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Pikula, K.;  Johari, S.A.;  Golokhvast, K. Carbon-Based Nanomaterials Biodegradation. Encyclopedia. Available online: https://encyclopedia.pub/entry/37137 (accessed on 17 June 2024).
Pikula K,  Johari SA,  Golokhvast K. Carbon-Based Nanomaterials Biodegradation. Encyclopedia. Available at: https://encyclopedia.pub/entry/37137. Accessed June 17, 2024.
Pikula, Konstantin, Seyed Ali Johari, Kirill Golokhvast. "Carbon-Based Nanomaterials Biodegradation" Encyclopedia, https://encyclopedia.pub/entry/37137 (accessed June 17, 2024).
Pikula, K.,  Johari, S.A., & Golokhvast, K. (2022, November 29). Carbon-Based Nanomaterials Biodegradation. In Encyclopedia. https://encyclopedia.pub/entry/37137
Pikula, Konstantin, et al. "Carbon-Based Nanomaterials Biodegradation." Encyclopedia. Web. 29 November, 2022.
Carbon-Based Nanomaterials Biodegradation
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Carbon-based nanomaterials (CNMs) have attracted a growing interest over the last decades. They have become a material commonly used in industry, consumer products, water purification, and medicine. The knowledge about the biodegradation of nanomaterials will facilitate the development of the principals of “biodegradable-by-design” nanoparticles which have promising application in medicine as nano-carriers and represent lower toxicity and risks for living species and the environment.

biodegradation carbon dots enzymes fate fullerenes

1. Enzymatic Biodegradation

The biological transformation of NPs is the most environmentally friendly degradation method [1]. Biodegradation of CNMs occurs due to the interaction of NPs with enzymes, organisms, and individual cells [2]. This section will discuss the main principles and current achievements in the field of CNMs’ biodegradation.
The contact of enzymes with NPs results in the changes in both sides of this interaction. NPs can be modified, degraded, or synthesized, while enzymes can be immobilized and optimized for further application. It was reported that different types of CNMs can cause either inhibition or enhancement of enzyme activity [3]. The effect of NMs on enzymatic activity depends on the types of enzymes, environmental conditions, physical and chemical properties of NPs, intentional and environmental modification of NPs [4][5][6].
Among the enzyme properties, the amino acid composition and orientation of an enzyme’s 3D structures play the key role [7]. Therefore, the effective enzyme interaction with NPs can be obtained by a proper match between enzyme composition/orientation and NPs properties. Suitable environmental conditions (pH, temperature, ionic strength, etc.) are also required for effective nano-bio interaction.
Enzymatic transformation of CNMs is the most studied and promising approach that can be used both for environmental purification from CNMs [8][9] and green synthesis of CNMs [10]. One of the first studies of enzyme-catalyzed degradation of CNM was performed by Allen et al. (2008) with SWCNTs and the plant enzyme horseradish peroxidase (HRP) [11]. In their following work, the same research group suggested that oxidation and degradation of CNTs occurs due to the hydrophilic interaction between the heme active site of HRP and the oxygen-containing defective sites on CNTs [12]. Zhao et al. (2011) showed the layer-by-layer degradation mechanism of MWCNTs exposed to HRP and H2O2, and highlighted that side wall defects facilitated degradation efficiency [13]. Kagan et al. (2010) demonstrated that bio-peroxidases, such as the human neutrophil enzyme myeloperoxidase (MPO) and its reactive radical intermediates, can catalyze the biodegradation of SWCNTs in vivo [14].
In general, mechanisms and achievements in enzymatic biodegradation of NPs, and the involvement in this process of reactive intermediates such as oxo-ferryl iron, hypochlorous and hypobromous acids were reviewed in a comprehensive work of Vlasova et al. (2016) [8]. Currently, the list of enzymes involved in the degradation of CNMs includes HRP, myeloperoxidase (MPO), lactoperoxidase (LPO), manganese peroxidase (MnP), lignin peroxidase (LiP), eosinophil peroxidase (EPO), xanthine oxidase (XO), and others [8][15]. Sureshbabu et al. (2015) demonstrated the importance of surface modification of NPs in their enzymatic degradation [16]. Moreover, metal-containing CNMs revealed peroxidase-like activity which can be responsible for self-biodegradation mechanism [8].

2. Microbial Biodegradation

Microorganisms have contact with all the substances present in the environment and take part in the production of a significant part of biomass on Earth. Chen et al. (2019) systematically reviewed the differences between the impact of varied types of CNMs on microbial communities [17]. It is worth noting that aside from negative effects, CNMs can stimulate the growth and the metabolic activities of tolerant microorganisms at relatively low concentrations. The ability of microorganisms to use CNMs as a source of carbon and the subsequent degradation of CNMs can be an accompanying effect of such microbial tolerance [18]. Therefore, microorganisms will inevitably have contact with CNMs [19]. The main mechanism of microbial transformation and degradation of CNMs is related to the ability of microorganisms to produce oxidative enzymes such as laccase, MnP, and LiP [20]. Microbial degradation of CNMs attracts the scientific community’s attention as a promising method of environment purification despite the current level of development of the process being fairly inefficient and not well-known [18].
Chen et al. (2017) summarized the works related to bacteria and fungi, which can degrade CNTs and graphene-related materials [1]
Aside from the transformation and degradation of CNMs, the contact of microorganisms with this type of NPs can have other beneficial effects, such as an alteration of biomass production in cultural plants [21][22], and the enhancement of organic pollutants’ degradation in the soil and the water environment [23][24].
Further studies are needed to improve the efficiency of microbial degradation of CNMs. These future works should include the development of mixed cultures of carbon-degrading microorganisms, identification of new species, and enzymes with high CNMs-degrading potential, exploring the impact of particle characteristics and media conditions on the process of biodegradation.

3. Biodegradation in Inflamatory Cells

The biomedical application of CNMs triggered the studies of their safety assessment including accumulation, excretion, impact on immune system, bio-corona formation, and degradation in higher organisms [25]. From this point of view, the role of the immune system which facilitates ‘digestion’ of CNMs through oxidative reactions represents a high interest in the elimination of possible toxicity of CNMs [25]. Moreover, the study of CNMs’ biodegradation in inflammatory cells was one of the most informative models that has helped to understand the main mechanisms of this process.
It was stated that the effective degradation of CNMs required a generation of reactive intermediates and a presence of a source of their oxidizing equivalents [8]. In this regard, inflammatory cells (neutrophils and eosinophils) support the production of the radicals (ROS and RNS) that are highly reactive towards CNMs [26][27] and facilitate enzymatic biodegradation of CNMs, specifically neutrophils via the production of MPO [14][28], and eosinophils via the production of EPO [29].
As reported by Kagan et al. (2010), neutrophils required activation to enhance the oxidative biodegradation of CNMs [14]. The other study demonstrated that neutrophils can produce so-called neutrophil extracellular traps (NETs) consisting of nuclear chromatin fibers studded with granule proteins which can capture and digest SWCNTs [25].
The ability of macrophages to digest CNTs was reported in several works [30][31]. Yang and Zhang (2019), in their work, reviewed the mechanisms and recent works related to the biodegradation of CNTs by macrophages in vitro and in vivo [32]. For macrophages, it was shown that the biodegradation of NPs occurred by the production of peroxynitrite (ONOO) and the activation of the superoxide/peroxynitrite oxidative pathway [30]. The mechanism of peroxynitrite-driven oxidation is independent of the protein-nanoparticle binding and, therefore, can effectively oxidize pristine CNMs increasing their reactivity to the enzymes of neutrophils and eosinophils [30]. The other study demonstrated a strong dependence of SWNTs’ degradation by MPO and ONOO− from NADPH oxidase [33]. Lu et al. demonstrated that the binding of fibrinogen reduces the toxicity of SWCNTs but does not inhibit biodegradation via MPO and ONOO− dependent pathways [34].
Further studies of CNMs’ degradation and transformation mechanisms via cell degradation will allow to regulate the fate of carbonaceous NPs in vivo and facilitate the production of biodegradable-by-design NPs.

References

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