Skip to main content
SpringerLink
Log in

Exogenous autoinducer-2 inhibits biofilm development of Desulfovibrio sp. Huiquan2017

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Sulfate-reducing bacteria (SRB) are culprits for microbiologically influenced corrosion, and biofilms are believed to play essential roles in the corrosion induced by SRB. However, little is known about the regulation of SRB biofilms. Quorum sensing signal molecules acyl-homoserine lactones (AHLs) and autoinducer-2 (AI-2) regulate biofilm formation of many bacteria. In this study, the production of AHLs and AI-2 by one SRB strain, Desulfovibrio sp. Huiquan2017, was detected, and the effect of exogenous AI-2 on bacterial biofilm formation was discussed. It was found that the cell-free supernatants of Desulfovibrio sp. Huiquan2017 induced luminescence in a ∆luxS mutant strain Vibrio harveyi BB170, indicating the production of functional AI-2 by the bacterium. In the presence of exogenous AI-2, the growth of Desulfovibrio sp. Huiquan2017 and early biofilm formation were not affected, but the later stage of biofilm development was inhibited significantly. The biofilms became looser, smaller, and thinner, and contained less bacteria and extracellular polymeric substances (EPS). The inhibition effect of AI-2 on the biofilm development of Desulfovibrio sp. Huiquan2017 was mainly achieved through reducing the amount of EPS in biofilms. These findings shed light on the biofilm regulation of SRB.

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

References

  • Anandkumar B, George RP, Maruthamuthu S, Parvathavarthini N, Mudali UK (2016) Corrosion characteristics of sulfate-reducing bacteria (SRB) and the role of molecular biology in SRB studies: an overview. Corros Rev 34:41–63

    Article  CAS  Google Scholar 

  • Caffrey SM, Park HS, Been J, Gordon P, Sensen CW, Voordouw G (2008) Gene expression by the sulfate-reducing bacterium Desulfovibrio vulgaris hildenborough grown on an iron electrode under cathodic protection conditions. Appl Environ Microb 74:2404–2413

    Article  CAS  Google Scholar 

  • Camesano TA, Logan BE (2000) Probing bacterial electrosteric interactions using atomic force microscopy. Environ Sci Technol 34:3354–3362

    Article  CAS  Google Scholar 

  • Clark ME, Edelmann RE, Duley ML, Wall JD, Fields MW (2007) Biofilm formation in Desulfovibrio vulgaris Hildenborough is dependent upon protein filaments. Environ Microbiol 9:2844–2854

    Article  CAS  Google Scholar 

  • Cornforth DM, Dees JL, Ibberson CB, Huse HK, Mathiesen IH, Kirketerp-Moller K, Wolcott RD, Rumbaugh KP, Bjarnsholt T, Whiteley M (2018) Pseudomonas aeruginosa transcriptome during human infection. Proc Natl Acad Sci USA 115:5125–5134

    Article  Google Scholar 

  • Cuadra GA, Frantellizzi AJ, Gaesser KM, Tammariello SP, Ahmed A (2016) Autoinducer-2 detection among commensal oral streptococci is dependent on pH and boric acid. J Microbiol 54:492–502

    Article  CAS  Google Scholar 

  • Decho AW, Visscher PT, Ferry J, Kawaguchi T, He LJ, Przekop KM, Norman RS, Reid RP (2009) Autoinducers extracted from microbial mats reveal a surprising diversity of N-acylhomoserine lactones (ahls) and abundance changes that may relate to diel pH. Environ Microbiol 11:409–420

    Article  CAS  Google Scholar 

  • Flemming HC (1996) Economical and technical overview. In: Heitz E, Flemming HC, Sand W (eds) Microbially influenced corrosion of materials. Springer Verlag, Berlin, New York, pp 5–14

    Chapter  Google Scholar 

  • Flemming HC, Wuertz S (2019) Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol 17:247–260

    Article  CAS  Google Scholar 

  • Greenberg EP, Hastings JW, Ulitzur S (1979) Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120:87–91

    Article  CAS  Google Scholar 

  • Gu T, Jia R, Unsal T, Xu D (2019) Toward a better understanding of microbiologically influenced corrosion cause by sulfate reducing bacteria. J Mater Sci Technol 4:631–636

    Article  Google Scholar 

  • Irie Y, Parsek MR (2008) Quorum sensing and microbial biofilms. Curr Top Microbiol 322:67–84

    CAS  Google Scholar 

  • Jia R, Unsal T, Xu D, Lekbach Y, Gu T (2019) Microbiologically influenced corrosion and current mitigation strategies: a state of the art review. Internat Biodeter Biodegr 137:42–58

    Article  CAS  Google Scholar 

  • Karatan E, Watnick P (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310–347

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Krumholz LR, Bradstock P, Sheik CS, Diao Y, Gazioglu O, Gorby Y, McInerney MJ (2015) Syntrophic growth of Desulfovibrio alaskensis requires genes for H2 and formate metabolism as well as those for flagellum and biofilm formation. Appl Environ Microbiol 81:2339–2348

    Article  CAS  Google Scholar 

  • Li E, Wu J, Zhang D, Sun Y, Chen J (2018) D-phenylalanine inhibits the corrosion of Q235 carbon steel caused by Desulfovibrio sp. Internat Biodeter Biodegr 127:178–184

    Article  CAS  Google Scholar 

  • Merritt J, Qi F, Goodman SD, Anderson MH (2003) Mutation of luxS affects biofilm formation in Streptococcus mutans. Infect Immun 71:1972–1979

    Article  CAS  Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp 353–355

    Google Scholar 

  • Nazir R, Zaffar MR, Amin I (2019) Bacterial biofilms: the remarkable heterogeneous biological communities and nitrogen fixing microorganisms in lakes. In: Bandh SA, Shafi S, Shameem N (eds) Freshwater microbiology. Academic Press, Pittsburgh, pp 307–340

    Chapter  Google Scholar 

  • Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222

    Article  CAS  Google Scholar 

  • O’Toole GA, Kolter R (1998) The initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis. Mol Microbiol 28:449–461

    Article  Google Scholar 

  • Papenfort K, Bassler B (2016) Quorum-sensing signal-response systems in gram-negative bacteria. Nat Rev Microbiol 14:576–588

    Article  CAS  Google Scholar 

  • Pereira CS, Thompson JA, Xavier KB (2013) AI-2-mediated signalling in bacteria. FEMS Microbiol Rev 37:156–181

    Article  CAS  Google Scholar 

  • Renner LD, Weibel DB (2011) Physicochemical regulation of biofilm formation. MRS Bull 36:347–355

    Article  CAS  Google Scholar 

  • Sakuragi Y, Kolter R (2007) Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J Bacteriol 189:5383–5386

    Article  CAS  Google Scholar 

  • Scarascia G, Wang T, Hong PY (2016) Quorum sensing and the use of quorum quenchers as natural biocides to inhibit sulfate-reducing bacteria. Antibiotics 5:39–58

    Article  Google Scholar 

  • Ustabasi GS, Baysal A (2020) Bacterial interactions of microplastics extracted from toothpaste under controlled conditions and the influence of seawater. Sci Total Environ 703:135024

    Article  CAS  Google Scholar 

  • Vorregaard M (2008) Comstat2-a modern 3D image analysis environment for biofilms. Technical University of Denmark, Denmark

    Google Scholar 

  • Wang S, Payne GF, Bentley WE (2020) Quorum sensing communication: molecularly connecting cells, their neighbors, and even devices. Annu Rev Chem Biomol 11:447–468

    Article  Google Scholar 

  • Wu J, Zhang D, Wang P, Cheng Y, Sun S, Sun Y, Chen S (2016) The influence of Desulfovibrio sp. and Pseudoalteromonas sp. on the corrosion of Q235 carbon steel in natural seawater. Corros Sci 112:552–562

    Article  CAS  Google Scholar 

  • Xavier KB, Bassler BL (2005) Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J Bacteriol 187:238–248

    Article  CAS  Google Scholar 

  • Xu D, Li Y, Gu T (2012a) A synergistic D-tyrosine and tetrakis hydroxymethyl phosphonium sulfate biocide combination for the mitigation of an SRB biofilm. World J Microbiol Biotechnol 28:3067–3074

    Article  CAS  Google Scholar 

  • Xu D, Wen J, Fu W, Gu T, Raad I (2012b) d-amino acids for the enhancement of a binary biocide cocktail consisting of THPS and EDDS against an SRB biofilm. World J Microbiol Biotechnol 28:1641–1646

    Article  CAS  Google Scholar 

  • Zhang M, Sun K, Sun L (2008) Regulation of autoinducer 2 production and luxS expression in a pathogenic Edwardsiella tarda strain. Microbiology 154:2060–2069

    Article  CAS  Google Scholar 

  • Zhang W, Culley DE, Nie L, Scholten JC (2007) Comparative transcriptome analysis of Desulfovibrio vulgaris grown in planktonic culture and mature biofilm on a steel surface. Appl Microbiol Biot 76:447–457

    Article  CAS  Google Scholar 

  • Zhu J, Chai Y, Zhong Z, Li S, Winans SC (2003) Agrobacterium bioassay strain for ultrasensitive detection of n-acylhomoserine lactone-type quorum-sensing molecules: detection of autoinducers in Mesorhizobium huakuii. Appl Environ Microb 69:6949–6953

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China [Grant Nmbers 51771180, 41806087, and U1906226], Key Deployment Project of Center for Ocean Mega-Research of Science, Chinese Academy of Sciences [Grant Number COMS2019Q13], and Key Projects of China National Key Research and Development Plan [Grant Number 2019YFE012026]. We thank Professor Jun Zhu, Huiming Zheng, and Li Sun for friendly providing bacterial reporter strains.

Author information

Authors and Affiliations

  1. Key Laboratory of Marine Environmental Corrosion and Bio-Fouling, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao, 266071, China

    Ee Li, Jiajia Wu & Dun Zhang

  2. Open Studio for Marine Corrosion and Protection, Qingdao National Laboratory for Marine Science and Technology, 1 Wenhai Road, Qingdao, 266237, China

    Ee Li, Jiajia Wu & Dun Zhang

Authors
  1. Ee Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiajia Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Investigation, material preparation, data collection and analysis, and original draft writing were performed by Ee Li. Jiajia Wu contributed to supervision and funding acquisition. Dun Zhang contributed to project administration, supervision, and funding acquisition. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Jiajia Wu or Dun Zhang.

Ethics declarations

Conflicts of interest

The author has no conflicts of interest to declare.

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 2282 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, E., Wu, J. & Zhang, D. Exogenous autoinducer-2 inhibits biofilm development of Desulfovibrio sp. Huiquan2017. World J Microbiol Biotechnol 37, 124 (2021). https://doi.org/10.1007/s11274-021-03071-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-021-03071-w

Keywords

Search

Navigation