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

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 tempe...

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Main Authors: Ting-ting Liu, Peng-cheng Gao, Jie-wen Cui, Wu-bin Wang, Fu-ying Zheng, Xue-rui Li, Yue-feng Chu
Format: Article
Language:English
Published: American Society for Microbiology 2025-08-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.02271-24
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author Ting-ting Liu
Peng-cheng Gao
Jie-wen Cui
Wu-bin Wang
Fu-ying Zheng
Xue-rui Li
Yue-feng Chu
author_facet Ting-ting Liu
Peng-cheng Gao
Jie-wen Cui
Wu-bin Wang
Fu-ying Zheng
Xue-rui Li
Yue-feng Chu
author_sort Ting-ting Liu
collection DOAJ
description 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.IMPORTANCEUnderstanding 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.
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institution Kabale University
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language English
publishDate 2025-08-01
publisher American Society for Microbiology
record_format Article
series Microbiology Spectrum
spelling doaj-art-f6e40cfd1c0c4b9cb11d4e22c2c976582025-08-20T03:44:01ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-08-0113810.1128/spectrum.02271-24Frenemy: adaptive temperate phage_SAP_1432 supports Staphylococcus aureus survival in changing temperaturesTing-ting Liu0Peng-cheng Gao1Jie-wen Cui2Wu-bin Wang3Fu-ying Zheng4Xue-rui Li5Yue-feng Chu6State Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu, ChinaState Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu, ChinaState Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu, ChinaState Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu, ChinaState Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu, ChinaState Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu, ChinaState Key Laboratory for Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu, ChinaABSTRACT 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.IMPORTANCEUnderstanding 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.https://journals.asm.org/doi/10.1128/spectrum.02271-24Staphylococcus aureusheat-resistant temperate phagetemperaturethermal performance curvelysogeny
spellingShingle Ting-ting Liu
Peng-cheng Gao
Jie-wen Cui
Wu-bin Wang
Fu-ying Zheng
Xue-rui Li
Yue-feng Chu
Frenemy: adaptive temperate phage_SAP_1432 supports Staphylococcus aureus survival in changing temperatures
Microbiology Spectrum
Staphylococcus aureus
heat-resistant temperate phage
temperature
thermal performance curve
lysogeny
title Frenemy: adaptive temperate phage_SAP_1432 supports Staphylococcus aureus survival in changing temperatures
title_full Frenemy: adaptive temperate phage_SAP_1432 supports Staphylococcus aureus survival in changing temperatures
title_fullStr Frenemy: adaptive temperate phage_SAP_1432 supports Staphylococcus aureus survival in changing temperatures
title_full_unstemmed Frenemy: adaptive temperate phage_SAP_1432 supports Staphylococcus aureus survival in changing temperatures
title_short Frenemy: adaptive temperate phage_SAP_1432 supports Staphylococcus aureus survival in changing temperatures
title_sort frenemy adaptive temperate phage sap 1432 supports staphylococcus aureus survival in changing temperatures
topic Staphylococcus aureus
heat-resistant temperate phage
temperature
thermal performance curve
lysogeny
url https://journals.asm.org/doi/10.1128/spectrum.02271-24
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