New perspectives on bacterial chlorine resistance: Phages encoding chlorine resistance genes improve bacterial adaptation

Abstract

Bacterial resistance to chlorine disinfectant reduces its effectiveness in killing pathogenic bacteria and poses a severe threat to environmental and health safety. The interaction between bacteria and phages is the most frequent biological activity in Earth's biosphere, but little is known about what role and mechanism phages play in the resistance of bacterial communities to chlorine disinfectants. Here, we investigated the changes in the abundance, activity and function of the bacterial-phage community under the effect of chlorine disinfectants in a 92-day running anaerobic-anoxic-oxic system, using metagenomics and metatranscriptomics sequencing. We found that transcriptional activities of both bacteria and phage are highly sensitive to chlorine disinfectants, although their relative abundance was not obviously altered. The increase in both phage diversity and the ratio of temperate to lytic phages’ average activity indicated phages, especially temperate, could play a crucial role in the response to chlorine disinfectants. Interestingly, the phages that carry chlorine resistance genes (CRGs) were the drivers of the phage and microbial community when chlorine disinfectants were present, but they followed the dynamics of community in the absence of chlorine disinfectants. Based on the association bipartite network, we further found that phages directly mediated the horizontal transfer of CRGs among bacteria, facilitating the spread of CRGs in the bacterial community. Moreover, the 4 CRGs related to cell wall repair, redox balance regulation, and efflux pumps that were carried by the phages but lacking in the hosts suggest the potential compensatory effects of the phage for the chlorine resistance of their hosts. Our findings reveal the important role of phages in improving the resistance of bacterial communities to chlorine disinfectants, providing a new perspective on the co-evolution of phages and bacteria to adapt to environments.