Gamma-Polyglutamic Acid Reduces Heavy Metal Uptake and Stabilize Microbial Biosafety in Edible Mushroom Cultures
Source abstract
Abstract
This study evaluated the influence of gamma-polyglutamic acid (γ-PGA) on the heavy metal sorption efficiency of three edible mushroom species—Pleurotus ostreatus, Agaricus bisporus, and Boletus edulis—exposed to cadmium (Cd), lead (Pb), and their mixtures (in a 1:1 ratio). The experiment presented an innovative approach—combining the natural sorption properties of mushrooms with the addition of γ-PGA, which has strong chelating properties. Sorption assays were performed using escalating γ-PGA concentrations (1, 2, and 5 mL to 250 mL of liquid medium), with data analyzed via generalized linear models employing a gamma distribution and a log link function. Results revealed that sorption efficiency was highest at the lowest γ-PGA concentration and decreased significantly with increasing γ-PGA levels across all species and metal treatments. Notably, P. ostreatus and A. bisporus demonstrated superior and more stable sorption capacities relative to B. edulis, which exhibited greater variability. These findings suggest that while edible mushrooms are effective biosorbents for heavy metals, higher γ-PGA concentrations may inhibit metal uptake by chelating metals in solution and reducing their bioavailability. Additionally, γ-PGA at 1 mM markedly enhanced antimicrobial activity against Salmonella enteritidis and Escherichia coli (with a 20% increase in growth inhibition zone compared to the control group) in mushroom cultures and when applied independently. This dual functionality underscores the potential of γ-PGA–mushroom systems for bioremediation and food safety applications, highlighting the need for the careful optimization of γ-PGA concentration to maximize biosorption efficacy and antimicrobial benefits.
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Research context
OpenAlex topics: Biopolymer Synthesis and Applications · Polyamine Metabolism and Applications · biodegradable polymer synthesis and properties
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
Department of Inorganic Chemistry and Pharmaceutical Analytics, Faculty of Pharmacy, Jagiellonian University Medical College, 9 Medyczna Street, 30-688 Kraków, Poland
AGH University of Krakow, Faculty of Materials Science and Ceramics, Department of Analytical Chemistry and Biochemistry, Al. Mickiewicza 30, 30-059 Krakow, Poland
Department of Pharmaceutical Microbiology, Faculty of Pharmacy, Jagiellonian University Medical College, 9 Medyczna Street, 30-688 Krakow, Poland
Department of Microbiology, University Hospital, Marii Orwid 11 Street, 30-680 Krakow, Poland
Doctoral School of Medical and Health Science, Department of Inorganic Chemistry and Pharmaceutical Analytics, Faculty of Pharmacy, Jagiellonian University Medical College, 9 Medyczna Street, 30-688 Kraków, Poland
Department of Medical Plant and Mushroom Biotechnology, Faculty of Pharmacy, Jagiellonian University Medical College, 9 Medyczna Street, 30-688 Kraków, Poland
Biotechnology Centre, Silesian University of Technology, Krzywoustego 8 Street, 44-100 Gliwice, Poland
Funding
Jagiellonian University Medical College’s statutory
References (68)
Show source-provided references
1. Removal of heavy metal ions from wastewaters: A review10.1016/j.jenvman.2010.11.011 ↗
2. Toxicity, mechanism and health effects of some heavy metals10.2478/intox-2014-0009 ↗
3. Bacterial biosorbents and biosorption10.1016/j.biotechadv.2008.02.002 ↗
4. Heavy metal toxicity and the environment
5. Recovery of precious metals through biosorption—A review10.1016/j.hydromet.2010.03.016 ↗
6. Levels of trace elements in the fruiting bodies of macrofungi growing in the East Black Sea region of Turkey10.1016/S0308-8146(98)00194-0 ↗
7. The effect of heavy metals on the growth and accumulation of bioelements and heavy metals in edible mushrooms
8. Biosorption: Critical review of scientific rationale, environmental importance and significance for pollution treatment
9. Biosorption and me: An interview
10. Application of polyglutamic acid in heavy metal removal from aqueous solutions: A review
11. The production and characterization of poly-γ-glutamic acid from microorganisms and its various applications10.1016/S0960-8524(01)00074-8 ↗
12. Poly (γ-glutamic acid)—An emerging biopolymer of commercial interest10.1016/j.biortech.2011.02.047 ↗
13. Soil contamination in China: Current status and mitigation strategies10.1021/es5047099 ↗
14. Kumar, D., and Khan, E.A. (2021). Remediation and detection techniques for heavy metals in the environment. Heavy Metals in the Environment, Elsevier.10.1016/B978-0-12-821656-9.00012-2 ↗
15. Technologies for removing heavy metal from contaminated soils on farmland: A review10.1016/j.chemosphere.2022.135457 ↗
16. Bontà, V., and Calvio, C. (2023). Poly-γ-Glutamic Acid and Its Application in Bioremediation: A Critical Review. Modern Approaches in Waste Bioremediation: Environmental Microbiology, Springer.10.1007/978-3-031-24086-7_11 ↗
17. Ogunleye, A.O. (2015). Bacterial Poly-gamma-glutamic Acid (γ-PGA): A Promising Biosorbent of Heavy Metals. [Ph.D. Thesis, University of Wolverhampton].
18. Poly-γ-glutamic acid, a bio-chelator, alleviates the toxicity of Cd and Pb in the soil and promotes the establishment of healthy Cucumis sativus L. seedling10.1007/s11356-018-1890-9 ↗
19. Sharma, M., Tellili, N., Kacem, I., and Rouissi, T. (2024). Microbial biopolymers: From production to environmental applications—A review. Appl. Sci., 14.10.3390/app14125081 ↗
20. Schill, S., Stessl, B., Meier, N., Tichy, A., Wagner, M., and Ludewig, M. (2021). Microbiological Safety and Sensory Quality of Cultivated Mushrooms (Pleurotus eryngii, Pleurotus ostreatus and Lentinula edodes) at Retail Level and Post-Retail Storage. Foods, 10.10.3390/foods10040816 ↗
21. Salmonella enterica serovar Kedougou contamination of commercially grown mushrooms10.1016/j.diagmicrobio.2004.08.006 ↗
22. High microbial loads found in minimally-processed sliced mushrooms from Italian market
23. Post-harvest treatment with citric acid or hydrogen peroxide to extend the shelf life of fresh sliced mushrooms10.1006/fstl.2000.0657 ↗
24. High relative humidity inpackage of fresh-cut fruits and vegetables: Advantage or disadvantage considering microbiological problems and antimicrobial delivering systems?
25. Microbiological quality of fresh minimally-processed fruit and vegetable, and sprouts from retail estrablishment10.1016/j.ijfoodmicro.2007.12.013 ↗
26. Microbiological quality of some fresh wild edible mushrooms10.3153/FH23029 ↗
27. Sapers, G.M., Gorny, J.R., and Yousef, A.E. (2006). Microbial spoilage of fresh mushrooms. Microbiology of Fruits and Vegetables, CRC Press.10.1201/9781420038934 ↗
28. Su, C., Tseng, C., Wu, S., Shih, B., Chen, Y., and Fang, H. (2019). Poly-Gamma-Glutamic Acid Functions as an Effective Lubricant with Antimicrobial Activity in Multipurpose Contact Lens Care Solutions. Polymers, 11.10.3390/polym11061050 ↗
29. Ajayeoba, T., Dula, S., and Ijabadeniyi, O. (2019). Properties of Poly-γ-Glutamic Acid Producing- Bacillus Species Isolated from Ogi Liquor and Lemon-Ogi Liquor. Front. Microbiol., 16.10.3389/fmicb.2019.00771 ↗
30. Selected edible medicinal mushrooms from Pleurotus genus as an answer for human civilization diseases10.1016/j.foodchem.2020.127084 ↗
31. An integrated strategy for recovery and purification of poly-γ-glutamic acid from fermentation broth and its techno-economic analysis10.1016/j.seppur.2021.119575 ↗
32. Poly-γ-glutamic acid: Production, properties and applications10.1099/mic.0.081448-0 ↗
33. Statistical optimization of fermentation conditions for γ-polyglutamic acid production by Bacillus subtilis NX-2
34. Galvanic current between dental alloys in vitro
35. Modele przewodu pokarmowego in vitro do badań nad biodostępnością składników odżywczych
36. Opoka, W., Muszyńska, B., Rojowski, J., and Rumian, J. (2016). Gastroel–2014. (Poland Patent Application P 417238).
37. Generalized linear models10.2307/2344614 ↗
38. McCullagh, P., and Nelder, J.A. (1989). Generalized Linear Models, Chapman and Hall/CRC. [2nd ed.].10.1007/978-1-4899-3242-6 ↗
39. Byers, S. (2010). Biostatistics with R: An Introduction to Statistics Through Biological Data, Wiley.
40. Dobson, A.J., and Barnett, A.G. (2008). An Introduction to Generalized Linear Models, Chapman and Hall/CRC. [3rd ed.].10.1201/9780367807849 ↗
41. Removal of heavy metals by adsorption on Pleurotus ostreatus10.1016/j.biombioe.2010.12.035 ↗
42. Zaidi, A., Oves, M., Ahmad, E., and Khan, M.S. (2011). Importance of free-living fungi in heavy metal remediation. Biomanagement of Metal-Contaminated Soils, Springer.10.1007/978-94-007-1914-9_21 ↗
43. Metals of King Bolete (Boletus edulis) Bull.: Fr. collected at the same site over two years
44. Falandysz, J. (2021). Nutritional and other trace elements and their associations in raw King Bolete mushrooms, Boletus edulis. Int. J. Environ. Res. Public Health, 19.10.3390/ijerph19010417 ↗
45. Survey on composition and bioconcentration potential of 12 metallic elements in King Bolete (Boletus edulis) mushroom that emerged at 11 spatially distant sites10.1080/03601234.2011.540528 ↗
46. Elbanna, K., Alsulami, F.S., Neyaz, L.A., and Abulreesh, H.H. (2024). Poly (γ) glutamic acid: A unique microbial biopolymer with diverse commercial applicability. Front. Microbiol., 15.10.3389/fmicb.2024.1348411 ↗
47. Poly-glutamic acid (PGA)-Structure, synthesis, genomic organization and its application: A Review
48. Investigating the role of poly-γ-glutamic acid in Pennisetum giganteum phytoextraction of mercury-contaminated soil10.1016/j.scitotenv.2024.173707 ↗
49. The accumulation and release of Cd and Pb from edible mushrooms and their biomass10.15244/pjoes/74898 ↗
50. Krakowska, A., Reczyński, W., Krakowski, T., Szewczyk, K., Opoka, W., and Muszyńska, B. (2020). A new biotechnology method of bioelements’ accumulation monitoring in in vitro culture of Agaricus bisporus. Molecules, 26.10.3390/molecules26175165 ↗
51. Włodarczyk, A., Krakowska, A., Sułkowska-Ziaja, K., Suchanek, M., Zięba, P., Opoka, W., and Muszyńska, B. (2020). Pleurotus spp. Mycelia Enriched in Magnesium and Zinc Salts as a Potential Functional Food. Molecules, 26.10.3390/molecules26010162 ↗
52. Advances in microbial production of poly-γ-glutamic acid: Strategies and applications
53. Bioactive potential and possible health effects of edible mushrooms
54. Medicinal mushroom science: History, current status, future trends, and unsolved problems
55. Food safety concerns of edible mushrooms: A review
56. Biocontrol potential of γ-polyglutamic acid against foodborne pathogens in fresh produce
57. Mechanisms of antibiotic resistance in Pseudomonas aeruginosa
58. Efflux pumps as antimicrobial resistance mechanisms10.1080/07853890701195262 ↗
59. Sharma, S. (2014). Microbial contamination of edible mushrooms: A review. Food Microbiol., 88.
60. (2011). FDA Food Safety Modernization Act (FSMA), U.S. Food & Drug Administration.
61. EFSA Panel on Contaminants in the Food Chain (CONTAM) (2009). Scientific Opinion on heavy metals in food. EFSA J., 7, 1570.10.2903/j.efsa.2009.1351 ↗
62. Consumer trends towards natural food preservatives and implications for microbiological safety
63. (2025, July 25). OECD Guidelines for the Testing of Chemicals. Available online: https://www.oecd.org/en/topics/sub-issues/testing-of-chemicals/test-guidelines.html.
64. Codex Alimentarius Commission (2003). Hazard Analysis and Critical Control Point (HACCP) System and Guidelines for Its Application, Codex Alimentarius Commission.
65. Biopolymers as food additives in microbial control
66. FSANZ Standards (2023). Food Safety Regulations, Australia New Zealand Food Standards Code, FSANZ Standards.
67. FAO (2022). Sustainable food systems and microbial safety: Regulatory perspectives. FAO Food Saf. Rev., 18, 1–27.
68. EMA (2024). Guideline on the Safety Assessment of Natural Polymers in Food, European Medicines Agency.