Abstract
Species of the genus Shewanella are widespread in nature in various habitats, however, little is known about phages affecting Shewanella sp. Here, we report the isolation of phages from diverse freshwater environments that infect and lyse strains of Shewanella oneidensis and other Shewanella sp. Sequence analysis and microscopic imaging strongly indicate that these phages form a so far unclassified genus, now named Shewanella phage Thanatos, which can be positioned within the subfamily of Tevenvirinae (Duplodnaviria; Heunggongvirae; Uroviricota; Caudoviricetes; Caudovirales; Myoviridae; Tevenvirinae). We characterized one member of this group in more detail using S. oneidensis MR-1 as a host. Shewanella phage Thanatos-1 possesses a prolate icosahedral capsule of about 110 nm in height and 70 nm in width and a tail of about 95 nm in length. The dsDNA genome exhibits a GC content of about 34.5%, has a size of 160.6 kbp and encodes about 206 proteins (92 with an annotated putative function) and two tRNAs. Out of those 206, MS analyses identified about 155 phage proteins in PEG-precipitated samples of infected cells. Phage attachment likely requires the outer lipopolysaccharide of S. oneidensis, narrowing the phage’s host range. Under the applied conditions, about 20 novel phage particles per cell were produced after a latent period of approximately 40 min, which are stable at a pH range from 4 to 12 and resist temperatures up to 55°C for at least 24 h. Addition of Thanatos to S. oneidensis results in partial dissolution of established biofilms, however, early exposure of planktonic cells to Thanatos significantly enhances biofilm formation. Taken together, we identified a novel genus of Myophages affecting S. oneidensis communities in different ways.
Highlights
Viruses that prey on prokaryotic organisms, archaea and bacteria, are amazingly abundant in nature
Under the conditions tested, all phage tails exhibited this appearance and length, which may suggest that all phage particles that were imaged under these conditions had an already contracted tail
We have aimed at further exploring phages preying on species of the highly widespread genus Shewanella, and here we describe the isolation of two phages, Shewanella phages Thanatos-1 and Thanatos-2, infecting and lysing S. oneidensis
Summary
Viruses that prey on prokaryotic organisms, archaea and bacteria, are amazingly abundant in nature. The number of viruses that infect bacteria, which are commonly referred to as bacteriophages or phages, is estimated to surpass that of their host cells by far in most environments (Clokie et al, 2011; Wigington et al, 2016; Parikka et al, 2017). Lysogenic phages may not immediately kill and lyse their host, but their genome is maintained in the host cell either integrated into that of the host or maintained as independent replicative units These phages may proliferate as prophages along with their host cells for many generations before being triggered into the lytic cycle, e.g., by environmental or intracellular signals. The examples illustrate that, being studied for more than 100 years, many aspects of phages and their interactions with their hosts are not understood and are yet to be discovered
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