Identification and characterization of thousands of bacteriophage satellites across bacteria

Abstract

Bacteriophage–bacteria interactions are affected by phage satellites, elements that exploit phages for transfer between bacteria. Satellites can encode defense systems, antibiotic resistance genes, and virulence factors, but their number and diversity are unknown. We developed SatelliteFinder to identify satellites in bacterial genomes, detecting the four best described families: P4-like, phage inducible chromosomal islands (PICI), capsid-forming PICI, and PICI-like elements (PLE). We vastly expanded the number of described elements to ∼5000, finding bacterial genomes with up to three different families of satellites. Most satellites were found in Proteobacteria and Firmicutes, but some are in novel taxa such as Actinobacteria. We characterized the gene repertoires of satellites, which are variable in size and composition, and their genomic organization, which is very conserved. Phylogenies of core genes in PICI and cfPICI indicate independent evolution of their hijacking modules. There are few other homologous core genes between other families of satellites, and even fewer homologous to phages. Hence, phage satellites are ancient, diverse, and probably evolved multiple times independently. Given the many bacteria infected by phages that still lack known satellites, and the recent proposals for novel families, we speculate that we are at the beginning of the discovery of massive numbers and types of satellites.

The defense island repertoire of the Escherichia coli pan-genome

“…Phage satellites were detected using SatelliteFinder (Galaxy Version 0.9) [56] analysis of the amino acid sequences of genes in each island. P4-like satellites were only considered if they were predicted to be of types A, B or C, and PICI satellites if predicted to be of types A or B, per the definitions in ref.…”

“…P4-like satellites were only considered if they were predicted to be of types A, B or C, and PICI satellites if predicted to be of types A or B, per the definitions in ref. [56]. Manual inspection of islands annotated to contain PICI satellites revealed several of these to be intact Uetakevirus prophages; the annotation was changed accordingly.…”

Nuclease genes occupy boundaries of genetic exchange between bacteriophages

“…Similar to the recently described cfPICIs (64), these satellites appear to encode genes required for capsid morphogenesis, such as major capsid proteins and decoration proteins. Nevertheless, these satellites lacked many of the other signature genes of the cfPICI group such as terminase genes, a prohead serine protease, an alpA homolog, head-tail adapter genes, and a Pri-Rep replication initiator (64). The new satellites also encode putative tape measure proteins and a predicted component of the phage-tail baseplate but lack the majority of genes required for tail morphogenesis.…”

“…These putative satellites encode a similar suite of predicted proteins, are flanked by attachment sites, and lack the full suite of genes for autonomous phage progeny production, suggestive of satellite function (Figure 8C). Similar to the recently described cfPICIs (64), these satellites appear to encode genes required for capsid morphogenesis, such as major capsid proteins and decoration proteins. Nevertheless, these satellites lacked many of the other signature genes of the cfPICI group such as terminase genes, a prohead serine protease, an alpA homolog, head-tail adapter genes, and a Pri-Rep replication initiator (64).…”

Polinton-like Viruses Associated with Entomopoxviruses Provide Insight into Replicon Evolution

“…parasites of other parasites, that rely on host or ‘helper’ viruses for their own propagation and spread (Gnanasekaran and Chakraborty 2018). Viral satellites are found throughout the tree of life, associating with viruses that infect each domain (de Sousa et al 2023; Ren et al 2013; Barreat and Katzourakis 2023). Within eukaryotes, satellites have been described in diverse hosts, including humans (Taylor 2012; Meier et al 2020), bees (Olivier et al 2008), yeast (Vepštaitė-Monstavičė et al 2018), amoebae (La Scola et al 2008), algae (Santini et al 2013), and many plant species (Fritsch and Mayo 2018).…”