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Environmental Microbiology

NisI Maturation and Its Influence on Nisin Resistance in Lactococcus lactis

Jiaheng Liu, Hui Xiong, Yuhui Du, Itsanun Wiwatanaratanabutr, Xiaofang Wu, Guangrong Zhao, Hongji Zhu, Qinggele Caiyin, Jianjun Qiao
Danilo Ercolini, Editor
Jiaheng Liu
aKey Laboratory of Systems Bioengineering (Ministry of Education), Tianjin University, Tianjin, China
bSchool of Chemical Engineering and Technology, Tianjin University, Tianjin, China
cSynBio Research Platform, Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), Tianjin, China
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Hui Xiong
aKey Laboratory of Systems Bioengineering (Ministry of Education), Tianjin University, Tianjin, China
bSchool of Chemical Engineering and Technology, Tianjin University, Tianjin, China
cSynBio Research Platform, Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), Tianjin, China
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Yuhui Du
dKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of Technology, Beijing, China
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Itsanun Wiwatanaratanabutr
eCenter of Excellence in Applied Biosciences, King Mongkut’s Institute of Technology Ladkrabang, Bangkok, Thailand
fDepartment of Plant Production Technology, Faculty of Agricultural Technology, King Mongkut’s Institute of Technology Ladkrabang, Bangkok, Thailand
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Xiaofang Wu
aKey Laboratory of Systems Bioengineering (Ministry of Education), Tianjin University, Tianjin, China
bSchool of Chemical Engineering and Technology, Tianjin University, Tianjin, China
cSynBio Research Platform, Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), Tianjin, China
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Guangrong Zhao
aKey Laboratory of Systems Bioengineering (Ministry of Education), Tianjin University, Tianjin, China
bSchool of Chemical Engineering and Technology, Tianjin University, Tianjin, China
cSynBio Research Platform, Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), Tianjin, China
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Hongji Zhu
aKey Laboratory of Systems Bioengineering (Ministry of Education), Tianjin University, Tianjin, China
bSchool of Chemical Engineering and Technology, Tianjin University, Tianjin, China
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Qinggele Caiyin
aKey Laboratory of Systems Bioengineering (Ministry of Education), Tianjin University, Tianjin, China
bSchool of Chemical Engineering and Technology, Tianjin University, Tianjin, China
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Jianjun Qiao
aKey Laboratory of Systems Bioengineering (Ministry of Education), Tianjin University, Tianjin, China
bSchool of Chemical Engineering and Technology, Tianjin University, Tianjin, China
cSynBio Research Platform, Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), Tianjin, China
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  • ORCID record for Jianjun Qiao
Danilo Ercolini
University of Naples Federico II
Roles: Editor
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DOI: 10.1128/AEM.01306-20
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ABSTRACT

NisI confers immunity against nisin, with high substrate specificity to prevent a suicidal effect in nisin-producing Lactococcus lactis strains. However, the NisI maturation process as well as its influence on nisin resistance has not been characterized. Here, we report the roles of lipoprotein signal peptidase II (Lsp) and prolipoprotein diacylglyceryl transferase (Lgt) in NisI maturation and nisin resistance of L. lactis F44. We found that the resistance of nisin of an Lsp-deficient mutant remarkably decreased, while no significant differences in growth were observed. We demonstrated that Lsp could cleave signal peptide of NisI precursor in vitro. Moreover, diacylglyceryl modification of NisI catalyzed by Lgt played a decisive role in attachment of NisI on the cell envelope, while it exhibited no effects on cleavage of the signal peptides of NisI precursor. The dissociation constant (KD) for the interaction between nisin and NisI exhibited a 2.8-fold increase compared with that between nisin and pre-NisI with signal peptide by surface plasmon resonance (SPR) analysis, providing evidence that Lsp-catalyzed signal peptide cleavage was critical for the immune activity of NisI. Our study revealed the process of NisI maturation in L. lactis and presented a potential strategy to enhance industrial nisin production.

IMPORTANCE Nisin, a safe and natural antimicrobial peptide, has a long and impressive history as a food preservative and is also considered a novel candidate to alleviate the increasingly serious threat of antibiotic resistance. Nisin is produced by certain L. lactis strains. The nisin immunity protein NisI, a membrane-bound lipoprotein, is expressed by nisin producers to avoid suicidal action. Here, we report the roles of Lsp and Lgt in NisI maturation and nisin resistance of L. lactis F44. The results verified the importance of Lsp to NisI-conferred immunity and Lgt to localization. Our study revealed the process of NisI maturation in L. lactis and presented a potential strategy to enhance industrial nisin production.

FOOTNOTES

    • Received 1 June 2020.
    • Accepted 22 July 2020.
    • Accepted manuscript posted online 24 July 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

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NisI Maturation and Its Influence on Nisin Resistance in Lactococcus lactis
Jiaheng Liu, Hui Xiong, Yuhui Du, Itsanun Wiwatanaratanabutr, Xiaofang Wu, Guangrong Zhao, Hongji Zhu, Qinggele Caiyin, Jianjun Qiao
Applied and Environmental Microbiology Sep 2020, 86 (19) e01306-20; DOI: 10.1128/AEM.01306-20

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NisI Maturation and Its Influence on Nisin Resistance in Lactococcus lactis
Jiaheng Liu, Hui Xiong, Yuhui Du, Itsanun Wiwatanaratanabutr, Xiaofang Wu, Guangrong Zhao, Hongji Zhu, Qinggele Caiyin, Jianjun Qiao
Applied and Environmental Microbiology Sep 2020, 86 (19) e01306-20; DOI: 10.1128/AEM.01306-20
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KEYWORDS

Lactococcus lactis
NisI maturation
lipoprotein signal peptidase
nisin resistance
prolipoprotein diacylglyceryl transferase

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