Lysogenic bacteriophages encoding arsenic resistance determinants promote bacterial community adaptation to arsenic toxicity

Abstract Emerging evidence from genomics gives us a glimpse into the potential contribution of lysogenic bacteriophages (phages) to the environmental adaptability of their hosts. However, it is challenging to quantify this kind of contribution due to the lack of appropriate genetic markers and the associated controllable environmental factors. Here, based on the unique transformable nature of arsenic (the controllable environmental factor), a series of flooding microcosms was established to investigate the contribution of arsM-bearing lysogenic phages to their hosts’ adaptation to trivalent arsenic [As(III)] toxicity, where arsM is the marker gene associated with microbial As(III) detoxification. In the 15-day flooding period, the concentration of As(III) was significantly increased, and this elevated As(III) toxicity visibly inhibited the bacterial population, but the latter quickly adapted to As(III) toxicity. During the flooding period, some lysogenic phages re-infected new hosts after an early burst, while others persistently followed the productive cycle (i.e., lytic cycle). The unique phage-host interplay contributed to the rapid spread of arsM among soil microbiota, enabling the quick recovery of the bacterial community. Moreover, the higher abundance of arsM imparted a greater arsenic methylation capability to soil microbiota. Collectively, this study provides experimental evidence for lysogenic phages assisting their hosts in adapting to an extreme environment, which highlights the ecological perspectives on lysogenic phage-host mutualism.