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. 2025 Aug 5;13(8):e0227124.
doi: 10.1128/spectrum.02271-24. Epub 2025 Jun 23.

Frenemy: adaptive temperate phage_SAP_1432 supports Staphylococcus aureus survival in changing temperatures

Affiliations

Frenemy: adaptive temperate phage_SAP_1432 supports Staphylococcus aureus survival in changing temperatures

Ting-Ting Liu et al. Microbiol Spectr. .

Abstract

It is important to understand how the presence of pathogens could benefit the survival of their hosts during climate change. In this study, we investigated the influence of the heat-resistant temperate phage phage_SAP_1432 on its bacterial host Staphylococcus aureus Q1432 at different temperatures. Thermal host performance curves at a multiplicity of infection of 0.001 showed that the phage killed the bacterium efficiently from 20 to 39°C and from 47 to 50°C. However, the phage resulted in a 41.2% increase in the maximal growth rate for the host bacterium from 1.53 (95% confidence interval [CI]: 1.42-1.63) in the absence of phage_SAP_1432 to 2.16 (95% CI: 2.02-2.37) in its presence, along with a shift in the optimum temperature from 41.0°C to 44.1°C. In the absence of phage, the maximum survival temperature of S. aureus Q1432 was 51°C, but after co-culture with phage_SAP_1432, a few bacteria survived at 55°C-80°C. Lysogenesis occurred more easily at lower temperatures; the percentage of lysogenesis increased with phage concentration, while the maximum growth rate of the host decreased. Our findings provide new evidence that heat-resistant temperate phages can benefit the survival of their bacterial host at specific temperatures, giving a new perspective on the effects of co-evolution of heat-resistant temperate phages and bacterial hosts in an era of global climate change.

Importance: Understanding pathogen-host interactions is crucial for predicting climate change impacts on microbial ecosystems. This study examined the heat-resistant temperate phage_SAP_1432 and its effects on Staphylococcus aureus Q1432 at various temperatures. Phage_SAP_1432 enhanced the thermal performance and survival at high temperatures of its host at a low MOI. This mutual benefit demonstrates the adaptive advantages phages provide in changing thermal environments. As global temperatures rise, such phage-host interactions may play a critical role in microbial survival and evolution. Our research highlights the potential for phages to act as allies, offering a new perspective on the co-evolution of heat-resistant temperate phages and their bacterial hosts.

Keywords: Staphylococcus aureus; heat-resistant temperate phage; lysogeny; temperature; thermal performance curve.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig 1
Fig 1
One-step curve of phage_SAP_1432.
Fig 2
Fig 2
Thermal stability of phage_SAP_1432.
Fig 3
Fig 3
pH stability of phage_SAP_1432.
Fig 4
Fig 4
TPCs of S aureus Q1432 in the absence of phage and in the presence of phage_SAP_1432 with different MOIs.
Fig 5
Fig 5
Prediction of optimum growth temperature of S. aureus Q1432 in the presence of phage_SAP_1432 at different MOIs and in the absence of phage (data labeled “bacteria”).
Fig 6
Fig 6
Prediction of activation and deactivation energy ranges of S. aureus Q1432 in the presence of phage_SAP_1432 at different MOIs and in the absence of phage (data labeled “bacteria”). (A) Prediction of activation energy. (B) Prediction of deactivation energy.
Fig 7
Fig 7
Percentage S. aureus Q1432 lysogens at different temperatures in the presence of different phage_SAP_1432 concentrations at 33 h.
Fig 8
Fig 8
Survival numbers of S. aureus Q1432 at high temperatures with different MOIs of phage_SAP_1432.

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