Journal Home > Volume 12 , Issue 4

Listeria monocytogenes is a worrisome food-borne pathogen threatening global food safety. Our previous study proved that lipopeptide brevilaterin B showed efficient antibacterial activity against L. monocytogenes by interacting with the cell membrane. This research further explored the antibacterial mechanism of brevilaterin B against L. monocytogenes at the sub-minimum inhibition concentration via transcriptomic analysis. Brevilaterin B induced growth inhibition rather than direct membrane lysis in L. monocytogenes at the minimum inhibitory concentration. Transcriptomic analysis showed 1779 difference expressed genes, including 895 up-regulated and 884 down-regulated genes. Gene Ontology and Kyoto Encyclopedia of Genes and Genomes analysis indicated that brevilaterin B influenced multiple pathways of L. monocytogenes, including peptidoglycan biosynthesis, membrane transport (ATP-binding cassette transports, ion transport), cellular metabolism (amino acid and lipid metabolism), ATP synthesis, and activation of the stress response (quorum sensing and bacterial chemotaxis). In conclusion, brevilaterin B affects gene expression related to biosynthesis, transport and stress response pathways on the membrane of L. monocytogenes. The present work provides the first transcriptomic assessment of the antibacterial mechanism of lipopeptide brevilaterin B at the gene level.


menu
Abstract
Full text
Outline
About this article

Transcriptomics reveals substance biosynthesis and transport on membranes of Listeria monocytogenes affected by antimicrobial lipopeptide brevilaterin B

Show Author's information Yangliu LiuaYawei NingbZhou ChenaPanpan HanaTongxin ZhiaSiting LiaAijin Maa( )Yingmin Jiaa( )
School of Food and Health, Beijing Technology and Business University, Beijing 100048, China
College of Food Science and Biology, Hebei University of Science and Technology, Shijiazhuang 050018, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Abstract

Listeria monocytogenes is a worrisome food-borne pathogen threatening global food safety. Our previous study proved that lipopeptide brevilaterin B showed efficient antibacterial activity against L. monocytogenes by interacting with the cell membrane. This research further explored the antibacterial mechanism of brevilaterin B against L. monocytogenes at the sub-minimum inhibition concentration via transcriptomic analysis. Brevilaterin B induced growth inhibition rather than direct membrane lysis in L. monocytogenes at the minimum inhibitory concentration. Transcriptomic analysis showed 1779 difference expressed genes, including 895 up-regulated and 884 down-regulated genes. Gene Ontology and Kyoto Encyclopedia of Genes and Genomes analysis indicated that brevilaterin B influenced multiple pathways of L. monocytogenes, including peptidoglycan biosynthesis, membrane transport (ATP-binding cassette transports, ion transport), cellular metabolism (amino acid and lipid metabolism), ATP synthesis, and activation of the stress response (quorum sensing and bacterial chemotaxis). In conclusion, brevilaterin B affects gene expression related to biosynthesis, transport and stress response pathways on the membrane of L. monocytogenes. The present work provides the first transcriptomic assessment of the antibacterial mechanism of lipopeptide brevilaterin B at the gene level.

Keywords: Transcriptomics, Antimicrobial lipopeptide, Brevilaterin B, Antibacterial mechanism, Listeria monocytogenes

References(55)

[1]

M. Gandhi, M.L. Chikindas, Listeria: a foodborne pathogen that knows how to survive, Int. J. Food Microbiol. 113 (2007) 1-15. https://doi.org/10.1016/j.ijfoodmicro.2006.07.008.

[2]

S.T. Duze, M. Marimani, M. Patel, Tolerance of Listeria monocytogenes to biocides used in food processing environments, Food Microbiol. 97 (2021) 103758. https://doi.org/10.1016/j.fm.2021.103758.

[3]

A.N. Olaimat, M.A. Al-Holy, H.M. Shahbaz, et al., Emergence of antibiotic resistance in Listeria monocytogenes isolated from food products: a comprehensive review, Compr. Rev. Food Sci. Food Saf. 17 (2018) 1277-1292. https://doi.org/10.1111/1541-4337.12387.

[4]

J. Wang, X. Dou, J. Song, et al., Antimicrobial peptides: promising alternatives in the post feeding antibiotic era, Med. Res. Rev. 39 (2019) 831-859. https://doi.org/10.1002/med.21542.

[5]

X. Yang, A.E. Yousef, Antimicrobial peptides produced by Brevibacillus spp.: structure, classification and bioactivity: a mini review, World J. Microbiol. Biotechnol. 34 (2018) 57. https://doi.org/10.1007/s11274-018-2437-4.

[6]

T. Barsby, K. Warabi, D. Sørensen, et al., The bogorol family of antibiotics: template-based structure elucidation and a new approach to positioning enantiomeric pairs of amino acids, J. Org. Chem. 71 (2006) 6031-6037. https://doi.org/10.1021/jo060667p.

[7]

Y. Ning, P. Han, J. Ma, et al., Characterization of brevilaterins, multiple antimicrobial peptides simultaneously produced by Brevibacillus laterosporus S62-9, and their application in real food system, Food Biosci. 42 (2020) 104743. https://doi.org/10.1016/j.fbio.2021.101091.

[8]

Y.X. Li, Z. Zhong, W.P. Zhang, et al., Discovery of cationic nonribosomal peptides as Gram-negative antibiotics through global genome mining, Nat. Commun. 9 (2018) 1-9. https://doi.org/10.1038/s41467-018-05781-6.

[9]

H. Jiang, X. Wang, C. Xiao, et al., Antifungal activity of Brevibacillus laterosporus JX-5 and characterization of its antifungal components, World J. Microbiol. Biotechnol. 31 (2015) 1605-1618. https://doi.org/10.1007/s11274-015-1912-4.

[10]

M. Miljkovic, S. Jovanovic, P.M. O'Connor, et al., Brevibacillus laterosporus strains BGSP7, BGSP9 and BGSP11 isolated from silage produce broad spectrum multi-antimicrobials, PLoS One 14 (2019) e0216773. https://doi.org/10.1371/journal.pone.0216773.

[11]

K.A. Odah, W.L. Dong, L. Lei, et al., Isolation, identification, and characterization of a novel bacteriocin produced by Brevibacillus laterosporus DS-3 against methicillin-resistant Staphylococcus aureus (MRSA), Int. J. Pept. Res. Ther. 26 (2020) 709-715. https://doi.org/10.1007/s10989-019-09878-4.

[12]

X. Yang, E. Huang, C. Yuan, et al., Isolation and structural elucidation of brevibacillin, an antimicrobial lipopeptide from Brevibacillus laterosporus that combats drug-resistant Gram-positive bacteria, Appl. Environ. Microbiol. 82 (2016) 2763-2772. https://doi.org/10.1128/AEM.00315-16.

[13]

Y. Liu, Z. Chen, L. Liu, et al., Broad-spectrum antifungal activity of lipopeptide brevilaterin B and its inhibition effects against Fusarium oxysporum and Penicillium chrysogenum, J. Appl. Microbiol. 132 (2022) 1330-1342. https://doi.org/10.1111/jam.15285.

[14]

Y. Liu, A. Ma, P. Han, et al., Antibacterial mechanism of brevilaterin B: an amphiphilic lipopeptide targeting the membrane of Listeria monocytogenes, Appl. Microbiol. Biotechnol. 104 (2020) 10531-10539. https://doi.org/10.1007/s00253-020-10993-2.

[15]

X. Yang, E. Huang, A.E. Yousef, Brevibacillin, a cationic lipopeptide that binds to lipoteichoic acid and subsequently disrupts cytoplasmic membrane of Staphylococcus aureus, Microbiol. Res. 195 (2017) 18-23. https://doi.org/10.1016/j.micres.2016.11.002.

[16]

Z. Li, R.H. de Vries, P. Chakraborty, et al., Novel modifications of nonribosomal peptides from Brevibacillus laterosporus MG64 and investigation of their mode of action, Appl. Environ. Microbiol. 86 (2020) e01981-20. https://doi.org/10.1128/AEM.1981-20.

[17]

X. Zhao, X. Wang, R. Shukla, et al., Brevibacillin 2V exerts its bactericidal activity via binding to Lipid Ⅱ and permeabilizing cellular membranes, Front. Microbiol. 12 (2021) 2040. https://doi.org/10.3389/fmicb.2021.694847.

[18]

X. Zhang, N. Gu, Y. Zhou, et al., Transcriptome analysis reveals the mechanisms involved in the enhanced antagonistic efficacy of Rhodotorula mucilaginosa induced by chitosan, LWT-Food Sci. Technol. 142 (2021) 110992. https://doi.org/10.1016/j.lwt.2021.110992.

[19]

Y. Liu, L. Wu, J. Han, et al., Inhibition of biofilm formation and related gene expression of Listeria monocytogenes in response to four natural antimicrobial compounds and sodium hypochlorite, Front. Microbiol. 11 (2021) 3523. https://doi.org/10.3389/fmicb.2020.617473.

[20]

Y. Ning, A. Yan, K. Yang, et al., Antibacterial activity of phenyllactic acid against Listeria monocytogenes and Escherichia coli by dual mechanisms, Food Chem. 228 (2017) 533-540. https://doi.org/10.1016/j.foodchem.2017.01.112.

[21]

A.M. Bolger, M. Lohse, B. Usadel, Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics 30 (2014) 2114-2120. https://doi.org/10.1093/bioinformatics/btu170.

[22]

B. Langmead, S.L. Salzberg, Fast gapped-read alignment with Bowtie 2, Nat. Methods 9 (2012) 357-359. https://doi.org/10.1038/nmeth.1923.

[23]

K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method, Methods 25 (2001) 402-408. https://doi.org/10.1006/meth.2001.1262.

[24]

L. Li, Y. Shi, M.J. Cheserek, et al., Antibacterial activity and dual mechanisms of peptide analog derived from cell-penetrating peptide against Salmonella typhimurium and Streptococcus pyogenes, Appl. Microbiol. Biotechnol. 97 (2013) 1711-1723. https://doi.org/10.1007/s00253-012-4352-1.

[25]

A. Apetrei, A. Asandei, Y. Park, et al., Unimolecular study of the interaction between the outer membrane protein OmpF from E. coli and an analogue of the HP(2-20) antimicrobial peptide, J. Bioenerg. Biomembr. 42 (2010) 173-180. https://doi.org/10.1007/s10863-010-9273-z.

[26]

J.L. Gifford, H.N. Hunter, H.J. Vogel, Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties, Cell Mol. Life Sci. 62 (2005) 2588-2598. https://doi.org/10.1007/s00018-005-5373-z.

[27]

S.J. Kim, J. Chang, M. Singh, Peptidoglycan architecture of Gram-positive bacteria by solid-state NMR, Biochim. Biophys. Acta-Biomembr. 1848 (2015) 350-362. https://doi.org/10.1016/j.bbamem.2014.05.031.

[28]

M. Beeby, J.C. Gumbart, B. Roux, et al., Architecture and assembly of the Gram-positive cell wall, Mol. Microbiol. 88 (2013) 664-672. https://doi.org/10.1111/mmi.12203.

[29]

D.J. Tipper, J.L. Strominger, Mechanism of action of penicillins: a proposal based on their structural similarity to acyl-D-alanyl-D-alanine, Proc. Natl. Acad. Sci. U.S.A. 54 (1965) 1133-1141. https://doi.org/10.1073/pnas.54.4.1133.

[30]

H. Brötz, M. Josten, I. Wiedemann, et al., Role of lipid-bound peptidoglycan precursors in the formation of pores by nisin, epidermin and other lantibiotics, Mol. Microbiol. 30 (1998) 317-327. https://doi.org/10.1046/j.1365-2958.1998.01065.x.

[31]

S. Brown, J.P. Santa Maria, S. Walker, Wall teichoic acids of gram-positive bacteria, Annu. Rev. Microbiol. 67 (2013) 313-336. https://doi.org/10.1146/annurev-micro-092412-155620.

[32]

R. Saar-Dover, A. Bitler, R. Nezer, et al., D-Alanylation of lipoteichoic acids confers resistance to cationic peptides in group B Streptococcus by Increasing the cell wall density, PLoS Pathog. 8 (2012) e1002891. https://doi.org/10.1371/journal.ppat.1002891.

[33]

F.C. Neuhaus, J. Baddiley, A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in Gram-positive bacteria, Microbiol. Mol. Biol. Rev. 67 (2003) 686-723. https://doi.org/10.1128/mmbr.67.4.686-723.2003.

[34]

S. Wu, P.L. Yu, D. Wheeler, et al., Transcriptomic study on persistence and survival of Listeria monocytogenes following lethal treatment with nisin, J. Glob. Antimicrob. Resist. 15 (2018) 25-31. https://doi.org/10.1016/j.jgar.2018.06.003.

[35]

R.M. Epand, C. Walker, R.F. Epand, et al., Molecular mechanisms of membrane targeting antibiotics, Biochim. Biophys. Acta-Biomembr. 1858 (2016) 980-987. https://doi.org/10.1016/j.bbamem.2015.10.018.

[36]

N. Malanovic, K. Lohner, Gram-positive bacterial cell envelopes: the impact on the activity of antimicrobial peptides, Biochim. Biophys. Acta-Biomembr. 1858 (2016) 936-946. https://doi.org/10.1016/j.bbamem.2015.11.004.

[37]

A.L. Davidson, E. Dassa, C. Orelle, et al., Structure, function, and evolution of bacterial ATP-binding cassette systems, Microbiol. Mol. Biol. Rev. 72 (2008) 317-364. https://doi.org/10.1128/mmbr.00031-07.

[38]

R.O. Miranda, M.E.M. Campos-Galvão, L.A. Nero, Expression of genes associated with stress conditions by Listeria monocytogenes in interaction with nisin producer Lactococcus lactis, Food Res. Int. 105 (2018) 897-904. https://doi.org/10.1016/j.foodres.2017.12.030.

[39]

M. Panhorst, U. Sorger-Herrmann, V.F. Wendisch, The pstSCAB operon for phosphate uptake is regulated by the global regulator GlxR in Corynebacterium glutamicum, J. Biotechnol. 154 (2011) 149-155. https://doi.org/10.1016/j.jbiotec.2010.07.015.

[40]

X. Wang, X. Cai, H. Ma, et al., A c-di-AMP riboswitch controlling kdpFABC operon transcription regulates the potassium transporter system in Bacillus thuringiensis, Commun. Biol. 2 (2019) 151. https://doi.org/10.1038/s42003-019-0414-6.

[41]

G. Liu, G. Ren, L. Zhao, et al., Antibacterial activity and mechanism of bifidocin A against Listeria monocytogenes, Food Control 73 (2017) 854-861. https://doi.org/10.1016/j.foodcont.2016.09.036.

[42]

G. Andrew Woolley, B.A. Wallace, Model ion channels: gramicidin and alamethicin, J. Membr. Biol. 129 (1992) 109-136. https://doi.org/10.1007/BF00219508.

[43]

S. Varma, D. Sabo, S.B. Rempe, K+/Na+ selectivity in K channels and valinomycin: over-coordination versus cavity-size constraints, J. Mol. Biol. 376 (2008) 13-22. https://doi.org/10.1016/j.jmb.2007.11.059.

[44]

T. Mogi, K. Kita, Gramicidin S and polymyxins: the revival of cationic cyclic peptide antibiotics, Cell Mol. Life Sci. 66 (2009) 3821-3826. https://doi.org/10.1007/s00018-009-0129-9.

[45]

M. Wenzel, A.I. Chiriac, A. Otto, et al., Small cationic antimicrobial peptides delocalize peripheral membrane proteins, Proc. Natl. Acad. Sci. U.S.A. 111 (2014) E1409-E1418. https://doi.org/10.1073/pnas.1319900111.

[46]

Y. Cui, Y. Zhao, Y. Tian, et al., The molecular mechanism of action of bactericidal gold nanoparticles on Escherichia coli, Biomaterials 33 (2012) 2327-2333. https://doi.org/10.1016/j.biomaterials.2011.11.057.

[47]

M. Aboulwafa, M.H. Saier, Dependency of sugar transport and phosphorylation by the phosphoenolpyruvate-dependent phosphotransferase system on membranous phosphatidyl glycerol in Escherichia coli: studies with a pgsA mutant lacking phosphatidyl glycerophosphate synthase, Res. Microbiol. 153 (2002) 667-677. https://doi.org/10.1016/S0923-2508(02)01376-1.

[48]

T. Shireen, A. Basu, M. Sarkar, et al., Lipid composition is an important determinant of antimicrobial activity of alpha-melanocyte stimulating hormone, Biophys. Chem. 196 (2015) 33-39. https://doi.org/10.1016/j.bpc.2014.09.002.

[49]

V. Sourjik, H.C. Berg, Functional interactions between receptors in bacterial chemotaxis, Nature 428 (2004) 437-441. https://doi.org/10.1038/nature02406.

[50]

J. Guo, X. Hu, Z. Gao, et al., Global transcriptomic response of Listeria monocytogenes exposed to Fingered Citron (Citrus medica L. var. sarcodactylis Swingle) essential oil, Food Res. Int. 143 (2021) 110274. https://doi.org/10.1016/j.foodres.2021.110274.

[51]

S.T. Rutherford, B.L. Bassler, Bacterial quorum sensing: its role in virulence and possibilities for its control, Cold Spring Harb. Perspect. Med. 2 (2012) a012427. https://doi.org/10.1101/cshperspect.a012427.

[52]

P. Piewngam, Y. Zheng, T.H. Nguyen, et al., Pathogen elimination by probiotic Bacillus via signalling interference, Nature 562 (2018) 532-537. https://doi.org/10.1038/s41586-018-0616-y.

[53]

S.M. McBride, A.L. Sonenshein, The dlt operon confers resistance to cationic antimicrobial peptides in Clostridium difficile, Microbiology 157 (2011) 1457-1465. https://doi.org/10.1099/mic.0.045997-0.

[54]

T. Mascher, S.L. Zimmer, T.A. Smith, et al., Antibiotic-inducible promoter regulated by the cell envelope stress-sensing two-component system LiaRS of Bacillus subtilis, Antimicrob. Agents Chemother. 48 (2004) 2888-2896. https://doi.org/10.1128/AAC.48.8.2888-2896.2004.

[55]

A. Khan, M. Davlieva, D. Panesso, et al., Antimicrobial sensing coupled with cell membrane remodeling mediates antibiotic resistance and virulence in Enterococcus faecalis, Proc. Natl. Acad. Sci. U.S.A. 116 (2019) 26925-26932. https://doi.org/10.1073/pnas.1916037116.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 07 September 2021
Revised: 27 September 2021
Accepted: 11 October 2021
Published: 18 November 2022
Issue date: July 2023

Copyright

© 2023 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.

Acknowledgements

Acknowledgements

This research was financially supported by the National Natural Science Foundation of China (31771951, 32072199, 31801510); the Beijing Natural Science Foundation (KZ201810011016).

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return