Skip to main content
SpringerLink
Log in

Inhibitory effects of hexanal on acylated homoserine lactones (AHLs) production to disrupt biofilm formation and enzymes activity in Erwinia carotovora and Pseudomonas fluorescens

  • ORIGINAL ARTICLE
  • Published:
Journal of Food Science and Technology Aims and scope Submit manuscript

Abstract

Erwinia carotovora and Pseudomonas fluorescens were two bacteria commonly caused the spoilage of vegetables through biofilm formation and secretion of extracellular enzymes. In this study, N-(3-oxohexanoyl)-L-homoserine lactone (3-oxo-C6-HSL) and N-Octanoyl-L-homoserine lactone (C8-HSL) were confirmed as acylated homoserine lactones (AHLs) signal molecule produced by E. carotovora and P. fluorescens, respectively. In addition, quorum sensing inhibitory (QSI) effects of hexanal on AHLs production were evaluated. Hexanal at 1/2 minimum inhibitory concentration (MIC) was achieved 76.27% inhibitory rate of 3-oxo-C6-HSL production in E. carotovora and a inhibitory rate of C8-HSL (60.78%) in P. fluorescens. The amount of biofilm formation and activity of extracellular enzymes treated with 1/2 MIC of hexanal were restored with different concentrations (10 ng/mL, 50 ng/mL, 100 ng/mL) of exogenous AHLs (P < 0.05), which verified QSI effect of hexanal on biofilm and extracellular enzymes were due to its inhibition on AHLs production. Molecular docking analysis showed that hexanal could interact with EcbI and PcoI protein to disrupt AHLs production. Furthermore, results showed that sub-MICs of hexanal could suppress expressions of ecbI and pcoI genes in AHL-mediated QS system of E. carotovora and P. fluorescens. This study provides theoretical support for the application of essential oils as QS inhibitors in the preservation of vegetables.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

All data generated or analysed during this study are included in this published article (and its supplementary information files).

Abbreviations

QS:

Quorum sensing

QSI:

Quorum sensing inhibitor

AHLs:

Acylated homoserine lactones

3-oxo-C6-HSL:

N-(3-oxohexanoyl)-L-homoserine lactone

C8-HSL:

N-Octanoyl-L-homoserine lactone

EPS:

Extracellular polymeric substances

ESI:

Electrospray ion source

MIC:

Minimal inhibitory concentration

MRM:

Multiple reaction monitoring

qRT-PCR:

Quantitative Real-Time PCR

References

  • Abbott DW, Boraston AB (2008) Structural biology of pectin degradation by Enterobacteriaceae. Microbiol Mol Biol Rev 72(2):301–316

    Article  CAS  Google Scholar 

  • Al-Shabib NA, Husain FM, Ahmad I, Baig MH (2017) Eugenol inhibits quorum sensing and biofilm of toxigenic MRSA strains isolated from food handlers employed in Saudi Arabia. Biotechnol Biotechnol Equip 31(2):387–396

    Article  CAS  Google Scholar 

  • Ding T, Li T, Li J (2018) Identification of natural product compounds as quorum sensing inhibitors in Pseudomonas fluorescens P07 through virtual screening. Bioorg Med Chem 26(14):4088–4099

    Article  CAS  Google Scholar 

  • Fan X, Ye T, Li Q, Bhatt P, Zhang L, Chen S (2020) Potential of a quorum quenching bacteria isolate Ochrobactrum intermedium D-2 against soft rot pathogen Pectobacterium carotovorum subsp. carotovorum. Front Microbiol 11:898

    Article  Google Scholar 

  • Galloway WRJD, Hodgkinson JT, Bowden SD, Welch M, Spring DR (2011) Quorum sensing in Gram-negative bacteria: small-molecule modulation of AHL and AI-2 quorum sensing pathways. Chem Rev 111(1):28–67

    Article  CAS  Google Scholar 

  • Gram L, Ravn L, Rasch M, Bruhn JB, Christensen AB, Givskov M (2002) Food spoilage—interactions between food spoilage bacteria. Int J Food Microbiol 78(1):79–97

    Article  Google Scholar 

  • Hu H, He J, Liu J, Yu H, Tang J, Zhang J (2016) Role of N-acyl-homoserine lactone (AHL) based quorum sensing on biofilm formation on packing media in wastewater treatment process. RSC Adv 6(14):11128–11139

    Article  CAS  Google Scholar 

  • Joshi J, Burdman S, Lipsky A, Yariv S, Yedidia I (2016) Plant phenolic acids affect the virulence of Pectobacterium aroidearum and P. carotovorum ssp. brasiliense via quorum sensing regulation. Mol Plant Pathol 17(4):487–500

    Article  CAS  Google Scholar 

  • Li T, Wang D, Liu N, Ma Y, Ding T, Mei Y, Li J (2018) Inhibition of quorum sensing-controlled virulence factors and biofilm formation in Pseudomonas fluorescens by cinnamaldehyde. Int J Food Microbiol 269:98–106

    Article  CAS  Google Scholar 

  • Li C, Xie Y, Guo Y, Cheng Y, Yu H, Qian H, Yao W (2021) Effects of ozone-microbubble treatment on the removal of residual pesticides and the adsorption mechanism of pesticides onto the apple matrix. Food Control 120:107548

    Article  CAS  Google Scholar 

  • Liu M, Wang H, Griffiths MW (2007) Regulation of alkaline metalloprotease promoter by N-acyl homoserine lactone quorum sensing in Pseudomonas fluorescens. J Appl Microbiol 103(6):2174–2184

    Article  CAS  Google Scholar 

  • Loper JMC, Joyce E (1998) Ecbl and EcbR: homologs of Luxl and LuxR affecting antibiotic and exoenzyme production by Erwinia carotovora subsp betavasculorum. Can J Microbiol 43(12):1164–1171

    Google Scholar 

  • Ma R, Qiu S, Jiang Q, Sun H, Xue T, Cai G, Sun B (2017) AI-2 quorum sensing negatively regulates rbf expression and biofilm formation in Staphylococcus aureus. Int J Med Microbiol 307(4–5):257–267

    Article  CAS  Google Scholar 

  • Mishra S, Huang Y, Li J, Wu X, Zhou Z, Lei Q, Bhatt P, Chen S (2022) Biofilm-mediated bioremediation is a powerful tool for the removal of environmental pollutants. Chemosphere 294:133609

    Article  CAS  Google Scholar 

  • Morohoshi T, Ogasawara Y, Xie X, Hamamoto H, Someya N (2019) Genetic and biochemical diversity for N-acylhomoserine lactone biosynthesis in the plant pathogen Pectobacterium carotovorum subsp. carotovorum. Microbes Environ 34(4):429–435

    Article  Google Scholar 

  • Myszka K, Olkowicz M, Radziejewska-Kubzdela E, Olejnik-Schmidt AK, Czaczyk K (2015) Impact of bacterial quorum sensing system on changes of organoleptic markers of storage cabbage. J Microbiol Biotechnol Food Sci 4(5):407

    Article  CAS  Google Scholar 

  • Myszka K, Schmidt MT, Majcher M, Juzwa W, Olkowicz M, Czaczyk K (2016) Inhibition of quorum sensing-related biofilm of Pseudomonas fluorescens KM121 by Thymus vulgare essential oil and its major bioactive compounds. Int Biodeterior Biodegradation 114:252–259

    Article  CAS  Google Scholar 

  • Niu C, Gilbert ES (2004) Colorimetric method for identifying plant essential oil components that affect biofilm formation and structure. Appl Environ Microbiol 70(12):6951

    Article  CAS  Google Scholar 

  • Sabidi S, Hoshiko Y, Maeda T (2022) Quorum quenching of autoinducer 2 increases methane production in anaerobic digestion of waste activated sludge. Appl Microbiol Biotechnol 106(12):4763–4774

    Article  CAS  Google Scholar 

  • Sauer K, Rickard AH, Davies DG (2007) Biofilms and biocomplexity. Microbe-Am Soc Microbiol 2(7):347

    Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101–1108

    Article  CAS  Google Scholar 

  • Shi C, Sun Y, Liu Z, Guo D, Sun H, Sun Z, Chen S, Zhang W, Wen Q, Peng X (2017) Inhibition of Cronobacter sakazakii virulence factors by citral. Sci Rep 7:43243

    Article  CAS  Google Scholar 

  • Simões M, Simões LC, Vieira MJ (2010) A review of current and emergent biofilm control strategies. LWT Food Sci Technol 43(4):573–583

    Article  Google Scholar 

  • Tang K, Zhang Y, Yu M, Shi X, Coenye T, Bossier P, Zhang X-H (2013) Evaluation of a new high-throughput method for identifying quorum quenching bacteria. Sci Rep 3:2935

    Article  Google Scholar 

  • Tapia-Rodriguez MR, Hernandez-Mendoza A, Gonzalez-Aguilar GA, Martinez-Tellez MA, Martins CM, Ayala-Zavala JF (2017) Carvacrol as potential quorum sensing inhibitor of Pseudomonas aeruginosa and biofilm production on stainless steel surfaces. Food Control 75:255–261

    Article  CAS  Google Scholar 

  • Truchado P, Gil-Izquierdo A, Tomás-Barberán F, Allende A (2009) Inhibition by chestnut honey of N-acyl-l-homoserine lactones and biofilm formation in Erwinia carotovora, Yersinia enterocolitica, and Aeromonas hydrophila. J Agric Food Chem 57(23):11186–11193

    Article  CAS  Google Scholar 

  • Truchado P, Tomás-Barberán FA, Larrosa M, Allende A (2012) Food phytochemicals act as Quorum sensing inhibitors reducing production and/or degrading autoinducers of Yersinia enterocolitica and Erwinia carotovora. Food Control 24(1–2):78–85

    Article  CAS  Google Scholar 

  • Villa-Rojas R, Zhu M-J, Paul NC, Gray P, Xu J, Shah DH, Tang J (2017) Biofilm forming Salmonella strains exhibit enhanced thermal resistance in wheat flour. Food Control 73:689–695

    Article  CAS  Google Scholar 

  • Von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41:455–482

    Article  Google Scholar 

  • Wang W, Li D, Huang X, Yang H, Qiu Z, Zou L, Liang Q, Shi Y, Wu Y, Wu S, Yang C, Li Y (2019) Study on antibacterial and quorum-sensing inhibition activities of Cinnamomum camphora leaf essential oil. Molecules 24(20):37925

    Article  Google Scholar 

  • Wei HL, Zhang LQ (2006) Quorum-sensing system influences root colonization and biological control ability in Pseudomonas fluorescens 2P24. Antonie Van Leeuwenhoek 89(2):267–280

    Article  Google Scholar 

  • Xue J, Chi L, Tu P, Lai Y, Liu CW, Ru H, Lu K (2021) Detection of gut microbiota and pathogen produced N-acyl homoserine in host circulation and tissues. NPJ Biofilms Microbiomes 7(1):53

    Article  CAS  Google Scholar 

  • Yu Z, Yu D, Mao Y, Zhang M, Ding M, Zhang J, Wu S, Qiu J, Yin J (2019) Identification and characterization of a LuxI/R-type quorum sensing system in Pseudoalteromonas. Res Microbiol 170(6–7):243–255

    Article  CAS  Google Scholar 

  • Yu H, Liu Y, Li L, Guo Y, Xie Y, Cheng Y, Yao W (2020) Ultrasound-involved emerging strategies for controlling foodborne microbial biofilms. Trends Food Sci Technol 96:91–101

    Article  CAS  Google Scholar 

  • Zhang Y, Kong J, Huang F, Xie Y, Guo Y, Cheng Y, Qian H, Yao W (2018a) Hexanal as a QS inhibitor of extracellular enzyme activity of Erwinia carotovora and Pseudomonas fluorescens and its application in vegetables. Food Chem 255:1

    Article  CAS  Google Scholar 

  • Zhang Y, Kong J, Xie Y, Guo Y, Cheng Y, Qian H, Yao W (2018b) Essential oil components inhibit biofilm formation in Erwinia carotovora and Pseudomonas fluorescens via anti-quorum sensing activity. LWT 92:133–139

    Article  CAS  Google Scholar 

  • Zhang Y, Djakpo O, Xie Y, Guo Y, Yu H, Cheng Y, Qian H, Shi R, Yao W (2019a) Anti-quorum sensing of Galla chinensis and Coptis chinensis on bacteria. LWT 101:806–811

    Article  CAS  Google Scholar 

  • Zhang Y, Kong J, Xie Y, Guo Y, Yu H, Cheng Y, Qian H, Shi R, Yao W (2019b) Quorum-sensing inhibition by hexanal in biofilms formed by Erwinia carotovora and Pseudomonas fluorescens. LWT 109:145–152

    Article  CAS  Google Scholar 

  • Zhang W, Fan X, Li J, Ye T, Mishra S, Zhang L, Chen S (2021) Exploration of the quorum-quenching mechanism in Pseudomonas nitroreducens W-7 and its potential to attenuate the virulence of Dickeya zeae EC1. Front Microbiol 12:694161

    Article  Google Scholar 

  • Zhou Z, Wu X, Li J, Zhang Y, Huang Y, Zhang W, Shi Y, Wang J, Chen S (2022) A novel quorum quencher, Rhodococcus pyridinivorans XN-36, is a powerful agent for the biocontrol of soft rot disease in various host plants. Biol Control 169:104889

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Ying Zhang would like to express sincere thanks to Hang Yu for Investigation, Software, Writing review & editing, Yunfei Xie for Project administration, Data curation, Yahui Guo for Investigation, Validation, Yuliang Cheng for Conceptualization, Weirong Yao for Funding acquisition, Supervision.

Funding

The following funding sources are gratefully acknowledged: National Nature Science Foundation of China (32202200), National Key R&D Program of China (2018YFC1602300), Research Fund of Qingdao Special Food Research Institute (66120007), Key R&D Program of Jiangsu Province (BE2019362), China Postdoctoral Science Foundation funded project (2018M642165), the Fundamental Research Funds for the Central Universities (JUSRP11904), the Natural Science Foundation of Jiangsu Province (BK20171139), Forestry science and technology innovation and extension project of Jiangsu Province (No.LYKJ[2017]26), National first-class discipline program of Food Science and Technology (JUFSTR20180509), Science and technology project of Jiangsu Bureau of Quality and Technical Supervision (KJ175923 and KJ185646), and Science and Technology Plan of Suzhou City (SS2019016).

Author information

Authors and Affiliations

  1. School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai, 200093, China

    Ying Zhang

  2. State Key Laboratory of Food Science and Technology, Jiangnan University, No.1800 Lihu Avenue, Wuxi, 214122, Jiangsu Province, China

    Ying Zhang, Hang Yu, Yunfei Xie, Yahui Guo, Yuliang Cheng & Weirong Yao

  3. School of Food Science and Technology, Jiangnan University, No.1800 Lihu Avenue, Wuxi, 214122, Jiangsu Province, China

    Ying Zhang, Hang Yu, Yunfei Xie, Yahui Guo, Yuliang Cheng & Weirong Yao

  4. Joint International Research Laboratory of Food Safety, Jiangnan University, No.1800 Lihu Avenue, Wuxi, 214122, Jiangsu Province, China

    Hang Yu, Yunfei Xie, Yahui Guo, Yuliang Cheng & Weirong Yao

  5. National Center for Technology Innovation On Fast Biological Detection of Grain Quality and Safety, Jiangnan University, No.1800 Lihu Avenue, Wuxi, 214122, Jiangsu Province, China

    Hang Yu, Yunfei Xie, Yahui Guo, Yuliang Cheng & Weirong Yao

Authors
  1. Ying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hang Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yunfei Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yahui Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuliang Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Weirong Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YZ: Writing-original draft, Data curation, Formal analysis. Hang YU: Investigation, Software, Writing-review & editing. YX: Project administration, Data curation. YG: Investigation, Validation. YC: Conceptualization. WY: Funding acquisition, Supervision.

Corresponding author

Correspondence to Weirong Yao.

Ethics declarations

Conflicts of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Consent to participate

All of the authors consent to participate.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 20 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Yu, H., Xie, Y. et al. Inhibitory effects of hexanal on acylated homoserine lactones (AHLs) production to disrupt biofilm formation and enzymes activity in Erwinia carotovora and Pseudomonas fluorescens. J Food Sci Technol 60, 372–381 (2023). https://doi.org/10.1007/s13197-022-05624-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-022-05624-9

Keywords

Search

Navigation