Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo
Abstract Background Staphylococcus aureus (SA) and Pseudomonas aeruginosa (PA) cause a wide variety of bacterial infections and coinfections, showing a complex interaction that involves the production of different metabolites and metabolic changes. Temperature is a key factor for bacterial survival...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2024-02-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-024-01830-3 |
| _version_ | 1797273275708997632 |
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| author | E. C. Solar Venero M. B. Galeano A. Luqman M. M. Ricardi F. Serral D. Fernandez Do Porto S. A. Robaldi B. A. Z. Ashari T. H. Munif D. E. Egoburo S. Nemirovsky J. Escalante B. Nishimura M. S. Ramirez F. Götz P. M. Tribelli |
| author_facet | E. C. Solar Venero M. B. Galeano A. Luqman M. M. Ricardi F. Serral D. Fernandez Do Porto S. A. Robaldi B. A. Z. Ashari T. H. Munif D. E. Egoburo S. Nemirovsky J. Escalante B. Nishimura M. S. Ramirez F. Götz P. M. Tribelli |
| author_sort | E. C. Solar Venero |
| collection | DOAJ |
| description | Abstract Background Staphylococcus aureus (SA) and Pseudomonas aeruginosa (PA) cause a wide variety of bacterial infections and coinfections, showing a complex interaction that involves the production of different metabolites and metabolic changes. Temperature is a key factor for bacterial survival and virulence and within the host, bacteria could be exposed to an increment in temperature during fever development. We analyzed the previously unexplored effect of fever-like temperatures (39 °C) on S. aureus USA300 and P. aeruginosa PAO1 microaerobic mono- and co-cultures compared with 37 °C, by using RNAseq and physiological assays including in vivo experiments. Results In general terms both temperature and co-culturing had a strong impact on both PA and SA with the exception of the temperature response of monocultured PA. We studied metabolic and virulence changes in both species. Altered metabolic features at 39 °C included arginine biosynthesis and the periplasmic glucose oxidation in S. aureus and P. aeruginosa monocultures respectively. When PA co-cultures were exposed at 39 °C, they upregulated ethanol oxidation-related genes along with an increment in organic acid accumulation. Regarding virulence factors, monocultured SA showed an increase in the mRNA expression of the agr operon and hld, pmsα, and pmsβ genes at 39 °C. Supported by mRNA data, we performed physiological experiments and detected and increment in hemolysis, staphyloxantin production, and a decrease in biofilm formation at 39 °C. On the side of PA monocultures, we observed an increase in extracellular lipase and protease and biofilm formation at 39 °C along with a decrease in the motility in correlation with changes observed at mRNA abundance. Additionally, we assessed host–pathogen interaction both in vitro and in vivo. S. aureus monocultured at 39οC showed a decrease in cellular invasion and an increase in IL-8—but not in IL-6—production by A549 cell line. PA also decreased its cellular invasion when monocultured at 39 °C and did not induce any change in IL-8 or IL-6 production. PA strongly increased cellular invasion when co-cultured at 37 and 39 °C. Finally, we observed increased lethality in mice intranasally inoculated with S. aureus monocultures pre-incubated at 39 °C and even higher levels when inoculated with co-cultures. The bacterial burden for P. aeruginosa was higher in liver when the mice were infected with co-cultures previously incubated at 39 °C comparing with 37 °C. Conclusions Our results highlight a relevant change in the virulence of bacterial opportunistic pathogens exposed to fever-like temperatures in presence of competitors, opening new questions related to bacteria-bacteria and host–pathogen interactions and coevolution. |
| first_indexed | 2024-03-07T14:41:11Z |
| format | Article |
| id | doaj.art-d031ba68359349dc9163eff129ea52bf |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-07T14:41:11Z |
| publishDate | 2024-02-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-d031ba68359349dc9163eff129ea52bf2024-03-05T20:21:45ZengBMCBMC Biology1741-70072024-02-0122111910.1186/s12915-024-01830-3Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivoE. C. Solar Venero0M. B. Galeano1A. Luqman2M. M. Ricardi3F. Serral4D. Fernandez Do Porto5S. A. Robaldi6B. A. Z. Ashari7T. H. Munif8D. E. Egoburo9S. Nemirovsky10J. Escalante11B. Nishimura12M. S. Ramirez13F. Götz14P. M. Tribelli15Instituto De Química Biológica de La Facultad de Ciencias Exactas y Naturales-CONICETInstituto De Química Biológica de La Facultad de Ciencias Exactas y Naturales-CONICETDepartment of Biology, Institut Teknologi Sepuluh NopemberIFIBYNE (UBA-CONICET), FBMC, FCEyN-UBAInstituto del Calculo-UBA-CONICETInstituto del Calculo-UBA-CONICETDepartamento de Química Biológica, FCEyN-UBADepartment of Biology, Institut Teknologi Sepuluh NopemberDepartment of Biology, Institut Teknologi Sepuluh NopemberDepartamento de Química Biológica, FCEyN-UBAInstituto De Química Biológica de La Facultad de Ciencias Exactas y Naturales-CONICETDepartment of Biological Science, College of Natural Sciences and Mathematics, California State University FullertonDepartment of Biological Science, College of Natural Sciences and Mathematics, California State University FullertonDepartment of Biological Science, College of Natural Sciences and Mathematics, California State University FullertonDepartment of Microbial Genetics, Interfaculty Institute of Microbiology and Infection Medicine Tübingen (IMIT), University of TübingenInstituto De Química Biológica de La Facultad de Ciencias Exactas y Naturales-CONICETAbstract Background Staphylococcus aureus (SA) and Pseudomonas aeruginosa (PA) cause a wide variety of bacterial infections and coinfections, showing a complex interaction that involves the production of different metabolites and metabolic changes. Temperature is a key factor for bacterial survival and virulence and within the host, bacteria could be exposed to an increment in temperature during fever development. We analyzed the previously unexplored effect of fever-like temperatures (39 °C) on S. aureus USA300 and P. aeruginosa PAO1 microaerobic mono- and co-cultures compared with 37 °C, by using RNAseq and physiological assays including in vivo experiments. Results In general terms both temperature and co-culturing had a strong impact on both PA and SA with the exception of the temperature response of monocultured PA. We studied metabolic and virulence changes in both species. Altered metabolic features at 39 °C included arginine biosynthesis and the periplasmic glucose oxidation in S. aureus and P. aeruginosa monocultures respectively. When PA co-cultures were exposed at 39 °C, they upregulated ethanol oxidation-related genes along with an increment in organic acid accumulation. Regarding virulence factors, monocultured SA showed an increase in the mRNA expression of the agr operon and hld, pmsα, and pmsβ genes at 39 °C. Supported by mRNA data, we performed physiological experiments and detected and increment in hemolysis, staphyloxantin production, and a decrease in biofilm formation at 39 °C. On the side of PA monocultures, we observed an increase in extracellular lipase and protease and biofilm formation at 39 °C along with a decrease in the motility in correlation with changes observed at mRNA abundance. Additionally, we assessed host–pathogen interaction both in vitro and in vivo. S. aureus monocultured at 39οC showed a decrease in cellular invasion and an increase in IL-8—but not in IL-6—production by A549 cell line. PA also decreased its cellular invasion when monocultured at 39 °C and did not induce any change in IL-8 or IL-6 production. PA strongly increased cellular invasion when co-cultured at 37 and 39 °C. Finally, we observed increased lethality in mice intranasally inoculated with S. aureus monocultures pre-incubated at 39 °C and even higher levels when inoculated with co-cultures. The bacterial burden for P. aeruginosa was higher in liver when the mice were infected with co-cultures previously incubated at 39 °C comparing with 37 °C. Conclusions Our results highlight a relevant change in the virulence of bacterial opportunistic pathogens exposed to fever-like temperatures in presence of competitors, opening new questions related to bacteria-bacteria and host–pathogen interactions and coevolution.https://doi.org/10.1186/s12915-024-01830-3InteractionTemperatureVirulencePseudomonas aeruginosaStaphylococcus aureus |
| spellingShingle | E. C. Solar Venero M. B. Galeano A. Luqman M. M. Ricardi F. Serral D. Fernandez Do Porto S. A. Robaldi B. A. Z. Ashari T. H. Munif D. E. Egoburo S. Nemirovsky J. Escalante B. Nishimura M. S. Ramirez F. Götz P. M. Tribelli Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo BMC Biology Interaction Temperature Virulence Pseudomonas aeruginosa Staphylococcus aureus |
| title | Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo |
| title_full | Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo |
| title_fullStr | Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo |
| title_full_unstemmed | Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo |
| title_short | Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo |
| title_sort | fever like temperature impacts on staphylococcus aureus and pseudomonas aeruginosa interaction physiology and virulence both in vitro and in vivo |
| topic | Interaction Temperature Virulence Pseudomonas aeruginosa Staphylococcus aureus |
| url | https://doi.org/10.1186/s12915-024-01830-3 |
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