Role of Lytic Polysaccharide Monooxygenases in Boosting the Action of PETases on PET Polymers

A recent article in ChemSusChem explored the binding of Lytic Polysaccharide Monooxygenases (LPMOs) to polyethylene terephthalate (PET), converting the hydrophobic surface of PET hydrophilic. Subsequent treatment with classical esterase enzymes (PETases) exhibited boosted product release.

A plastic bottle floats in the Pacific Ocean. Plastics break down into tiny pieces which enter the food chain and can be harmful to many species, including humans.

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Background

The mechanical and chemical properties of plastic, including strength and inertness, have made them indispensable across several applications worldwide. However, these same properties, combined with limited recycling efforts, have led to the accumulation of plastics in landfills and natural environments.

Some organisms have adapted to utilize plastics. For instance, the PET-assimilating bacterium Ideonella sakaiensis has developed metabolic capabilities to use these materials as an energy source. This bacterium secretes PETase, an enzyme that breaks down the polymeric chains in PET.

However, many fungi and bacteria struggle with the inertness and hydrophobicity of plastic substrates. LPMO enzymes are capable of cleaving polysaccharide chains through a strong oxidative mechanism. Given the great similarity between the properties of PET and polysaccharides, this study examined the potential of LPMOs in boosting the action of PETases on PET through a similar oxidative cleavage mechanism.

Methods

Coupons (~0.6×0.4 cm) of PET bottle, high-density polyethylene, and polypropylene were reacted with AfLPMO9A on a phosphoric acid swollen cellulose (PASC) substrate. Subsequently, cello-oligosaccharides were detected as in “detection of products from LPMO.”

LPMO deposition on plastic coupons was analyzed using X-ray photoelectron spectroscopy (XPS) and atomic force microscopy (AFM). Products from LPMO were detected using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-ToF MS), electrospray ionization mass spectrometry (ESI-MS), and high-performance anion-exchange chromatography coupled with pulsed amperometric detection (HPAEC-PAD).

The interaction between AfLPMO9A and IsPETase was assessed through both sequential and simultaneous enzyme assays using PET powder as the substrate.

In sequential assays, PET was pretreated with AfLPMO9A, and the residual substrates were washed with Milli-Q water or sodium dodecyl sulfate. The washed residual substrates were then made to react with IsPETase.

In the simultaneous assays, AfLPMO9A and IsPETase were added simultaneously for reaction with PET. The concentration of mono(2-hydroxyethyl)-terephthalate (MHET), terephthalic acid (TPA), and bis(2-hydroxyethyl)-terephthalate (BHET) released by IsPETase was determined by high-performance liquid chromatography (HPLC). Reactions with only IsPETase were the controls for simultaneous and sequential assays.

The protein bound to PET was estimated indirectly from the remaining soluble fraction after incubation with AfLPMO9A, measured using a spectrophotometer. The hydrophobicity average for different samples was also calculated using the Kyte-Doolittle scale in Chimera27. Finally, the data was analyzed statistically by ANOVA and Tukey′s test at a 5 % significance level.

Results and Discussion

Adding a combined solution of AfLPMO9A and IsPETase to PET lowered the esterase activity compared to adding IsPETase alone to PET. Thus, LPMOs and/or ascorbate could degrade PETase through undefined redox chemistry, highlighting the deleterious effects of reactive oxygen species generated by LPMOs without a natural substrate.

The simultaneous addition of CuSO4 and IsPETase to PET resulted in a slight increase in MHET and TPA production. However, combinations of ascorbate+CuSO4 and ascorbate+CuSO4+H2O2 reduced MHET and TPA release by 70 % and 100 %, respectively. Similarly, the simultaneous addition of AfLPMO9A and IsPETase to PET did not enhance the activity of IsPETase.

In contrast, pre-treating milled PET bottles with AfLPMO9A, followed by washing and sonication to remove residual LPMO, and then applying IsPETase, increased the release of MHET and TPA by 24–64 %.

MALDI-ToF MS analysis of PET before and after LPMO treatment detected no products directly attributable to LPMO action. Additionally, HPLC failed to detect BHET, MHET, or TPA when the supernatant from the AfLPMO9A reaction was incubated with IsPETase. However, ESI-MS analysis of the supernatant from reactions of AfLPMO9A with milled PET identified a soluble product, tentatively identified as D-xylonate.

When milled PET was reacted with AfLPMO9A alongside the known substrate PASC, no significant difference in cello-oligosaccharide production was observed. This suggests that the interaction between milled PET and catalytically active AfLPMO9A was minimal or absent. The protein detected on the PET surface by XPS was likely denatured LPMO protein present in the sample, which remained adhered to the surface and could not be removed even after aqueous washing and sonication.

Conclusion

The researchers found no evidence of oxidized products from PET after treatment with AfLPMO9A. Data from XPS and AFM, including analyses with a catalytically inactive mutant of AfLPMO9A, suggested that the observed enhancement of PETase activity following LPMO pre-treatment was likely due to the hydrophobin effect. In this phenomenon, the LPMO binds to the PET surface and facilitates the recruitment of PETases to the polymer, improving their interaction with the substrate.

The hydrophobin effect of LPMOs contributes to biotechnological approaches for enhancing PETase activity on PET. However, the researchers recommend further studies on the interaction of biomolecules with synthetic polymers such as polyethylene and polypropylene to extend the applicability of similar strategies. This could support the development of methods for the bioremediation of a broader range of synthetic polymers.

Journal Reference

Corrêa, T.LR., et al. (2024). On the Non‐Catalytic Role of Lytic Polysaccharide Monooxygenases in Boosting the Action of PETases on PET Polymers. ChemSusChem. DOI: 10.1002/cssc.202401350, https://chemistry-europe.onlinelibrary.wiley.com/doi/full/10.1002/cssc.202401350​​​​​​​​​​​​​​

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Nidhi Dhull

Written by

Nidhi Dhull

Nidhi Dhull is a freelance scientific writer, editor, and reviewer with a PhD in Physics. Nidhi has an extensive research experience in material sciences. Her research has been mainly focused on biosensing applications of thin films. During her Ph.D., she developed a noninvasive immunosensor for cortisol hormone and a paper-based biosensor for E. coli bacteria. Her works have been published in reputed journals of publishers like Elsevier and Taylor & Francis. She has also made a significant contribution to some pending patents.  

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