Single-stranded DNA phages: from early molecular biology tools to recent revolutions in environmental microbiology

Abstract

Single-stranded DNA (ssDNA) phages are profoundly different from tailed phages in many aspects including the nature and size of their genome, virion size and morphology, mutation rate, involvement in horizontal gene transfer, infection dynamics and cell lysis mechanisms. Despite the importance of ssDNA phages as molecular biology tools and model systems, the environmental distribution and ecological roles of these phages have been largely unexplored. Viral metagenomics and other culture-independent viral diversity studies have recently challenged the perspective of tailed, double-stranded DNA (dsDNA) phages, dominance by demonstrating the prevalence of ssDNA phages in diverse habitats. However, the differences between ssDNA and dsDNA phages also substantially limit the efficacy of simultaneously assessing the abundance and diversity of these two phage groups. Here we provide an overview of the major differences between ssDNA and tailed dsDNA phages that may influence their effects on bacterial communities. Furthermore, through the analysis of 181 published metaviromes we demonstrate the environmental distribution of ssDNA phages and present an analysis of the methodological biases that distort their study through metagenomics.

Reef invertebrate viromics: diversity, host specificity and functional capacity

“…Members of the Microviridae have also been identified in the human gut, where they are responsible for increased variability in comparison to temperate phages (Minot et al ., ). The abundance of this viral family shown here and also recently reported in global ocean surveys (Labonté and Suttle, ; Székely and Breitbart, ) highlights the ubiquity and importance of Microviridae in marine environments.…”

“…Members of the Microviridae have also been identified in the human gut, where they are responsible for increased variability in comparison to temperate phages (Minot et al, 2013). The abundance of this viral family shown here and also recently reported in global ocean surveys (Labont e and Suttle, 2013; Sz ekely and Breitbart, 2016) highlights the ubiquity and importance of Microviridae in marine environments. Representatives from the Megavirales family Ascoviridae, Iridoviridae, Poxviridae and Marseilleviridae (Colson et al, 2013) were observed in individual replicates across multiple species (Fig.…”

Virus taxonomy in the age of metagenomics

“…A recent comprehensive metagenomic analysis of thousands of diverse samples has led to the discovery of approximately 125,000 new viral genomes and a 16-fold increase in the number of identified viral genes 24 . Similarly, as technology advances, it is becoming clear that ssDNA and RNA viruses in marine and other ecosystems are far more diverse than currently characterized viruses; however, these new viruses remain understudied despite their ecological importance 11,[25][26][27][28][29][30][31] . Many ssDNA viruses identified in metagenomic data encode an evolutionarily conserved replication-associated protein (Rep), whereas the number, orientation and evolutionary origin of other genes are highly variable in these circular Rep-encoding ssDNA viruses (CRESS-DNA viruses) 32 .…”

Viral coinfection is shaped by host ecology and virus–virus interactions across diverse microbial taxa and environments

“…Thus, enhanced coinfection, perhaps due to the long, persistent infection cycles of some ssDNA viruses, particularly the Inoviridae (Rakonjac et al 2011), might be a major factor explaining findings of phages with chimeric genomes composed of different types of nucleic acids (Diemer and Stedman 2012; Roux et al 2013). Filamentous or rod-shaped ssDNA phages (family Inoviridae; Székely and Breitbart 2016) often conduct multiple replications without killing their bacterial hosts (Rakonjac et al 2011; Mai-Prochnow et al 2015; Székely and Breitbart 2016), allowing more time for other viruses to coinfect the cell and providing a potential mechanistic basis for the enhanced dsDNA–ssDNA coinfections. In line with this prediction, over 96% of dsDNA–ssDNA host culture coinfections contained at least one virus from the Inoviridae , a greater (and statistically distinguishable) percentage than contained in ssDNA-only coinfections or ssDNA single infections.…”