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European Biophysics Journal

, Volume 48, Issue 7, pp 621–633 | Cite as

Unveiling the binding and orientation of the antimicrobial peptide Plantaricin 149 in zwitterionic and negatively charged membranes

  • Patricia S. Kumagai
  • Victor K. Sousa
  • Maressa Donato
  • Rosangela Itri
  • Leila M. Beltramini
  • Ana P. U. Araujo
  • Jochen Buerck
  • B. A. Wallace
  • Jose L. S. LopesEmail author
Original Article
  • 133 Downloads

Abstract

Antimicrobial peptides are a large group of natural compounds which present promising properties for the pharmaceutical and food industries, such as broad-spectrum activity, potential for use as natural preservatives, and reduced propensity for development of bacterial resistance. Plantaricin 149 (Pln149), isolated from Lactobacillus plantarum NRIC 149, is an intrinsically disordered peptide with the ability to inhibit bacteria from the Listeria and Staphylococcus genera, and which is capable of promoting inhibition and disruption of yeast cells. In this study, the interactions of Pln149 with model membranes composed of zwitterionic and/or anionic phospholipids were investigated using a range of biophysical techniques, including isothermal titration calorimetry, surface tension measurements, synchrotron radiation circular dichroism spectroscopy, oriented circular dichroism spectroscopy, and optical microscopy, to elucidate these peptides’ mode of interactions and provide insight into their functional roles. In anionic model membranes, the binding of Pln149 to lipid bilayers is an endothermic process and induces a helical secondary structure in the peptide. The helices bind parallel to the surfaces of lipid bilayers and can promote vesicle disruption, depending on peptide concentration. Although Pln149 has relatively low affinity for zwitterionic liposomes, it is able to adsorb at their lipid interfaces, disturbing the lipid packing, assuming a similar parallel helix structure with a surface-bound orientation, and promoting an increase in the membrane surface area. Such findings can explain the intriguing inhibitory action of Pln149 in yeast cells whose cell membranes have a significant zwitterionic lipid composition.

Keywords

Antimicrobial peptide Oriented circular dichroism spectroscopy Mechanism of action Peptide–lipid interactions Synchrotron radiation circular dichroism spectroscopy 

Notes

Acknowledgements

We are grateful for the financial support of the following: a paired Biotechnology and Biological Sciences Research Council (BBSRC) Grant N012763/1/Sao Paulo Research Foundation (FAPESP) Grant 2015/50347-2 (to APUA and BAW), CNPq/PIBIC fellowship (to VKS), Grants 303513/2016-0 and 406429/2016-2 from CNPq-Brazil (to JLSL), FAPESP/CEPID Grant 2013/07600-3 (to LMB), FAPESP Grant 2018/19546-7 (to JLSL), Grant P02409 from the BBSRC (to BAW). APU, JLSL, LMB, and RI are recipients of research CNPq fellowships. Access to the AU-CD at ASTRID2 was supported by a beamtime grant (to PSK and JLSL). Access to beamline UV-CD12 of the Institute of Biological Interfaces (IBG2) and the Institute for Beam Physics and Technology (IBPT) storage ring, the Karlsruhe Research Accelerator (KARA) was enabled by grants from the Karlsruhe Institute of Technology.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

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Copyright information

© European Biophysical Societies' Association 2019

Authors and Affiliations

  1. 1.Instituto de Física de São CarlosUniversidade de São PauloSão CarlosBrazil
  2. 2.Departamento Física Aplicada, Instituto de FísicaUniversidade de São PauloSão PauloBrazil
  3. 3.Institute of Biological Interfaces (IBG-2)Karlsruhe Institute of Technology (KIT)KarlsruheGermany
  4. 4.Institute of Structural and Molecular Biology, Birkbeck CollegeUniversity of LondonLondonUK

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