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Streptococcal arginine deiminase system defences macrophage bactericidal effect mediated by XRE family protein XtrSs

Yumin Zhanga Sanya Institute of Nanjing Agricultural University, Nanjing Agricultural University, Sanya, China;b College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;c OIE Reference Lab for Swine Streptococcosis, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;d Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;e Key Laboratory of Animal Bacteriology, Ministry of Agriculture, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaView further author information

Song Lianga Sanya Institute of Nanjing Agricultural University, Nanjing Agricultural University, Sanya, China;b College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;c OIE Reference Lab for Swine Streptococcosis, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;d Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;e Key Laboratory of Animal Bacteriology, Ministry of Agriculture, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaView further author information

Shidan Zhanga Sanya Institute of Nanjing Agricultural University, Nanjing Agricultural University, Sanya, China;b College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;c OIE Reference Lab for Swine Streptococcosis, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;d Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;e Key Laboratory of Animal Bacteriology, Ministry of Agriculture, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaView further author information

Qiankun Baia Sanya Institute of Nanjing Agricultural University, Nanjing Agricultural University, Sanya, China;b College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;c OIE Reference Lab for Swine Streptococcosis, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;d Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;e Key Laboratory of Animal Bacteriology, Ministry of Agriculture, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaView further author information

Lei Daif Hainan Animal Disease Prevention and Control Center, Haikou, ChinaView further author information

Jinxiu Wangf Hainan Animal Disease Prevention and Control Center, Haikou, ChinaView further author information

Huochun Yaoa Sanya Institute of Nanjing Agricultural University, Nanjing Agricultural University, Sanya, China;b College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;c OIE Reference Lab for Swine Streptococcosis, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;d Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;e Key Laboratory of Animal Bacteriology, Ministry of Agriculture, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaView further author information

Wei Zhanga Sanya Institute of Nanjing Agricultural University, Nanjing Agricultural University, Sanya, China;b College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;c OIE Reference Lab for Swine Streptococcosis, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;d Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;e Key Laboratory of Animal Bacteriology, Ministry of Agriculture, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaView further author information

Guangjin Liua Sanya Institute of Nanjing Agricultural University, Nanjing Agricultural University, Sanya, China;b College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;c OIE Reference Lab for Swine Streptococcosis, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;d Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China;e Key Laboratory of Animal Bacteriology, Ministry of Agriculture, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaCorrespondence[email protected]

https://orcid.org/0000-0001-7857-9444 View further author information

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ABSTRACT

The arginine deiminase system (ADS) has been identified in various bacteria and functions to supplement energy production and enhance biological adaptability. The current understanding of the regulatory mechanism of ADS and its effect on bacterial pathogenesis is still limited. Here, we found that the XRE family transcriptional regulator XtrSs negatively affected Streptococcus suis virulence and significantly repressed ADS transcription when the bacteria were incubated in blood. Electrophoretic mobility shift (EMSA) and lacZ fusion assays further showed that XtrSs directly bind to the promoter of ArgR, an acknowledged positive regulator of bacterial ADS, to repress ArgR transcription. Moreover, we provided compelling evidence that S. suis could utilize arginine via ADS to adapt to acid stress, while ΔxtrSs enhanced this acid resistance by upregulating the ADS operon. Moreover, whole ADS-knockout S. suis increased arginine and antimicrobial NO in the infected macrophage cells, decreased intracellular survival, and even caused significant attenuation of bacterial virulence in a mouse infection model, while ΔxtrSs consistently presented the opposite results. Our experiments identified a novel ADS regulatory mechanism in S. suis, whereby XtrSs regulated ADS to modulate NO content in macrophages, promoting S. suis intracellular survival. Meanwhile, our findings provide a new perspective on how Streptococci evade the host’s innate immune system.

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Acknowledgements

We thank Shaynoor Dramsi for providing the plasmid pTCV-lac.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data Availability statement

The datasets are available from the corresponding author on reasonable request.

Supplemental data

Supplemental data for this article can be accessed online at https://doi.org/10.1080/21505594.2024.2306719

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Funding

This work was supported by grants from the Hainan Province Science and Technology Special Fund [ZDYF2022XDNY236], Fundamental Research Funds for the Central Universities [KYTZ2023002], and Youth Foundation of the National Natural Science Foundation of China [31502085].

Streptococcal arginine deiminase system defences macrophage bactericidal effect mediated by XRE family protein XtrSs

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Streptococcal arginine deiminase system defences macrophage bactericidal effect mediated by XRE family protein XtrSs

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Acknowledgements

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Data Availability statement

Supplemental data

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