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Listeria monocytogenes exposed to antimicrobial peptides displays differential regulation of lipids and proteins associated to stress response

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Abstract

With the onset of Listeria monocytogenes resistance to the bacteriocin nisin, the search for alternative antimicrobial treatments is of fundamental importance. In this work, we set out to investigate proteins and lipids involved in the resistance mechanisms of L. monocytogenes against the antimicrobial peptides (AMPs) nisin and fengycin. The effect of sub-lethal concentrations of nisin and lipopeptide fengycin secreted by Bacillus velezensis P34 on L. monocytogenes was investigated by mass spectrometry-based lipidomics and proteomics. Both AMPs caused a differential regulation of biofilm formation, confirming the promotion of cell attachment and biofilm assembling after treatment with nisin, whereas growth inhibition was observed after fengycin treatment. Anteiso branched-chain fatty acids were detected in higher amounts in fengycin-treated samples (46.6%) as compared to nisin-treated and control samples (39.4% and 43.4%, respectively). In addition, a higher relative abundance of 30:0, 31:0 and 32:0 phosphatidylglycerol species was detected in fengycin-treated samples. The lipidomics data suggest the inhibition of biofilm formation by the fengycin treatment, while the proteomics data revealed downregulation of important cell wall proteins involved in the building of biofilms, such as the lipoteichoic acid backbone synthesis (Lmo0927) and the flagella-related (Lmo0718) proteins among others. Together, these results provide new insights into the modification of lipid and protein profiles and biofilm formation in L. monocytogenes upon exposure to antimicrobial peptides.

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Availability of data and material

The lipidomics and proteomics mass spectrometry data are publicly available through the MassIVE repository under the following accession numbers: MSV000088672 and MSV000088738.

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Acknowledgements

Authors thank Dr. Adriana Franco Paes Leme, M.Sc. Romenia Ramos Domingues and Dr. Bianca Alves Pauletti, from Mass Spectrometry Laboratory of LNBio/CNPEM (Campinas, Brazil) for hel** us to perform the LC-MS/MS procedures.

Funding

This work received financial support from CNPq (Brasilia, Brazil) [grant 308880/2021–8]. PS was a former recipient of a PhD fellowship from CAPES. PS and DP were supported through the Deutsche Forschungsgemeinschaft through the CMFI Cluster of Excellence (EXC 2124).

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Authors and Affiliations

  1. Laboratório de Bioquímica e Microbiologia Aplicada, ICTA-UFRGS, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves 9500, Porto Alegre, 91501-970, Brazil

    Paolo Stincone, Flávio Fonseca Veras & Adriano Brandelli

  2. Chromaleont S.R.L., c/o Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, viale Annunziata, 98168, Polo AnnunziataMessina, Italy

    Giuseppe Micalizzi, Danilo Donnarumma & Luigi Mondello

  3. Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Polo Annunziata, viale Annunziata, 98168, Messina, Italy

    Luigi Mondello

  4. Department of Veterinary Medicine, University of Bari Aldo Moro, Prov. le Casamassima, km 3, Valenzano, 70010, Bari, Italy

    Gaetano Vitale Celano

  5. CMFI Cluster of Excellence, Interfaculty Institute of Microbiology and Medicine, University of Tübingen, 72076, Tübingen, Germany

    Daniel Petras

  6. Department of Soil, Plant and Food Sciences, University of Bari Aldo Moro, 70126, Bari, Italy

    Maria de Angelis

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  1. Paolo Stincone
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  2. Flávio Fonseca Veras
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  3. Giuseppe Micalizzi
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  4. Danilo Donnarumma
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  5. Gaetano Vitale Celano
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  6. Daniel Petras
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  7. Maria de Angelis
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  8. Luigi Mondello
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  9. Adriano Brandelli
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PS, AB, LM, and MdA contributed to the study conception and design. Material preparation, data collection, data analysis, and statistical analysis were performed by PS, FFV, GM, DD, DP and GVC. The manuscript was written by PS and critically revised by AB. All the authors read and approved the final manuscript.

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Correspondence to Adriano Brandelli.

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Stincone, P., Fonseca Veras, F., Micalizzi, G. et al. Listeria monocytogenes exposed to antimicrobial peptides displays differential regulation of lipids and proteins associated to stress response. Cell. Mol. Life Sci. 79, 263 (2022). https://doi.org/10.1007/s00018-022-04292-4

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  • DOI: https://doi.org/10.1007/s00018-022-04292-4

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