Fitness benefits to bacteria of carrying prophages and prophage‐encoded antibiotic‐resistance genes peak in different environments

Abstract

Understanding the role of horizontal gene transfer (HGT) in adaptation is a key challenge in evolutionary biology. In microbes, an important mechanism of HGT is prophage acquisition (phage genomes integrated into bacterial chromosomes). Prophages can influence bacterial fitness via the transfer of beneficial genes (including antibiotic‐resistance genes, ARGs), protection from superinfecting phages, or switching to a lytic lifecycle that releases free phages infectious to competitors. We expect these effects to depend on environmental conditions because of, for example, environment‐dependent induction of the lytic lifecycle. However, it remains unclear how costs/benefits of prophages vary across environments. Here, studying prophages with/without ARGs in Escherichia coli, we disentangled the effects of prophages alone and adaptive genes they carry. In competition with prophage‐free strains, benefits from prophages and ARGs peaked in different environments. Prophages were most beneficial when induction of the lytic lifecycle was common, whereas ARGs were more beneficial upon antibiotic exposure and with reduced prophage induction. Acquisition of prophage‐encoded ARGs by competing strains was most common when prophage induction, and therefore free phages, were common. Thus, selection on prophages and adaptive genes they carry varies independently across environments, which is important for predicting the spread of mobile/integrating genetic elements and their role in evolution.

Comprehensive in silico survey of the Mycolicibacterium mobilome reveals an as yet underexplored diversity

“…Among the antibiotic resistance genes analysed, 73 (~30 %) were associated with antibiotic inactivation (most of them related to beta-lactams and aminoglycosides), of which 22 presented functional domains listed in the ResFams database (Table S14, genes marked in red). Thus, they can also play a role as a reservoir, with a further impact on their host’s fitness [93, 112, 113]. The exception was the cryptic Mycolicibacterium goodii X7B prophage encoding an arr gene with high similarity (92 % identity) to a functional gene of M.…”

Conjugative plasmid transfer is limited by prophages but can be overcome by high conjugation rates

“…Estimating fitness cost of plasmid carriage: To better parameterize our model, we determined fitness costs associated with plasmid carriage using pairwise competition assays as described in [10].…”

“…There were no significant fitness costs for recipients for carrying the fluorescent and the chloramphenicol marker (Figure S5), nor when recipients acquired the plasmid (Figure S5) or the prophage [10].…”

“…This switch happens either spontaneously (at low rates) or in response to stressful conditions (at high rates). Released phages can then kill competing cells that are susceptible to these phages because they are not carrying the respective prophage, which usually confers protection against superinfection [10, 11].…”

The Age of Phage: Friend or Foe in the New Dawn of Therapeutic and Biocontrol Applications?

“…It is important to note that transduction would be an inconsequential process if it did not provide benefits to both bacteria and bacteriophages. Observations of the competitive advantages which lysogens have over prophage-lacking competitors supports the notion that the presence of prophages may function as a mutualistic trait [111,112]. Once considered as bacterial parasites which silently persist within bacteria, prophages are now understood to have a symbiotic relationship with their bacterial hosts [113].…”