Abstract
Background
The high mortality associated with drug-resistant bacterial infections is an intractable clinical problem resulting from the low susceptibility of these bacteria to antibiotics and the high incidence of recurrent infections.
Methods
Herein, a photosynthetic bacteria-based multiplex system (Rp@Al) composed of natural Rhodopseudomonas palustris (Rp) and Food and Drug Administration-approved aluminum (Al) adjuvant, was developed to combat drug-resistant bacterial infections and prevent their recurrence. We examined its photothermal performance and in vitro and in vivo antibacterial ability; revealed its protective immunomodulatory effect; verified its preventative effect on recurrent infections; and demonstrated the system’s safety.
Results
Rp@Al exhibits excellent photothermal properties with an effective elimination of methicillin-resistant Staphylococcus aureus (MRSA). In addition, Rp@Al enhances dendritic cell activation and further triggers a T helper 1 (TH1)/TH2 immune response, resulting in pathogen-specific immunological memory against recurrent MRSA infection. Upon second infection, Rp@Al-treated mice show significantly lower bacterial burden, faster abscess recovery, and higher survival under near-lethal infection doses than control mice.
Conclusions
This innovative multiplex system, with superior photothermal and immunomodulatory effects, presents great potential for the treatment and prevention of drug-resistant bacterial infections.
Graphical Abstract
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Background
In clinics, antibiotics are the preferred line of treatment for bacterial infections. However, their misuse has resulted in the emergence and rapid increase of multidrug-resistant pathogens [1,2,3,4]. A comprehensive study of 204 countries and territories estimated that there were 4.95 million deaths associated with antimicrobial resistance (AMR), which has become the third leading cause of death worldwide [5]. Furthermore, a review on AMR, commissioned by the UK government, reported that AMR-related deaths will exceed 10 million annually by 2050, surpassing cancer-related deaths [6]. The high mortality associated with drug-resistant bacterial infections is ascribed not only to the low susceptibility of these bacteria to antibiotics, but also to the high incidence of recurrent infections [7, 8]. Methicillin-resistant Staphylococcus aureus (MRSA), with a high risk of recurrence, is one of the most common drug-resistant bacteria in bacteremia, endocarditis, skin and soft tissue infections, bone and joint infections, and hospital-acquired infections [9]. Therefore, it is imperative to develop non-antibiotic therapies that integrate treatment and prevention against drug-resistant bacteria and their recurrent infections.
Bacteria-mediated therapies have attracted remarkable attention in recent years [10,11, In summary, we presented a multiplex system that utilizes photothermal ablation to achieve drug-resistant bacteria abrogation, while also preventing recurrent infections with drug-resistant bacteria through adjuvant-like modulation of the host immune response. Specifically, we i) developed a PSB-based multiplex system (Rp@Al) that was fabricated through electrostatic-driven self-assembly for combating drug-resistant bacterial infections; ii) demonstrated that Rp@Al, containing BChl, which absorbs NIR light at around 805 and 865 nm, exhibited prominent photothermal properties and photothermal ablation ability toward drug-resistant bacteria; iii) revealed that Rp@Al exerts an adjuvant-like effect to enhance the antigen presentation of activated DCs, thereby priming TH1/TH2 immune responses, resulting in a protective pathogen-specific immunological memory against recurrent infections with drug-resistant bacteria; and iv) illustrated that Rp@Al not only eliminates drug-resistant bacteria through photothermal killing but also plays a preventive role in reducing infection burden and prolonging the survival period of mice during recurrent infections (Fig. 7). Schematic illustration of PSB-based multiplex system for the treatment of drug-resistant bacterial infections. Photosynthetic bacteria (PSB)-based Rp@Al, fabricated through an electrostatic-driven self-assembly process, containing bacteriochlorophyll (BChl) that absorbs near-infrared (NIR) light at around 805 and 865 nm, exhibited effective photothermal ablation of MRSA. Rp@Al also exerted an adjuvant-like effect to enhance the antigen presentation of activated DCs, thereby priming the T helper 1 (TH1)/TH2 immune response, resulting in a protective pathogen-specific immunological memory against recurrent infections with the same drug-resistant bacteriaConclusions
Availability of data and materials
The data that support the findings of this study are available from the corresponding authors upon reasonable request.
Abbreviations
- AMR:
-
Antimicrobial resistance
- MRSA :
-
Methicillin-resistant Staphylococcus aureus
- PSB:
-
Photosynthetic bacteria
- BChl:
-
Bacteriochlorophyll
- NIR:
-
Near-infrared
- PRRs:
-
Pattern recognition receptors
- TLRs:
-
Toll-like receptors
- NLRs:
-
NOD-like receptors
- BHI:
-
Brain Heart Infusion
- IFNγ:
-
Interferon γ
- IL:
-
Interleukin
- ELISA:
-
Enzyme-linked immunosorbent assay
- ALT:
-
Alanine aminotransferase
- AST:
-
Aspartate aminotransferase
- CRE:
-
Creatinine
- BUN:
-
Blood urea nitrogen
- TC:
-
Total cholesterol
- TG:
-
Triglyceride
- GLU:
-
Glucose
- Rp:
-
Rhodopseudomonas palustris
- PBS:
-
Phosphate-buffered saline
- PFA:
-
Paraformaldehyde
- DCs:
-
Dendritic cells
- H&E:
-
Hematoxylin and eosin
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Acknowledgements
We acknowledge the Anhui Center for Surveillance of Bacterial Resistance for providing the MRSA strain and the China Center of Industrial Culture Collection for providing the Rp strain.
Funding
This work was supported by the National Natural Science Foundation of China [grant numbers 81871788 and 32171375]; the Outstanding Youth Fund of Natural Science Foundation of Anhui Province [grant number 2108085J41]; the Key Research and Development Program of Anhui Province [grant number 202004j07020013]; the Anhui Provincial Postdoctoral Science Foundation [grant number 2019 B302]; the Scientific Research Fund of Anhui Education Office [grant number 2020jyxm2316]; and the Anhui Province Natural Science Foundation (grant numbers 1908085MH263).
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Additional file 1: Fig. S1.
Stability of Rp@Al on days 0, 3, and 7. Fig. S2. The preparation mechanism of Rp@Al. Fig. S3. Statistical analysis of scanning electron microscopy (SEM) images of Rp showing its diameter distribution. Fig. S4. Representative image of a growing Rp culture. Fig. S5. Time-lapse images showing the photothermal conversion of PBS, Rp, and Rp@Al. Fig. S6. Time-lapse images showing the photothermal conversion of PBS and different concentrations of Rp@Al. Fig. S7. Time-lapse images showing the photothermal conversion of Rp@Al using an 808-nm laser. Fig. S8. Levels of reactive oxygen species in methicillin-resistant Staphylococcus aureus (MRSA) after different treatment. Fig. S9. Temperature monitoring of the abscess site in mice under 808 nm laser irradiation. Fig. S10. Quantitative analysis showing collagen deposition levels in different treatment groups. Fig. S11. Representative flow scatter plot showing the percentage of CD4+ T cells in total leukocytes. Fig. S12. Comparative analysis of the proportion of memory B cells in mice from different treatment groups. Fig. S13. Time-lapse images showing the abscess recovery in treatment groups after second subcutaneous injection of MRSA. Fig. S14. The abscess recovery in different treatment groups after a second subcutaneous infection of MRSA. Fig. S15. Weight of the mice before intravenous re-infection with MRSA. Table S1. Summary of the photothermal conversion efficiency (η) of some photothermal agents that have been reported. Table S2. Summary of the pros and cons for different nanomaterials for antibacterial applications.
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Xu, Y., Wu, Y., Hu, Y. et al. Bacteria-based multiplex system eradicates recurrent infections with drug-resistant bacteria via photothermal killing and protective immunity elicitation. Biomater Res 27, 27 (2023). https://doi.org/10.1186/s40824-023-00363-0
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DOI: https://doi.org/10.1186/s40824-023-00363-0