Riboflavin-mediated extracellular electron transfer enhances microbiologically influenced corrosion of 316L stainless steel by Listeria monocytogenes
Source abstract
Abstract
316L stainless steel (SS) is commonly used in medical implants due to its outstanding mechanical properties and biocompatibility. However, increasing use of metallic implants has raised concerns about microbiologically influenced corrosion (MIC) in intestinal environments. This study presents the first evidence that Listeria monocytogenes can induce significant MIC on 316L SS under simulated intestinal conditions. L. monocytogenes forms dense biofilms on metal surfaces, accelerating corrosion and causing severe pitting. Corrosion rates are further heightened under carbon starvation, indicating extracellular electron transfer (EET) involvement. Electrochemical analyses reveal that L. monocytogenes disrupts the protective oxide layer via a riboflavin-mediated EET pathway. Riboflavin intensifies corrosion by enhancing electron transfer between bacteria and metal surfaces. These results highlight the critical role of EET in L. monocytogenes -induced MIC and provide new insights into corrosion mechanisms of metallic implants in intestinal environments, laying the foundations for developing corrosion-resistant biomaterials and protective strategies.
Source: openalex_inverted_index · Quality: baseline
Research context
OpenAlex topics: Corrosion Behavior and Inhibition · Hydrogen embrittlement and corrosion behaviors in metals · Magnesium Alloys: Properties and Applications
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (63)
Show source-provided references
1. Pal, M. K. & Lavanya, M. Microbial influenced corrosion: understanding bioadhesion and biofilm formation. J. Bio- Tribo-Corros. 8, 76 (2022).10.1007/s40735-022-00677-x ↗
2. Lv, M. & Du, M. A review: microbiologically influenced corrosion and the effect of cathodic polarization on typical bacteria. Rev. Environ. Sci. Biotechnol. 17, 431–446 (2018).10.1007/s11157-018-9473-2 ↗
3. Little, B. J. et al. Microbially influenced corrosion—Any progress?. Corros. Sci. 170, 108641 (2020).10.1016/j.corsci.2020.108641 ↗
4. Jia, R., Unsal, T., Xu, D., Lekbach, Y. & Gu, T. Microbiologically influenced corrosion and current mitigation strategies: a state of the art review. Int. Biodeterior. Biodegrad. 137, 42–58 (2019).10.1016/j.ibiod.2018.11.007 ↗
5. Knisz, J. et al. Microbiologically influenced corrosion—more than just microorganisms. FEMS Microbiol. Rev. 47, fuad041 (2023).10.1093/femsre/fuad041 ↗
6. Maji, K. & Lavanya, M. Microbiologically influenced corrosion in stainless steel by Pseudomonas aeruginosa: an overview. J. Bio Tribo Corros. 10, 16 (2024).10.1007/s40735-024-00820-w ↗
7. Mystkowska, J. et al. The role of oral cavity biofilm on metallic biomaterial surface destruction–corrosion and friction aspects. Int. J. Mol. Sci. 19, 743 (2018).10.3390/ijms19030743 ↗
8. Sharma, P. et al. Alternative uses of lumen apposing metal stents. World J. Gastroenterol. 26, 2715 (2020).10.3748/wjg.v26.i21.2715 ↗
9. Li, H. & Cong, Y. Past and recent progress on metallic digestive tract stents. ACS Appl. Bio Mater. 7, 7088–7100 (2024).10.1021/acsabm.4c00823 ↗
10. Wongpanya, P., Siritapetawee, J., Wongpinij, T. & Photongkam, P. Effect of antiplatelet drugs on corrosion of 316L stainless steel for application to biomaterials. Mater. Chem. Phys. 278, 125596 (2022).10.1016/j.matchemphys.2021.125596 ↗
11. Korei, N., Solouk, A., Nazarpak, M. H. & Nouri, A. A review on design characteristics and fabrication methods of metallic cardiovascular stents. Mater. Today Commun. 31, 103467 (2022).10.1016/j.mtcomm.2022.103467 ↗
12. Beshchasna, N. et al. Recent advances in manufacturing innovative stents. Pharmaceutics 12, 349 (2020).10.3390/pharmaceutics12040349 ↗
13. Zheng, Y. et al. Accelerated corrosion of 316L stainless steel in a simulated oral environment via extracellular electron transfer and acid metabolites of subgingival microbiota. Bioact. Mater. 35, 56–66 (2024).
14. Eduok, U. Microbiologically induced intergranular corrosion of 316L stainless steel dental material in saliva. Mater. Chem. Phys. 313, 128799 (2024).10.1016/j.matchemphys.2023.128799 ↗
15. Mystkowska, J., Łysik, D. & Klekotka, M. Effect of saliva and mucin-based saliva substitutes on fretting processes of 316 austenitic stainless steel. Metals 9, 178 (2019).10.3390/met9020178 ↗
16. Wang, Q. et al. Oral microbiota accelerates corrosion of 316L stainless steel for orthodontic applications. J. Mater. Sci. Technol. 128, 118–132 (2022).10.1016/j.jmst.2022.04.012 ↗
17. Yang, Y. et al. Streptococcus mutans biofilms induce metabolite-mediated corrosion of 316 L stainless steel in a simulated oral environment. Corros. Sci. 182, 109286 (2021).10.1016/j.corsci.2021.109286 ↗
18. Xu, W. et al. Microbial corrosion of metallic biomaterials in the oral environment. Acta Biomater. 184, 22–36 (2024).10.1016/j.actbio.2024.06.032 ↗
19. Zhu, B., Wang, X. & Li, L. Human gut microbiome: the second genome of human body. Protein Cell 1, 718–725 (2010).10.1007/s13238-010-0093-z ↗
20. Rago, L., Popp, D., Heiker, J. T. & Harnisch, F. Electroactive microorganisms in mouse feces. Electrochim. Acta 365, 137326 (2021).10.1016/j.electacta.2020.137326 ↗
21. Schwab, L., Rago, L., Koch, C. & Harnisch, F. Identification of Clostridium cochlearium as an electroactive microorganism from the mouse gut microbiome. Bioelectrochemistry 130, 107334 (2019).10.1016/j.bioelechem.2019.107334 ↗
22. Quereda, J. J. et al. Pathogenicity and virulence of Listeria monocytogenes: A trip from environmental to medical microbiology. Virulence 12, 2509–2545 (2021).10.1080/21505594.2021.1975526 ↗
23. Light, S. H. et al. A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. Nature 562, 140–144 (2018).10.1038/s41586-018-0498-z ↗
24. Radoshevich, L. & Cossart, P. Listeria monocytogenes: towards a complete picture of its physiology and pathogenesis. Nat. Rev. Microbiol. 16, 32–46 (2018).10.1038/nrmicro.2017.126 ↗
25. Lovley, D. R. & Holmes, D. E. Electromicrobiology: the ecophysiology of phylogenetically diverse electroactive microorganisms. Nat. Rev. Microbiol. 20, 5–19 (2022).10.1038/s41579-021-00597-6 ↗
26. Li, J., Liu, Z., Lou, Y., Du, C. & Li, X. Evidencing the uptake of electrons from X80 steel by Bacillus licheniformis with redox probe, 5-cyano-2,3-ditolyl tetrazolium chloride. Corros. Sci. 168, 108569 (2020).10.1016/j.corsci.2020.108569 ↗
27. Kato, S. Microbial extracellular electron transfer and its relevance to iron corrosion. Microb. Biotechnol. 9, 141–148 (2016).10.1111/1751-7915.12340 ↗
28. Li, Z. et al. Adaptive bidirectional extracellular electron transfer during accelerated microbiologically influenced corrosion of stainless steel. Commun. Mater. 2, 67 (2021).10.1038/s43246-021-00173-8 ↗
29. Stewart, P. S. & Franklin, M. J. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6, 199–210 (2008).10.1038/nrmicro1838 ↗
30. Gu, T., Wang, D., Lekbach, Y. & Xu, D. Extracellular electron transfer in microbial biocorrosion. Curr. Opin. Electrochem. 29, 100763 (2021).10.1016/j.coelec.2021.100763 ↗
31. Deng, X., Dohmae, N., Kaksonen, A. H. & Okamoto, A. Biogenic iron sulfide nanoparticles to enable extracellular electron uptake in sulfate-reducing bacteria. Angew. Chem. 132, 6051–6055 (2020).10.1002/ange.201915196 ↗
32. Xu, D. & Gu, T. Carbon source starvation triggered more aggressive corrosion against carbon steel by the Desulfovibrio vulgaris biofilm. Int. Biodeterior. Biodegrad. 91, 74–81 (2014).10.1016/j.ibiod.2014.03.014 ↗
33. Lazanas, A. C. & Prodromidis, M. I. Electrochemical Impedance Spectroscopy─A Tutorial. ACS Meas. Sci. Au 3, 162–193 (2023).10.1021/acsmeasuresciau.2c00070 ↗
34. Zhao, J. et al. Microbial extracellular electron transfer and strategies for engineering electroactive microorganisms. Biotechnol. Adv. 53, 107682 (2021).10.1016/j.biotechadv.2020.107682 ↗
35. Zhang, J., Li, F., Liu, D., Liu, Q. & Song, H. Engineering extracellular electron transfer pathways of electroactive microorganisms by synthetic biology for energy and chemicals production. Chem. Soc. Rev. 53, 1375–1446 (2024).10.1039/D3CS00537B ↗
36. Thapa, B. S. et al. Overview of electroactive microorganisms and electron transfer mechanisms in microbial electrochemistry. Bioresour. Technol. 347, 126579 (2022).10.1016/j.biortech.2021.126579 ↗
37. Kitamoto, S., Nagao-Kitamoto, H., Hein, R., Schmidt, T. M. & Kamada, N. The bacterial connection between the oral cavity and the gut diseases. J. Dent. Res. 99, 1021–1029 (2020).10.1177/0022034520924633 ↗
38. Raheem, A., Liang, L., Zhang, G. & Cui, S. Modulatory effects of probiotics during pathogenic infections with emphasis on immune regulation. Front. Immunol. 12, 616713 (2021).10.3389/fimmu.2021.616713 ↗
39. Renier, S., Hébraud, M. & Desvaux, M. Molecular biology of surface colonization by Listeria monocytogenes: an additional facet of an opportunistic Gram-positive foodborne pathogen. Environ. Microbiol. 13, 835–850 (2011).10.1111/j.1462-2920.2010.02378.x ↗
40. Hamon, M., Bierne, H. & Cossart, P. Listeria monocytogenes: a multifaceted model. Nat. Rev. Microbiol. 4, 423–434 (2006).10.1038/nrmicro1413 ↗
41. Gopalakrishnan, U. et al. Assessing the potential association between microbes and corrosion of intra-oral metallic alloy-based dental appliances through a systematic review of the literature. Front. Bioeng. Biotechnol. 9, 631103 (2021).10.3389/fbioe.2021.631103 ↗
42. Morgan, R. & Adam, A. Use of metallic stents and balloons in the esophagus and gastrointestinal tract. J. Vasc. Interv. Radiol. 12, 283–297 (2001).10.1016/S1051-0443(07)61906-X ↗
43. Telegdi, J., Shaban, A. & Trif, L. Review on the microbiologically influenced corrosion and the function of biofilms. Int. J. Corros. Scale Inhib. 9, 1–33 (2020).
44. Kumar, R., Singh, L., Wahid, Z. A. & Din, M. F. M. Exoelectrogens in microbial fuel cells toward bioelectricity generation: a review. Int. J. Energy Res. 39, 1048–1067 (2015).10.1002/er.3305 ↗
45. Gu, T., Jia, R., Unsal, T. & Xu, D. Toward a better understanding of microbiologically influenced corrosion caused by sulfate reducing bacteria. J. Mater. Sci. Technol. 35, 631–636 (2019).10.1016/j.jmst.2018.10.026 ↗
46. Yi, Y., Zhao, T., Zang, Y., Xie, B. & Liu, H. Different mechanisms for riboflavin to improve the outward and inward extracellular electron transfer of Shewanella loihica. Electrochem. Commun. 124, 106966 (2021).10.1016/j.elecom.2021.106966 ↗
47. Wang, D. et al. Aggressive corrosion of carbon steel by Desulfovibrio ferrophilus IS5 biofilm was further accelerated by riboflavin. Bioelectrochemistry 142, 107920 (2021).10.1016/j.bioelechem.2021.107920 ↗
48. Abdali, A., Hossein Nedjad, S., Hamed Zargari, H., Saboori, A. & Yildiz, M. Predictive tools for the cooling rate-dependent microstructure evolution of AISI 316L stainless steel in additive manufacturing. J. Mater. Res. Technol. 29, 5530–5538 (2024).10.1016/j.jmrt.2024.03.008 ↗
49. Lin, W. et al. Long-term in vivo corrosion behavior, biocompatibility and bioresorption mechanism of a bioresorbable nitrided iron scaffold. Acta Biomater. 54, 454–468 (2017).10.1016/j.actbio.2017.03.020 ↗
50. Wang, J. et al. EGCG regulates cell apoptosis of human umbilical vein endothelial cells grown on 316L stainless steel for stent implantation. Drug Des. Dev. Ther. 15, 493–499 (2021).10.2147/DDDT.S296548 ↗
51. Gomaa, E. Z. Antimicrobial activity of a biosurfactant produced by Bacillus licheniformis strain M104 grown on whey. Afr. J. Microbiol. Res. 6, 4396–4403 (2012).
52. Li, Z. et al. Carbon source starvation of a sulfate-reducing bacterium–elevated MIC deterioration of tensile strength and strain of X80 pipeline steel. Front. Mater. 8, 794051 (2021).10.3389/fmats.2021.794051 ↗
53. Dou, W. et al. Electrochemical investigation of increased carbon steel corrosion via extracellular electron transfer by a sulfate reducing bacterium under carbon source starvation. Corros. Sci. 150, 258–267 (2019).10.1016/j.corsci.2019.02.005 ↗
54. Du, Y. et al. Surface nanocoating-based universal platform for programmed delivery of microorganisms in complicated digestive tract. J. Colloid Interface Sci. 673, 765–780 (2024).10.1016/j.jcis.2024.06.093 ↗
55. Faizan, M. et al. Incorporation of Silane-Modified Halloysite into hydrogels for Cefaclor drug Release: Potential for wound healing application. Inorg. Chem. Commun. 163, 112351 (2024).10.1016/j.inoche.2024.112351 ↗
56. Cao, H. et al. Performance of bioelectrode based on different carbon materials in bioelectrochemical anaerobic digestion for methanation of maize straw. Sci. Total Environ. 832, 154997 (2022).10.1016/j.scitotenv.2022.154997 ↗
57. Nguyen, H. T. T., Noori, M. T. & Min, B. Accelerating anaerobic digestion process with novel single chamber microbial electrochemical systems with baffle. Bioresour. Technol. 359, 127474 (2022).10.1016/j.biortech.2022.127474 ↗
58. Flitt, H. J. & Schweinsberg, D. P. Evaluation of corrosion rate from polarisation curves not exhibiting a Tafel region. Corros. Sci. 47, 3034–3052 (2005).10.1016/j.corsci.2005.06.014 ↗
59. Puig-Collderram, B. et al. ATP Bioluminescence Assay To Evaluate Antibiotic Combinations against Extensively Drug-Resistant (XDR) Pseudomonas aeruginosa. Microbiol. Spectr. 10, e00651–00622 (2022).10.1128/spectrum.00651-22 ↗
60. Zhao, H. et al. Improved corrosion resistance and biofilm inhibition ability of copper-bearing 304 stainless steel against oral microaerobic Streptococcus mutans. J. Mater. Sci. Technol. 66, 112–120 (2021).10.1016/j.jmst.2020.06.027 ↗
61. Hanlon, D. N., Todd, I., Peekstok, E., Rainforth, W. M. & Van Der Zwaag, S. The application of laser scanning confocal microscopy to tribological research. Wear 251, 1159–1168 (2001).10.1016/S0043-1648(01)00727-X ↗
62. Li, Z. et al. Rhamnolipid as an eco-friendly corrosion inhibitor for microbiologically influenced corrosion. Corros. Sci. 204, 110390 (2022).10.1016/j.corsci.2022.110390 ↗
63. Da Silva, N. S. et al. Corrosion Properties and Surface Chemistry of Graphene Oxide-Coated AZ91D Magnesium Alloy in Sodium Chloride Solution. Metals 14, 1019 (2024).10.3390/met14091019 ↗