ReviewInsights into the microbial degradation and biochemical mechanisms of carbamates
Graphical abstract
Introduction
The direct or indirect applications of pesticides along with their long-lived toxic residues into the environment, cause potential hazardous effects on human health and wildlife, via food chain and contamination of natural resources (Sun et al., 2018; Mathew et al., 2018; Hageman et al., 2019). Carbamates and the related compounds replaced organophosphates (OPs), as carbamate compounds were considered as low persistence compared to organochlorines (OCs) and less toxic than neurotoxic OPs (Hernandez et al., 2013; Vale and Bradberry, 2017). Carbamates are chemical ester compounds derived from carbamic acids and are structurally simpler and considered to be safer than OPs; due to their easier breakdown, low bioaccumulation and less persistence and thus, they are exceedingly used in agriculture as well as in household and industrial workplaces. Carbamates are frequently used in the modern agricultural sector as insecticides, herbicides, fungicides, nematicides, molluscicides, and acaricides due to their broad horizon of biological activity. In the last two decades, the widespread use of carbamate compounds in pest control grew over that of OCs or OPs (Silberman and Taylor, 2020; Cazaro-Rojas et al., 2018; Gupta, 2006).
Therefore, the extensive exposure of carbamates in the environment has raised severe public concerns regarding the public health, crop quality and environmental safety (Carvalho, 2017; Nicolopoulou-Stamati et al., 2016). Carbamate compounds are a reversible inhibitor of acetylcholine esterase enzymes, which result in the improper functioning of nerve synapses and neuromuscular junctions. Carbamate compounds have toxic symptoms and can adversely affect reproductive, hepatic, renal, neurological, and immune functions in honeybees, fish, birds, mammals and aquatic animals (Luo and Wu, 2019; Piel et al. 2019; Kaur et al., 2019; Dias et al., 2015). High concentration of carbamate compounds causes significant changes in protein level, acid and alkaline phosphatase, hemoglobin (Hb) content, glucose, total serum lipids, melondialdehyde (MDA) and glutathione (GSH) levels in mammals (Bhalodiya et al., 2014; Hamid et al., 2013; Morais et al., 2012; Sharma et al., 2012; Rai et al., 2011). Carbamate compounds also have cytotoxic effects in human and animal cells. In-vitro studies have revealed that carbamate compounds had cytotoxic effects in hamster ovarian cells (CHO–K1), inhibiting cell viability and succinic dehydrogenase activity (Soloneski et al., 2015). It has also been reported that carbamates can significantly induce apoptosis and necrosis in human natural killer cells (Li et al., 2014), and trigger apoptosis in human immune cells and in lymphocytes cells (Li et al. 2011, 2015; Eren et al., 2015). Carbamates can also induce oxidative stress, inhibit enzymatic activity of red blood cells, cause lipid peroxidation, and disturb cellular membrane integrity (Agarwal and Sharma, 2010). The long term-exposure of carbamate compounds cause behavioral abnormalities and slow growth rate in honey bees, birds and aquatic animals (Kumar et al., 2020; Ramesh et al., 2015; Mitra et al., 2011; Moore et al., 2010). Thus, carbamate residues are an acute threat to living beings, and their degradation/detoxification via rapid and eco-friendly remediation technologies is needed. However, many conventional approaches used for removing pesticide contamination cannot be accepted due to their expensive high cost and post-waste generation and contamination problems (Kumar et al., 2017; Mustapha et al., 2019a; Feng et al., 2020). In this regard, microbial technology is of great interest, and can be used as a smart biological tool instead of conventional treatment approaches for the remediation of pesticide-contaminated sites (Holmsgaard et al., 2017; Mandal and Das, 2018; (Pang et al., 2020).
Microbial degradation is a primary mechanistic remedial application, which efficiently degrades and detoxifies complex organic pollutants into simple and small molecules (Hlihor et al., 2017; Zhan et al., 2018; Mishra et al., 2020). Microbial degradation is a naturally safe, clean, and less disruptive approach to the environment than excavation-based processes, as it can be performed as an on site treatment (in situ) (Sharma et al., 2016; Sharma, 2019). Microbial methods mostly degrade pollutants either completely to water and carbon dioxide, or into less toxic forms, and reduce the need for disposal of contaminated material (Azubuike et al., 2016; Parte et al., 2017; Mustapha et al., 2019b). Moreover, microbial methods are highly feasible and effective for remediation processes due to their low cost and ability to survive under extreme environmental conditions (Verma et al., 2014; Malla et al., 2018; Mishra et al., 2021). Thus, the environmentally friendly nature and low cost of microbial technology make it a useful and attractive approach compared to physico-chemical treatment approaches for the decontamination of polluted environments (Cycoń et al., 2017; Huang et al., 2019; Bhatt et al., 2019). To date, several bacterial strains belonging to the genera Sphingomonas (Kim et al., 2004; Yan et al., 2018), Pseudomonas (Singh et al., 2013; Naqvi et al., 2013; Zhu et al., 2018), Microbacterium (Mohamed, 2017), Enterobacter (Fareed et al., 2017; Ekram et al., 2020), Achromobacter (Naqvi et al., 2009), Arthrobacter (Lawrence et al., 2005; Hayatsu et al., 2001, Hayatsu et al., 1999), Aminobacter (Osborn et al., 2010; Zhang et al., 2017), Novosphingobium (Nguyen et al., 2015), Bacillus (Roy and Das, 2017), Stenotrophomonas (Mohamed, 2009; Yang et al., 2017), Cupriavidus (Gupta et al., 2019), Sphingbium (Jiang et al., 2020), and Burkholderia (Seo et al., 2013) have been isolated and well characterized from pesticide-contaminated soils to understand the function of microbial species in the degradation of carbamates from contaminated environments.
Bacterial plasmids play a significant role in the continuous evolution and dissemination of novel biodegradation genes (Chen et al., 2011). These genes have endowed microorganisms with the capability to degrade a wide range of environmental pollutants (Phale et al., 2019). However, only a few of bacterial strains from the genera Sphingomonas, Achromobacter, and Pseudomonas have been recognized for plasmid-encoded catabolic genes (Trivedi et al., 2016; Yan et al., 2018; Zhu et al., 2019). Feng et al. (1997) reported the plasmid-mediated mineralization of carbofuran in Sphingomonas sp. CF06, which harbors five plasmids—CF01, CF02, CF03, CF04 and CF05—associated with its carbofuran degradation ability. Hayatsu et al. (1999) evaluated the involvement of plasmids in the degradation of carbaryl compounds in Arthrobacter sp. RC100. The strain RC100 carries three plasmids (pRC1, pRC2 and pRC300), among which two conjugative plasmids, pRC1 and pRC2, were found to be involved in the complete degradation of carbaryl. The plasmid pAC200, carrying the cehA gene encoding carbaryl hydrolase activity in Rhizobium sp. AC100, is also involved in carbaryl degradation (Hashimoto et al., 2002). Moreover, Zhu et al. (2019) reported a plasmid, pXWY-1, carrying a carbaryl-degrading gene cluster, in Pseudomonas putida XWY-1, and 13 genes in the cluster were directly involved in carbaryl biodegradation. The plasmid may facilitate the horizontal transfer of catabolic genes from one microbe to another, ensuring microbes have the ability to adapt to unfavorable environments. However, the limited application of the plasmid-carrying microbial population remains a challenge for microbial bioremediation studies. Hitherto, there have been relatively few studies exploring the degradation potential of microorganisms in the biodegradation of carbamates, but their genetic basis and molecular biology of the biodegradation strategy have not been well explained (Mustapha et al., 2020; Kaur and Balomajumdar, 2019; Fareed et al., 2019; Sharma et al., 2016). The extensive application of carbamates increases their toxicity concern to the environment and human health. Nowadays, microbial degradation is one of the major and ecofriendly process for the removal of carbamates from the environment. Therefore, the aim of this review is to explore in-depth information on the carbamate degradation mechanisms with microbial strains, their metabolic pathways, with special emphasis on carbamate hydrolase enzyme/genes crucially important for the biodegradation process by evolving new metabolic functions.
Section snippets
Carbamate compounds: chemistry and toxicology structures
Carbamate compounds are commonly derived from carbamic acids, and the chemical compositions of the carbamate compounds presented in Fig. 1 contain three different functional moieties: R1, R2, and R3. Generally, R1 and R2 represent organic functional groups. When R1 is methyl and R2 is hydrogen, the carbamate exhibits insecticidal properties. However, when R1 has an aromatic functional group, the compound is employable as a herbicide, and when R1 is a benzimidazole moiety, it demonstrates
The microbial degradation of carbamates
Microbial technology is an effective and sustainable system for pesticide degradation in agricultural and industrial fields due to its ability to complete the mineralization of pollutants with economic benefits (Fang et al., 2018; Parte et al., 2017; Khan et al., 2016). The major routes of the microbial degradation of carbamate compounds are hydrolysis and oxidation (Gupta et al., 2019; Jiang et al., 2020; Chaudhry et al., 2002). Hydrolysis of carbamate compounds is the initial metabolic step,
Carbamate hydrolyzing and detoxifying enzymes
The characterization of pesticide-degrading microbial enzymes has gained interest due to their inexpensiveness, feasibility, and straightforward degradation and detoxification (Scott et al., 2009; Zhang et al., 2020; Bhatt et al., 2021d). Biochemical degradation reactions for any pollutant can be achieved through various enzymes, such as hydrolases, hydroxylases, cytochrome P450, oxidases, and ligninases (Chen et al., 2013; Yang et al., 2018; Zhang et al., 2021). A cytochrome P450 system in
The genetic basis of the microbial degradation of carbamate compounds
The molecular and genetic mechanisms include decisive information regarding the microbial remediation of carbamates and have attracted much attention. For several pesticides, the metabolic pathways and degradation relationships are well distinguished but we lack understanding and knowledge regarding their degradation enzymes, respective genes and encoded plasmids (Rousidou et al., 2016; (Chen et al., 2015); Zhan et al., 2020; Trivedi et al., 2016). The distribution of plasmid-mediated
Conclusions and future perspectives
Microorganisms exhibit remarkable metabolic diversity and are able to degrade carbamates in contaminated environments. Microbes can adapt relatively quickly and evolve new metabolic functions to degrade hazardous carbamate compounds, opening a new prospect of their possible exploitation in bioremediation studies of contaminated matrixes. However, the success rate of biodegradation depends on the efficacy and potentiality of microorganisms and their degradation traits. Modern technological
Declaration of competing interest
Authors declare that they have no competing interests.
Acknowledgements
This work was financially supported by grants from the Key-Area Research and Development Program of Guangdong Province, China (2018B020206001), the Natural Science Foundation of Guangdong Province, China (2021A1515010889), the National Natural Science Foundation of China, China (31401763) and the Guangdong Special Branch Plan for Young Talent with Scientific and Technological Innovation, China (2017TQ04N026).
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