that these structures serve as sites for incubation and multiplication of bacteria 25 , which can later move to the funicular cords and travel inside them towards incubation chambers containing a larva, thereby corroborating the idea of their vertical transfer 47 . In addition, collapsing bacteria and a variety of virus-like particles were recently detected in the funicular bodies of two bryozoan species 20 .…”