Skip to main content

Advertisement

SpringerLink
Log in

AHLs-produced bacteria in refrigerated shrimp enhanced the growth and spoilage ability of Shewanella baltica

  • Original Article
  • Published:
Journal of Food Science and Technology Aims and scope Submit manuscript

Abstract

Shewanella baltica is the predominant bacteria in spoiled shrimp (Litopenaeus vannamei), however, the spoilage ability and the mechanism of S. baltica is still unknown. S. baltica can’t produce the signal molecule of acyl-homoserine-lactones (AHLs), so the aim of this study was to investigate how wild type S. baltica SA03 (WT SA03) eavesdrop exogenous AHLs to enhance its spoilage ability through LuxR receptor. The results indicated that Aeromonas spp. (Aer), Acinetobacter spp. (Aci) and Serratia spp. (Ser) isolated from refrigerated shrimp can produce different AHLs. WT SA03 can eavesdrop the AHLs of Aer (C4-HSL), Aci (O-C6-HSL) and Ser (C6-HSL, O-C6-HSL) to enhance its growth, especially Ser. Exogenous C4-HSL and C6-HSL enhanced biofilm formation of WT SA03, and C6-HSL and O-C6-HSL enhanced thioredoxin reductase trxB mRNA expression. However, the luxR mutant of WT SA03 (ΔluxR SA03) lost or weakened the role of using environmental AHLs. In vivo experiments, the lag time of WT SA03 was shortened by 6.4 h, 6.2 h and 14.4 h by co-inoculated with Aer, Aci and Ser, respectively. The total volatile basic nitrogen (TVB-N) were significantly enhanced in the samples co-inoculated with WT SA03 and Aer (or Aci, Ser) than those of ΔluxR SA03 and Aer (or Aci, Ser) (p < 0.05). The results showed that S. baltica SA03 can utilize AHLs produced by other bacteria to enhance its growth and spoilage ability through LuxR receptor system. Quorum sensing based on AHLs of bacteria might as the potential targets for food spoilage control.

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

Similar content being viewed by others

Abbreviations

WT SA03:

Wild type Shewanella baltica SA03

ΔluxR SA03:

The luxR mutant of Shewanella baltica SA03

Aer:

Aeromonas spp.

Aci:

Acinetobacter spp.

Ser:

Serratia spp.

C4-HSL:

N-butanoyl-l-homoserine lactone

C6-HSL:

N-hexanoyl-l-homoserine lactone

C8-HSL:

N-3-hydroxyoctanoyl-l-homoserine lactone

O-C6-HSL:

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

O-C8-HSL:

N-(3-oxo hydroxyoctanoyl)-l-homoserine lactone

References

  • Botta JR, Lauder JT, Jewer MA (1984) Effect of methodology on total volatile basic nitrogen (TVB-N) determination as an index of quality of fresh atlantic cod (Gadus morhua). J Food Sci 49:734–736

    Article  CAS  Google Scholar 

  • Bruhn JB, Christensen AB, Flodgaard LR, Nielsen KF, Larsen TO, Givskov M, Gram L (2004) Presence of acylated homoserine lactones (AHLs) and AHL-producing bacteria in meat and potential role of AHL in spoilage of meat. Appl Environ Microbiol 70:4293–4302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christensen AB, Riedel K, Eberl L, Flodgaard LR, Molin S, Gram L, Givskov M (2003) Quorum-sensing-directed protein expression in Serratia proteamaculans B5a. Microbiology 149:471–483

    Article  CAS  Google Scholar 

  • Fonnesbech VB, Venkateswaran K, Satomi M, Gram L (2005) Identification of Shewanella baltica as the most important H2S-producing species during iced storage of danish marine fish. Appl Environ Microbiol 71:6689–6697

    Article  CAS  Google Scholar 

  • Fu L, Wang C, Liu N, Ma A, Wang Y (2018) Quorum sensing system-regulated genes affect the spoilage potential of Shewanella baltica. Food Res Int 107:1–9

    Article  CAS  PubMed  Google Scholar 

  • Gu Q, Fu L, Wang Y, Lin J (2013) Identification and characterization of extracellular cyclic dipeptides as quorum-sensing signal molecules from Shewanella baltica, the specific spoilage organism of Pseudosciaena crocea during 4°C storage. J Agric Food Chem 61:11645–11652

    Article  CAS  PubMed  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108

    Article  CAS  Google Scholar 

  • Hudaiberdiev S, Choudhary KS, Alvarez RV, Gelencsér Z, Ligeti B, Lamba D, Pongor S (2015) Census of solo LuxR genes in prokaryotic genomes. Front Cell Infect Microbiol 5:1–6

    Article  CAS  Google Scholar 

  • Jie J, Yu H, Han Y, Liu Z, Zeng M (2018) Acyl-homoserine-lactones receptor LuxR of Shewanella baltica involved in the development of microbiota and spoilage of refrigerated shrimp. J Food Sci Technol 55:2795–2800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawaguchi T, Chen YP, Norman RS, Decho AW (2008) Rapid screening of quorum-sensing signal N-acyl homoserine lactones by an in vitro cell-free assay. Appl Environ Microbiol 74:3667–3671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Park W (2013) Identification and characterization of genes regulated by AqsR, a LuxR-type regulator in Acinetobacter oleivorans DR1. Appl Microbiol Biotechnol 97:6967–6978

    Article  CAS  PubMed  Google Scholar 

  • Martínez P, Huedo P, Martinezservat S, Planell R, Ferrernavarro M, Daura X, Yero D, Gibert I (2015) Stenotrophomonas maltophilia responds to exogenous AHL signals through the LuxR solo SmoR (Smlt1839). Front Cell Infect Microbiol 5:1–13

    Google Scholar 

  • Patel HK, Ferrante P, Covaceuszach S, Lamba D, Scortichini M, Venturi V (2014) The kiwifruit emerging pathogen Pseudomonas syringae pv. actinidiae does not produce AHLs but possesses three LuxR solos. PLoS ONE 9:e87862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ravn FL, Christensen AB, Molin S, Givskov M, Gram L (2003) Influence of food preservation parameters and associated microbiota on production rate, profile and stability of acylated homoserine lactones from food-derived Enterobacteriaceae. Int J Food Microbiol 84:145–156

    Article  CAS  Google Scholar 

  • Remya S, Mohan CO, Venkateshwarlu G, Sivaraman GK, Ravishankar CN (2017) Combined effect of O2 scavenger and antimicrobial film on shelf life of fresh cobia (Rachycentron canadum) fish steaks stored at 2°C. Food Control 71:71–78

    Article  CAS  Google Scholar 

  • Rul F, Monnet V (2015) How microbes communicate in food: a review of signaling molecules and their impact on food quality. Curr Opin Food Sci 2:100–105

    Article  Google Scholar 

  • Smith JL, Fratamico PM, Yan X (2011) Eavesdropping by bacteria: the role of SdiA in Escherichia coli and Salmonella enterica serovar typhimurium quorum sensing. Foodborne Pathog Dis 8:169–178

    Article  CAS  PubMed  Google Scholar 

  • Subramoni S, Venturi V (2009) PpoR is a conserved unpaired LuxR solo of Pseudomonas putida which binds N-acyl homoserine lactones. BMC Microbiol 9:1–15

    Article  CAS  Google Scholar 

  • Sun X, Zhang C, Zhu S, Zeng M (2015) Isolation, identification and regulation of quorum sensing signal molecules of Acinetobacter in Litopenaeus vannamei. Microbiol China 42:437–443

    CAS  Google Scholar 

  • Wang H, Liu X, Zhang Y, Lu H, Xu Q, Shi C, Luo Y (2016) Spoilage potential of three different bacteria isolated from spoiled grass carp (Ctenopharyngodon idellus) fillets during storage at 4°C. LWT Food Sci Technol 81:10–17

    Article  CAS  Google Scholar 

  • Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Ye K, Wang H, Xiao H, Xu X, Zhou G (2014) Inhibition of biofilm formation of Pseudomonas aeruginosa by an acylated homoserine lactones-containing culture extract. LWT Food Sci Technol 57:230–235

    Article  CAS  Google Scholar 

  • Zhang C, Zhu S, Jatt AN, Zeng M (2016) Characterization of N-acyl homoserine lactones (AHLs) producing bacteria isolated from vacuum-packaged refrigerated turbot (Scophthalmus maximus) and possible influence of exogenous AHLs on bacterial phenotype. J Gen Appl Microbiol 62:60–67

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Zhu S, Jatt AN, Pan Y, Zeng M (2017) Proteomic assessment of the role of N-acyl homoserine lactone in Shewanella putrefaciens spoilage. Lett Appl Microbiol 65:388–394

    Article  CAS  PubMed  Google Scholar 

  • Zhao D, Fei L, Liu S, Zhang J, Ding Y, Chen W, Zhou X (2018) Involvement of bacterial quorum sensing signals in spoilage potential of Aeromonas veronii bv. veronii isolated from fermented surimi. J Food Biochem 42:e12487

    Article  CAS  Google Scholar 

  • Zhu S, Wu H, Zeng M, Liu Z, Wang Y (2015) The involvement of bacterial quorum sensing in the spoilage of refrigerated Litopenaeus vannamei. Int J Food Microbiol 192:26–33

    Article  CAS  PubMed  Google Scholar 

  • Zhu S, Wu H, Zhang C, Jie J, Liu Z, Zeng M, Wang C (2018) Spoilage of refrigerated Litopenaeus vannamei: eavesdropping on Acinetobacter acyl-homoserine lactones promotes the spoilage potential of Shewanella baltica. J Food Sci Technol 55:1903–1912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zwietering MH, Jongenburger I, Rombouts FM, Van’t RK (1990) Modeling of the bacterial growth curve. Appl Environ Microbiol 56:1875–1881

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (No. 31671919) and Key Projects of Ningbo Agricultural Science and Technology (2017C110006).

Author information

Author notes

  1. Honglei Yu and Jianpeng Li have contributed equally to the work and should be considered joint first authors.

Authors and Affiliations

  1. College of Food Science and Engineering, Ocean University of China, 5 Yushan Road, Qingdao, 266003, China

    Honglei Yu, Jianpeng Li, Yunyan Han, Guocui Shi, Zunying Liu & Mingyong Zeng

Authors
  1. Honglei Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianpeng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yunyan Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guocui Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zunying Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mingyong Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zunying Liu or Mingyong Zeng.

Ethics declarations

Conflict of interest

The authors declared that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, H., Li, J., Han, Y. et al. AHLs-produced bacteria in refrigerated shrimp enhanced the growth and spoilage ability of Shewanella baltica. J Food Sci Technol 56, 114–121 (2019). https://doi.org/10.1007/s13197-018-3464-8

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-018-3464-8

Keywords

Search

Navigation