Temperature-dependent carrier state mediated by H-NS promotes the long-term coexistence of Y. pestis and a phage in soil

PLoS Pathog. 2023 Jun 22;19(6):e1011470. doi: 10.1371/journal.ppat.1011470. eCollection 2023 Jun.

Abstract

The study of carrier state phages challenged the canonical lytic-lysogenic binary, and carrier state appears to be ubiquitous and ecologically important. However, the mechanisms of the carrier state are not well elucidated due to the limited phage models. Herein, we reported phage HQ103, similar to Escherichia coli phage P2. In contrast to the temperate P2 phage, the HQ103 phage does not insert its genome into the bacterial chromosome and displays a dual behavior depending on the temperature. At 37°C, HQ103 lyses the host and forms clear plaques due to the truncation of repressor CI and mutation of promoter Pc. In contrast, HQ103 maintains a carrier state lifestyle with Y. pestis at an environmental temperature (21°C). Mechanistically, we found that the host-encoded histone-like nucleoid-structuring protein H-NS, which is highly expressed at 21°C to silence the Cox promoter Pe and inhibits the phage lytic cycle. Subsequently, the HQ103 carrier state Y. pestis could grow and co-exist with the phage in the soil at 21°C for one month. Thus, this study reveals a novel carrier state lifestyle of phage HQ103 due to the H-NS mediated xenogeneic silencing and demonstrates that the carrier state lifestyle could promote long-term phage-host coexist in nature.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteriophages* / genetics
  • Carrier State
  • Lysogeny
  • Soil
  • Temperature
  • Yersinia pestis*

Substances

  • Soil

Grants and funding

This study was supported by the National Natural Science Foundation of China (NSFC) under award number 32260039 (PW), Yunnan Medical leading talent training project under award number L-2019001 (PW), the National Key Research and Development Program of China under award number 2021YFA0911200 (SL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.