Mining of Thousands of Prokaryotic Genomes Reveals High Abundance of Prophages with a Strictly Narrow Host Range

Abstract

Phages and prophages are one of the principal modulators of microbial populations. However, much of their diversity is still poorly understood. Here, we extracted 33,624 prophages from 13,713 complete prokaryotic genomes to explore the prophage diversity and their relationships with their host. Our results reveal that prophages were present in 75% of the genomes studied. In addition, Enterobacterales were significantly enriched in prophages. We also found that pathogens are a significant reservoir of prophages. Finally, we determined that the prophage relatedness and the range of genomic hosts were delimited by the evolutionary relationships of their hosts. On a broader level, we got insights into the prophage population, identified in thousands of publicly available prokaryotic genomes, by comparing the prophage distribution and relatedness between them and their hosts. IMPORTANCE Phages and prophages play an essential role in controlling their host populations either by modulating the host abundance or providing them with genes that benefit the host. The constant growth in next-generation sequencing technology has caused the development of powerful computational tools to identify phages and prophages with high precision. Making it possible to explore the prophage populations integrated into host genomes on a large scale. However, it is still a new and under-explored area, and efforts are still required to identify prophage populations to understand their dynamics with their hosts.

Keywords: archaea; bacteria; bacteriophages; eubacteria; prophages; viral diversity.

FIG 1

Distribution of the number of prophages (A) and the average of prophages (B) per host genome based on the genome size (Mb). The total number of prophages (green line) and prophages ≥30 Kb (brown line) are shown in each plot.

FIG 2

Bacteria and Archaea prophage distribution. The phylogenetic tree was generated using Lifemap at order level. The phyla are shown in different colors. The Archaea and Bacteria branches are shown in dashed and solid lines, respectively.

FIG 3

Boxplots of P-values for different genera. P-values were calculated by collecting and bootstrapping (100 times randomly) the number of prophages in 10 genomes for each genus, using the Wilcoxon test (see methods). The blue dotted line indicates the significant Wilcoxon tests (p <0.05). The boxplots are colored with respect to the Order taxonomic level.

FIG 4

(A) Prophage network generated with prophages with ≥80 AAI (2,485 prophages), visualization produced with Cytoscape (see methods). Nodes represent prophages and edges represent their weighted pairwise similarities of AAI. Nodes (prophages) are depicted with different colors according to their phylum host. (B) Prophage fraction which shared an AAI value ≥80 between prophages of different lysogens at all taxonomic levels.