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Reduction of nicotine content in tobacco through microbial degradation: research progress and potential applications

Biotechnology for Biofuels and Bioproducts volume 17, Article number: 144 (2024) Cite this article

Abstract

Originally native to South America, tobacco and is now distributed worldwide as a major cash crop. Nicotine is the main harmful component of tobacco leaves, cigarette smoke and tobacco waste, which severely affects not only the flavor of the tobacco leaf, but also causes great damage to human health. As the anti-smoking movement continued to grow since the 1950s, and consumers become more aware of their health and environmental protection, the world tobacco industry has been committed to research, develop and produce low nicotine cigarette products with relatively low risk to human health. Among various approaches, the use of microorganisms to reduce nicotine content and improve tobacco quality has become one of the most promising methods. Due to increasing interest in nicotine-degrading microorganisms (NDMs), this article reviews recent reports on NDMs, nicotine-degrading enzymes, regulation of nicotine-degrading bacterial consortia and optimization of fermentation conditions, aiming to provide updated references for the in-depth research and application of microorganisms for the degradation of nicotine.

Graphical Abstract

Background

Since its earliest domestication in South America, tobacco has been cultivated in over 125 countries, generating billions of dollars in revenue each year and playing a vital role in the economy of many countries [1]. However, due to a lack of advanced processing technologies, the content of harmful substances in tobacco is high, which has caused serious damage to human health and has led to campaigns against tobacco use [2, 3]. The characteristic harmful substances of tobacco mainly include nicotine, N-nitrosamines (TS-NAs) and tar. Nicotine (3-(1-methyl-2-pyrrolidinyl)pyridine), a heterocyclic compound with a pyridine and a pyrrolidine ring moiety, is the major harmful component in tobacco leaves, cigarette smoke and tobacco waste [4]. Nicotine is a central nervous stimulant that can cause physiological and psychological dependence, which has led to its classification as an addictive substance. Moreover, it can also lead to tobacco-related lung cancer and peripheral artery disease, causing irreversible damage to the human body. A large amount of high nicotine tobacco is produced every year, which not only seriously affects the flavor of tobacco products, but also increases their harmfulness [5,6,7,8,9,10,11,12]. Therefore, reducing the content of nicotine in tobacco is of great importance for maintaining human health and protecting the ecological environment. With the constant advancement of science and technology, microbiology has been widely used in the fields of food, medicine and health care products, and also provides a premise to improve the quality of tobacco [13,14,15,16,17,18]. Microbial treatment is an effective way to reduce the content of nicotine in tobacco and the environment, while preventing the loss of tobacco flavor, and also improving the quality of smoke, increasing the efficiency of tobacco resources, and more importantly, reducing the damage of nicotine to human health, showing great potential for development. To date, a large amount of basic and applied research work has been carried out in the use of microorganisms for nicotine degradation [15, 19,20,21,22,23,24,25,26,27,28,29]. In particular, some progress has been made in recent years in the study of molecular mechanisms such as key enzymes and related genes for nicotine degradation. This review summarizes recent reports on nicotine-degrading microorganisms, nicotine-degrading enzymes, regulation of nicotine-degrading bacterial consortia, and optimization of fermentation conditions, with the aim of promoting basic microbiological research in the tobacco industry.

Nicotine-degrading microorganisms

To date, researchers have developed physical, chemical and biological methods for nicotine degradation. However, physical and chemical methods have the disadvantages of low degradation efficiency and complex equipment. By contrast, microbial methods use a variety of nicotine-degrading microorganisms and enzymes, which are cheaper, more efficient, and more ecologically friendly [21, 24, 30]. Some large tobacco companies, such as B&W Tobacco and British American Tobacco, have been using microorganisms to degrade nicotine in tobacco for a long time. Microorganisms that degrade nicotine have been mainly isolated and screened from the surface of tobacco leaves or soil [31]. They can usually utilize nicotine as the sole carbon, nitrogen and energy source for their growth [32, 33].

Since Reid et al. first discovered in 1944 that nicotine-degrading bacteria and molds are present on the surface of cigar tobacco leaves, a large number of nicotine-degrading microorganisms were screened, isolated and identified [34]. For example, Gutierrez et al. isolated the Enterobacter cloacae strain E-15040 from the surface of dried tobacco leaves, which was able to degrade nicotine [35]. In 2004, Pseudomonas putida S16 was isolated from soil ( Shandong, P.R. China), and exhibited a high nicotine degradation capacity, degrading 4 g L−1 nicotine in 13 h and tolerating concentrations of up to 6 g L−1 nicotine [36]. Similarly, Yuan et al. [37] used enrichment culture technique to isolate the highly efficient nicotine degrading strain Ochrobactrum intermedium DN2 (Fujian, P.R. China), which had high degradation activity in the temperature range of 30 ~ 40 Â°C and pH 6.0 ~ 9.0, reaching a degradation efficiency of 97.56% after 36 h. In 2008, Pseudomonas sp. Nic22 was isolated and its crude enzyme extract was found to not only reduce the nicotine content, but also improve the quality of tobacco leaves (Zimbabwe and, P.R. China) [38]. In addition, the Agrobacterium sp. strain S33, which could degrade 3 g L−1 nicotine in 1.5 h, was isolated from soil in a tobacco-growing area by Wang et al. (Shandong, P.R. China) [39]. In 2012, Ochrobactrum sp. 4–40, isolated from tobacco leaves, was discovered to be effective in degrading nicotine in tobacco (Mile, Yunnan, P.R. China) [40]. A few years later, Pseudomonas aeruginosa TND35 was revealed to degrade 4.92 g L−1 of nicotine in 44 h by Raman et al., and the degradation rate of nicotine was increased during accelerated growth of bacterial cells (Ottanchathiram, Tamil Nadu, India) [41]. In recent years, many more novel nicotine-degrading strains have been isolated. Particularly surprisingly, Chen et al. recently discovered for the first time that the gut bacterium Bacteroides xylanisolvens can effectively degrade nicotine in the human gut and identified the novel nicotine-metabolizing enzyme NicX and its metabolites [42]. As shown in Table 1 and Fig. 1. In general, the bacteria that can degrade nicotine mainly belong to the genera Pseudomonas [32], Arthrobacter [32], and Ochrobactrum intermedium [37]. The main nicotine-degrading fungi are Cunninghamella echinulata [41], Microsporum gypseum, Streptomyces griseus, S. platensis and Pellicularia filamentosa [43]. These microorganisms play an important role in tobacco processing and tobacco waste treatment. For example, Pseudomonas spp. are highly favored by researchers as they produce many intermediate products with high added value in the process of nicotine degradation. To date, a number of wild-type strains capable of degrading nicotine have been widely used to degrade nicotine and treat waste from tobacco manufacturing processes [44].

Table 1 List of reported nicotine degrading strains
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Fig. 1
figure 1

Phylogenetic relationships of nicotine-degrading bacteria and related species were analyzed using 16S rRNA gene sequences. A neighbor-joining tree was constructed with MEGA 5.0

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Catabolism of nicotine in microorganism

With the continuous development of science and technology, as well as the improvement of the level of instrumental analysis, in recent years, studies went beyond the screening, isolation and identification of nicotine-degrading microorganisms, and have further explored the genetic background of their special metabolic processes. As a result, the specific reaction steps of nicotine degradation and the enzymes involved in catalysis have gradually been clarified in some strains [14, 28, 45,46,47,48,49,50].

Omics technologies have greatly accelerated the comprehensive understanding of nicotine metabolism and regulation in microorganisms. Based on this, three biodegradation pathways of nicotine have been summarized [43, 51]. One is the pyrrolidine pathway present in Pseudomonas spp. and Cunninghamella echinulata. The second is the pyridine pathway found in Arthrobacter sp. The third is the Me pathway present in tobacco plants and fungi. Among these three metabolic pathways, the pyridine pathway based on plasmid pAO1-mediated degradation of nicotine by Arthrobacter nicotinovorans is the most well-studied.

The pyridine pathway was first studied in detail by Baitsch et al. [14] and Brandsch et al. [13], who found that the biodegradation of nicotine is accomplished stepwise by several different enzymes [13]. A more detailed summary of the pathway is as follows (Fig. 2): (1) nicotine enters bacterial cells and is converted into 6-hydroxynicotine (6-HN) by nicotine dehydrogenase (NDH). Then, 6-HN can be processed to synthesize pyridine, which is an important precursor compound for industrial synthesis of painkillers [15, 27, 52]. (2) 6-Hydroxynicotine oxidase (6-HNO) catalyzes the dehydrogenation and oxidation of 6NH to 6-hydroxy-N-methylmyosmine (6-HMM), which is unstable and is spontaneously hydrolyzed to produce 6-hydroxy-pseudooxynicotine (6-HPON) [29]. (3) The pyridine ring is further opened to produce 2,6-dihydroxy pseudooxynicotine (2,6-DPHON) [53]. (4) The side chain of 2,6-DHPON is broken and cleaved by 2,6-dihydroxy pseudooxynicotine hydrolase (DHPONhl) to produce 2,6-dihydroxypyridine (2,6-DHP) and γ-N-methyl-aminobutyrate (MGABA). (5) Under the catalysis of 2,6-dihydroxypyridine-3-hydroxylase (DHPhl), 2,6-DHP is transformed into 2,3,6-trihydroxypyridine (2,3,6-THP). Finally, in the presence of oxygen, 2,3,6-THP is spontaneously oxidized and dimerizes to form nicotine blue and several other organic acids [54].

Fig. 2
figure 2

Pyridine pathway of nicotine degradation in Arthrobacter sp. involves key enzymes: nicotine dehydrogenase (NDH), 6-hydroxy-l-nicotine oxidase (6-HLNO), 6-hydroxy-d-nicotine oxidase (6HDNO), ketone oxidase (KO), ketone dehydrogenase (KDH), 2,6-dihydroxy-pseudooxynicotine hydrolase (2,6-DHPONH), 2,6-dihydroxypyridine-3-hydroxylase (2,6-DHPH), γ-N-methylaminobutyrate oxidase (MABO), monoamine oxidase (MAO), amine oxidase (AO), and succinic semialdehyde dehydrogenase (SsaDH)

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Ganas et al. [47] conducted a deeper molecular study of Arthrobacter nicotinovorans, and identified the positions of some genes encoding key enzymes related to nicotine degradation in the Nic gene cluster, achieving a significant breakthrough in the understanding of microbial nicotine degradation at the molecular level. Further studies revealed that nicotine can activate nicotinic acetylcholine receptors (nAChRs) in the ventral tegmental area (VTA) of the midbrain, where dopaminergic (DAergic) neurons are enriched, and that nicotine-induced activation of corticotropin reward circuits in the midbrain may trigger addiction [55]. Accordingly, these receptors may provide new molecular targets for smoking cessation treatment.

Nicotine-degrading Pseudomonas spp. were isolated from soil as early as 1954 and were extensively studied (Fig. 3) [56]. Recently, many researchers [36, 46, 57, 58] conducted numerous excellent studies in elaborating the metabolic pathways and related mechanisms of nicotine degradation by Pseudomonas putida S16. On the basis of these studies, Tang et al. cloned, sequenced, and expressed a 4879 bp-long nicotine metabolizing gene cluster from the genome of Pseudomonas putida S16 by cell fusion. The intermediate metabolites produced by the recombinant engineered cells were the same as those produced by the wild-type strain, and were derived from the pyrrole pathway [48]. In 2015, the nicotine-degrading enzyme NicA2, a flavoprotein derived from Pseudomonas putida, was found to have special biochemical properties and degrade nicotine into non-addictive substances, making Nic A2 a promising candidate in the field of nicotine addiction treatment [59]. In 2019, Thisted et al. [60] found that mutating the relevant active site of the P. putida S16-derived Nic A2 enzyme could significantly increase its catalytic activity, providing an approach to optimize nicotine degradation by increasing enzyme activity. However, the nicotine degradation efficiency is not high due to the fact that nicotine-degrading microorganisms tend to preferentially use glucose in the fermentation broth as a carbon source when degrading nicotine in tobacco waste extracts. To address this problem, Zhang et al. [61] used homologous recombination to knock out all five genes related to glucose metabolism. The resulting Pseudomonas sp. strain JY-Q/5∆ could completely degrade 0.8 g L−1 of nicotine in 5% tobacco waste extract dilution within 24 h, expanded applications of Pseudomonas spp. in practice.

Fig. 3
figure 3

Pyrrolidine pathways of nicotine degradation have been identified in various Pseudomonas species: Pseudomonas sp. HZN6, Pseudomonas sp. HF-1, Pseudomonas sp. Nic22, and Pseudomonas sp. CS3. Key enzymes involved include nicotine oxidoreductase (NicA), pseudooxynicotine amine oxidase (PNAO), 3-succinoylsemialdehyde pyridine dehydrogenase (SAPD), and 6-hydroxy-3-succinoyl pyridine hydroxylases (HspA and HspB)

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Notably, tobacco plants and fungi also play distinct roles in nicotine degradation, with mechanisms that differ significantly from those of bacteria. For example, fungi such as Aspergillus oryzae and Phanerochaete chrysosporium primarily degrade nicotine through the demethylation pathway (Me pathway). In this process, nicotine is gradually converted into intermediates such as N-methylmyosmine and pseudooxynicotine, eventually producing less toxic compounds like nicotinic acid. These fungi also secrete various enzymes, such as lignin peroxidase, to further break down other components of tobacco, including lignin. Compared to bacterial pathways that rely on oxidoreductases and hydrolases, the fungal degradation pathways demonstrate unique evolutionary adaptations in environmental versatility and degradation diversity, giving fungi an advantage in processing complex biomass and generating diverse chemical products. In addition, beyond bacteria and fungi, other microbial populations have also shown high efficiency in nicotine degradation. For instance, Ochrobactrum intermedium DN2 degrades nicotine primarily through a variant pyridine and pyrrolidine pathway (VPP pathway), which integrates upstream and downstream reactions of the classic pyridine and pyrrolidine pathways, enabling the strain to utilize nicotine as the sole source of carbon, nitrogen, and energy, ultimately converting it into non-toxic or low-toxicity products [62].

In summary, it can be seen that the microbial degradation of nicotine is a complex metabolic process, and there are still some metabolic steps and enzymes have not been elucidated. Future studies should aim to identify new nicotine degradation enzymes from different sources and co-express them in nicotine-degrading strains (Fig. 4), or to knock out the genes that inhibit nicotine degradation, so that we can quickly and effectively obtain genetically engineered strains with stronger degradation ability than wild-type strains, which can maximize their potential to improve tobacco quality and protect the environment.

Fig. 4
figure 4

Some of the reported nicotine degradation gene clusters. All gene clusters contain genes encoding key enzymes. The presence and varied arrangement of auxiliary genes indicate evolutionary divergence and functional specialization among the nicotine-degrading bacteria

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Regulation of nicotine degradation by microbial consortia

The fermentation of tobacco is a sophisticated process that involves spontaneous oxidation, as well as microbial and enzymatic action. However, reducing the nicotine content to a reasonable level is an important factor irrespective of the mechanism. In addition to reducing the nicotine content, some microorganisms can also act on the sugars and proteins in the tobacco leaves, converting them into alcohols, esters, various organic acids and amino acids, which neither destroy the original good quality of the tobacco leaves, nor increase the aroma of the tobacco leaves. Therefore, using microorganisms to solve the problem of excessive nicotine content in tobacco leaves is an efficient, environmentally friendly and low-cost approach.

Related research and applications have been carried out by tobacco researchers from various countries since the 1950s. A pioneering study published by Frankenburg et al. showed that the natural fermentation process of cigar tobacco was accompanied by a considerable degradation of nicotine [63]. In 1957, he isolated microorganisms from the surface of three types of tobacco seeds for nicotine degradation research. After degradation, oxamic acid, formamide, trace amounts of malonic acid and succinic acid can be generated [64]. Geiss et al. [21] placed several bacteria (such as Cellulomonas sp. and P. putida) in media containing nicotine and nitrate and used these cultures to treat white-ribbed tobacco under aerobic or anaerobic conditions. The levels of nitrate and nicotine in the treated tobacco were found to be reduced, and when used to treat tobacco products, the amount of nitrogen oxides, hydrogen cyanide, and nicotine in the smoke was diminished. At the same time, there was no loss of desirable flavor or smoking properties. Subsequently, Meher et al. [24] reduced chemical oxygen demand (COD), nicotine, and biological oxygen demand (BOD) in tobacco by 60%, 75%, and 80%, respectively, using fermentation with a mixture of methanogenic bacteria. Moreover, the microflora can also play an important role in reducing nicotine content when dealing with tobacco waste. For example, compost fermentation of tobacco solids was investigated by Briski [65] and it was revealed that at the end of composting, the nicotine in tobacco waste was reduced by 80%. The dominant microorganisms in the fermentation process were fungi and thermophilic bacteria, mainly yeasts, Pseudomonas, Bacillus and thermophilic actinomycetes.

Currently, Pseudomonas spp. are the most widely used bacteria in the degradation of nicotine to improve the quality of tobacco leaves [32, 38, 66]. Because Pseudomonas spp. has the highest degradation capacity[67]. In addition, optimizing culture conditions and utilising metabolic engineering strategies can significantly enhance the efficiency of nicotine degradation in tobacco leaves and products. Bacteria play a critical role in this process, particularly species such as Bacillus subtilis, Bacillus coagulans, Bacillus circulans, Bacillus megaterium, and Bacillus thuringiensis, which are commonly used to treat tobacco leaves and products. These bacteria help to generate desirable aromas in tobacco, thereby improving the sensory qualities and smoking characteristics of the tobacco [68,69,70,71]. In addition to these bacteria, fungi, yeasts, and thermophilic actinomycetes are also crucial in the tobacco degradation process. Fungi like Aspergillus oryzae and Phanerochaete chrysosporium, as well as certain yeasts, secrete a variety of enzymes, such as lignin peroxidase and cellulase, which break down complex organic compounds in tobacco, including lignin, cellulose, and hemicellulose. The secretion of these enzymes not only aids in nicotine degradation but also enhances the generation of tobacco aromas and produces a range of potentially valuable by-products during the degradation process. In contrast, thermophilic actinomycetes, such as members of the genera Thermomonospora and Streptomyces, are highly effective at degrading nicotine and other harmful substances in tobacco under high-temperature conditions. This makes them particularly valuable in the treatment of high-temperature composting and other thermally processed tobacco waste [13, 47, 51, 62, 71].

Thus, in the regulation of microbial consortia for tobacco degradation, bacteria, fungi, yeasts, and thermophilic actinomycetes each play unique and complementary roles. By combining the strengths of these different microorganisms, the overall efficiency of tobacco leaf and product degradation can be significantly improved, while also enhancing the quality of tobacco products to better meet market demands. Future research can explore several feasible strategies to further enhance the efficiency of tobacco degradation. First, optimizing microbial synergy is crucial; studying the optimal combinations of different microbial communities, such as co-cultivating fungi and bacteria, can lead to synergistic effects, maximizing degradation efficiency by complementing each other's capabilities in breaking down various organic components. Second, genetic engineering of key microorganisms could enable the expression of more efficient enzymes or metabolic pathways involved in nicotine degradation. By employing gene editing techniques, it may be possible to enhance the ability of microorganisms to process recalcitrant components in tobacco. In addition, precise control of environmental conditions during fermentation, including temperature, pH, and oxygen concentration, can promote the selective growth of advantageous microbial communities, thereby improving overall degradation efficiency. For instance, dynamically adjusting fermentation temperatures can fully exploit the characteristics of thermophilic actinomycetes and other microorganisms. Finally, there is potential to further develop the valuable by-products generated during microbial degradation into commercially viable products, such as flavor compounds, chemical precursors, or bioenergy, thereby enhancing the economic viability of the entire degradation process.

Optimization of fermentation conditions

During tobacco fermentation, there are regular changes in the microbial community, and the number of microorganisms is significantly correlated with enzyme activity, indicating that the quality of tobacco may be related to the enzymes secreted by microorganisms and their activities.

Temperature and pH are the two most important factors affecting microbial growth and enzymatic activities [72,73,74]. In general, a higher microbial biomass will result in a lower residual nicotine content. However, the optimal culture conditions for nicotine degradation vary among different nicotine-degrading microorganisms. For example, the optimal nicotine degradation temperature of Pseudomonas sp. CS3 was 30 Â°C and the nicotine degradation ability was sharply decreased at temperatures above 37 Â°C or below 25 Â°C. Similarly, the nicotine-degradation activity of Pseudomonas sp. Nic22 was stable at 30–34 Â°C, but greatly decreased at temperatures below 28 Â°C or above 34 Â°C. However, he optimal temperature for nicotine degradation by Pseudomonas stutzeri ZCJ was 37 Â°C. By contrast, Shinella sp. HZN7 degraded nicotine efficiently within 30–35 Â°C. Finally, P. putida S16 had a high nicotine degradation efficiency at 30 Â°C [75]. In addition to temperature, the pH also affects the growth of microorganisms, which will in turn affect the degradation of exogenous compounds. Wang et al. [76] reported that the most favorable pH for degradation of nicotine by Pseudomonas sp. CS3 was 7.0. The suitable pH ranges for nicotine catabolism of Acinetobacter sp. TW was between 7.0 and 8.0, compared to a range from 6.0 to 7.0 for Sphingomonas sp. TY. Similarly, stable degradation of nicotine by Pseudomonas geniculata N1 was observed at pH 6.0–7.5 [77]. In order to improve the degradation efficiency, temperature and pH are usually optimized together. For example, the optimum temperature for the degradation of nicotine by Ochrobactrum intermedium DN2 is 30–37 Â°C, the optimum pH is 7.0, and the average degradation rate of nicotine reaches 140.5 mg/l/h under these optimal conditions [78].

In addition, in the fermentation process, the optimization of dissolved oxygen levels and medium composition is critical for enhancing the efficiency of microbial nicotine degradation. Dissolved oxygen levels directly influence microbial metabolic activity, particularly under aerobic conditions. Studies have shown that Pseudomonas putida S16 achieves the highest nicotine degradation rate of 160 mg/L/h at a dissolved oxygen level of 50%, while the rate significantly drops to 70 mg/L/h when the oxygen level decreases to 20% [48]. Similarly, in cultures of Pseudomonas fluorescens, increasing the dissolved oxygen level from 20 to 60% resulted in approximately a 50% increase in nicotine degradation rate, along with a 40% reduction in the accumulation of intermediate metabolites [30]. Simultaneously, the degradation efficiency can also be significantly improved by adjusting the carbon and nitrogen sources as well as other auxiliary components in the medium. Shu et al. [46] reported that 3 g L−1 nicotine could be completely degraded within 5 h when the nicotine degradation experiment was carried out in 0.05 M sodium phosphate buffer (pH 7.0). By contrast, when degradation was performed with distilled water, it took more than 8 h to be fully completed. At the same time, a number of inorganic salts were also added to the experiment to observe their effects on the nicotine degradation rate. It was found that ZnSO4â‹…7H2O and NiCl2â‹…6H2O had little effect on nicotine degradation, while Na2MoO4 and CuCl2–4H2O would inhibit the degradation of nicotine [79]. Yeast extract, glucose and Tween 80 are also noteworthy [79]. In addition, glucose is an important carbon source for promoting cell growth and increasing the rate of nicotine degradation [79,80,81]. Zhao et al. and Huang et al. found that 1 g L−1 glucose can enhance nicotine degradation, although glucose had no effect in solid-state fermentation experiments [79, 82]. Similarly, Agrobacterium sp. strain S33, isolated from tobacco rhizosphere soil (Shandong, P.R. China), which can completely degrade 1.0 g L−1 nicotine in 6 h at 30 Â°C and pH 7.0, did not completely degrade nicotine within 10 h when grown on glucose–ammonium medium [39]. This means that the fermentation conditions should be tailored to each specific strain or consortium. By comprehensively optimizing factors such as temperature, pH, dissolved oxygen levels, osmotic pressure, and medium composition, the efficiency of microbial nicotine degradation during fermentation can be significantly enhanced, thereby improving the overall quality of tobacco leaves and products. These optimization strategies not only lay a solid foundation for large-scale industrial applications but also present potential for further refinement in future research.

Conclusions and perspectives

Nicotine is the most important alkaloid in tobacco, largely the quality of cigarettes and other tobacco products. Nicotine plays a critical role in smoking addiction and is well known to be harmful to human health, because it easily crosses the blood–brain barrier and biological membranes [83]. At the same time, the production and consumption of large amounts of tobacco products generates toxic and hazardous waste containing high concentrations of nicotine and other alkaloids, which also cause serious environmental problems due to a lack of recycling methods [32, 33]. According to EU regulations, these wastes are classified as "toxic and hazardous" when the nicotine content exceeds 0.5 g kg−1 [81, 84]. If left untreated, these wastes have a high potential to cause harm to human health and the environment. Nicotine has a relatively stable chemical structure, and if physical or chemical methods are used to remove nicotine, the cost will be high, there will be many harmful by-products, and sometimes even the quality of treated tobacco products will deteriorate. By contrast, microbial methods can specifically degrade nicotine [38], offering advantages in cost, efficiency, and sustainability [85].

Over the past few decades, increasing numbers of nicotine-degrading microorganisms have been isolated and identified from tobacco planting soil, tobacco leaves and tobacco waste, mainly including species of Pseudomonas, Arthrobacter, Acinetobacter, Agrobacterium, Sinorhizobium, and Sphingomonas, many of which showed high activity in degrading nicotine in tobacco leaves. Based on these early findings, researchers have conducted numerous studies on the metabolic pathways and related mechanisms of nicotine degradation by microorganisms and have successfully elucidated the pathways of several classical nicotine-degrading microorganisms, such as A. nicotinovorans [18, 86, 87], P. putida [18, 46, 58, 71], and A. tumefaciens [88, 89].

Furthermore, with the growing use of nicotine-degrading microorganisms, they have been found to show potential not only in reducing the content of nicotine, but several intermediates in the nicotine degradation pathway are important precursors for the synthesis of biologically active compounds [90]. Particularly, in Pseudomonas spp., nicotine is metabolized to produce 6-hydroxy-3-succinyl pyridine, which can be used in the synthesis of the insecticide imidacloprid and antiparkinsonian agents, as well as 2,5-dihydroxypyridine, which can be used in the synthesis of plant growth hormones and vitamin B12 [91]. However, although microbial degradation has become a major tool in the treatment of nicotine contamination, it is often limited to a few strains, such as Pseudomonas sp. HF-1 [39, 92, 93], P. putida S16 [94], Pseudomonas sp. Nic22 [38] and Acinetobacter sp. TW [95]. As research continues, the mining of new nicotine-degrading microorganisms and the molecular biology of microbial metabolism of nicotine will be the future research trends in this field (Fig. 5). However, it should be noted that much of the research has been done on the small-scale laboratory level, and it is expected that the large-scale industrial application of nicotine degrading microorganisms for tobacco product quality improvement, tobacco waste treatment or even the conversion of nicotine to produce high value-added compounds will become a research hot spot in the future. Moreover, although some metabolic pathways have been elucidated, there are still no specific strategies for effectively improving the quality of tobacco products while reducing the harmful effects of nicotine and its metabolites on humans and the environment. Therefore, it is an urgent research challenge to combine genetic modification and metabolic engineering with abundant nicotine-degrading microbial resources to achieve these goals.

Fig. 5
figure 5

Overview of potential strategies for enhancing microbial nicotine degradation through genetic modification and metabolic engineering

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Availability of data and materials

The data and materials generated during and/or analyzed during the current study are publicly available.

References

  1. Pammel LH, Library CU. A manual of poisonous plants: chiefly of eastern North America, with brief notes on economic and medicinal plants, and numerous illustrations. Iowa: Torch Press; 1911.

    Google Scholar 

  2. FAO. Food and Agriculture Organization of the United Nations. Faostat Database Collections. 2014. http://www.fao.org/faostat/en/.

  3. Hecht SS. Tobacco smoke carcinogens and lung cancer. J Natl Cancer Inst. 1999;91:53–74.

    Article  Google Scholar 

  4. Armstrong DW, Wang X, Ercal N. Enantiomeric composition of nicotine in smokeless tobacco, medicinal products, and commercial reagents. Chirality. 1998;10:587–91.

    Article  CAS  Google Scholar 

  5. Thorgeirsson TE, Geller F, Sulem P. A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature. 2008;452:638–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hawkins BT, Abbruscato TJ, Egleton RD, Brown RC, Huber JD, Campos CR, Davis TP. Nicotine increases in vivo blood–brain barrier permeability and alters cerebral microvascular tight junction protein distribution. Brain Res. 2004;1027:48–58.

    Article  CAS  PubMed  Google Scholar 

  7. Karina C, Montan MF, Cássia CD, et al. In vitro evaluation of the effect of nicotine, cotinine, and caffeine on oral microorganisms. Can J Microbiol. 2008;54:501–8.

    Article  Google Scholar 

  8. Yildiz DJT. Nicotine, its metabolism and an overview of its biological effects. Toxicon. 2004;43:619–32.

    Article  CAS  PubMed  Google Scholar 

  9. Brunnemann KD, Prokopczyk B, Djordjevic MV. Formation and analysis of tobacco-specific N-nitrosamines. Crit Rev Toxicol. 1996;26:121–37.

    Article  CAS  PubMed  Google Scholar 

  10. Campain JA. Nicotine: potentially a multifunctional carcinogen? Toxicol Sci. 2004;79:1–3.

    Article  CAS  PubMed  Google Scholar 

  11. Yildiz D, Ercal N, Armstrong DW. Nicotine enantiomers and oxidative stress. Toxicology. 1998;130:155–65.

    Article  CAS  PubMed  Google Scholar 

  12. Qiao D, Seidler FJ, Slotkin TA. Oxidative mechanisms contributing to the developmental neurotoxicity of nicotine and chlorpyrifos. Toxicol Appl Pharmacol. 2005;206:17–26.

    Article  CAS  PubMed  Google Scholar 

  13. Brandsch R. Microbiology and biochemistry of nicotine degradation. Appl Microbiol Biotechnol. 2006;69:493–8.

    Article  CAS  PubMed  Google Scholar 

  14. Baitsch D, Sandu C, Brandsch R. Gene cluster on pAO1 of Arthrobacter nicotinovorans involved in degradation of the plant alkaloid nicotine: cloning, purification, and characterization of 2,6-Dihydroxypyridine 3-Hydroxylase. J Bacteriol. 2001;183:5262–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Holmes PE, Rittenberg SC. The bacterial oxidation of nicotine. VII. Partial purification and properties of 2,6-dihydroxypyridine oxidase. J Biol Chem. 1973;247:7622–7.

    Article  Google Scholar 

  16. Sindelar RD, Rosazza JP, Barfknecht CF. N-demethylation of nicotine and reduction of nicotine-1’-N-oxide by Microsporum gypseum. Appl Environ Microbiol. 1979;38:836–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Uchida S, Maeda S, Kisaki T. Conversion of nicotine into nornicotine and N-methylmyosmine by fungi. Agric Biol Chem. 1983;47:1949–53.

    CAS  Google Scholar 

  18. Tang H, Wang L, Wang W, Yu H, Zhang K, Yao Y, Xu P. Systematic unraveling of the unsolved pathway of nicotine degradation in Pseudomonas. PLoS Genet. 2013;9: e1003923.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Wada E. Microbial degradation of the tobacco alkaloids, and some related compounds. Arch Biochem Biophys. 1957;72:145–62.

    Article  CAS  PubMed  Google Scholar 

  20. Decker K, Bleeg H. Induction and purification of stereospecific nicotine oxidizing enzymes from Arthrobacter oxidans. Biochim Biophys Acta. 1965;105:313–24.

    Article  CAS  PubMed  Google Scholar 

  21. Geiss VL, Gregory CF, Newton RP, Gravely LE. Process for reduction of nicotine content of tobacco by microbial treatment. US patent. 1979; 4557280.

  22. Civilini M, Domenis C, Sebastianutto N. Nicotine decontamination of tobacco agro-industrial waste and its degradation by micro-organisms. Waste Manage Res. 1997;15:349–58.

    Article  CAS  Google Scholar 

  23. Lenkey AA. Nicotine removal process and product produced thereby: mixing with alkaline agent in aerobic environment. US patent. 1978; 4557280.

  24. Meher KK, Panchwagh AM, Rangrass S. Biomethanation of tobacco waste. Environ Pollut. 1995;90:199–202.

    Article  CAS  PubMed  Google Scholar 

  25. Mesnard F, Girard S, Fliniaux O, Bhogal RK. Chiral specificity of the degradation of nicotine by Nicotiana plumbaginifolia cell suspension cultures. Plant Sci. 2001;161:1011–8.

    Article  CAS  Google Scholar 

  26. Carl B, Arnold A, Hauer B. Sequence and transcriptional analysis of a gene cluster of Pseudomonas putida 86 involved in quinoline degradation. Gene. 2004;331:177–88.

    Article  CAS  PubMed  Google Scholar 

  27. Grether-Beck S, Igloi GL, Pust S, Schilz E, Decker K. Structural analysis and molybdenum-dependent expression of the pAO1-encoded nicotine dehydrogenase genes of Arthrobacter nicotinovorans. Mol Microbiol. 1994;13:929–36.

    Article  CAS  PubMed  Google Scholar 

  28. Igloi GL, Brandsch R. Sequence of the 165-Kilobase catabolic plasmid pAO1 from Arthrobacter nicotinovorans and identification of a pAO1-dependent nicotine uptake system. J Bacteriol. 2003;185:1976–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Koetter J, Schulz G. Crystal structure of 6-hydroxy-D-nicotine oxidase from Arthrobacter nicotinovorans. J Mol Biol. 2005;352:418–28.

    Article  CAS  PubMed  Google Scholar 

  30. Yuan YJ, Lu ZX, Huang LJ, Bie XM, Lu FX, Li Y. Optimization of a medium for enhancing nicotine biodegradation by Ochrobactrum intermedium DN2. J Appl Microbiol. 2006;101:691–7.

    Article  CAS  PubMed  Google Scholar 

  31. Eberhardt H. The biological degradation of nicotine by nicotinophilic microorganisms. Beitrage zur Tabakforschung Int. 1995;16:119–29.

    CAS  Google Scholar 

  32. Li H, Li X, Duan Y, Zhang KQ, Yang J. Biotransformation of nicotine by microorganism: the case of Pseudomonas spp. Appl Microbiol Biotechnol. 2010;86:11–7.

    Article  CAS  PubMed  Google Scholar 

  33. Raman G, Sakthivel N. Current status on biochemistry and molecular biology of microbial degradation of nicotine. Sci World J. 2013;2013:1653–6.

    Google Scholar 

  34. Reid JJ, Gribbons MF, Haley DE. The fermentation of cigar leaf tobacco as influenced by the addition of yeast. J Agric Res. 1944;69:373–81.

    Google Scholar 

  35. Gutierrez R, Spain S. Nicotine degradation by bacteria, 2: Enterobacter cloacae as nicotine degrader. Degrader (Spain). 1983;22:85–98.

    Google Scholar 

  36. Wang S, Xu P, Tang H. Biodegradation and detoxification of nicotine in tobacco solid waste by a Pseudomonas sp. Biotechnol Lett. 2004;26:1493–6.

    Article  CAS  PubMed  Google Scholar 

  37. Yuan YJ, Lu ZX, Wu N, Huang LJ. Biodegradation, isolation and preliminary characterization of a novel nicotine-degrading bacterium, Ochrobactrum intermedium DN2. Int Biodeterior Biodegrad. 2005;56:45–50.

    Article  CAS  Google Scholar 

  38. Chen C, Li X, Yang J, Gong X, Bing L, Zhang KQ. Isolation of nicotine-degrading bacterium Pseudomonas sp. Nic22, and its potential application in tobacco processing. Int Biodeterior Biodegrad. 2008;62:226–31.

    Article  CAS  Google Scholar 

  39. Wang SN, Liu Z, Xu P. Biodegradation of nicotine by a newly isolated Agrobacterium sp. strain S33. J Appl Microbiol. 2009;107:838–47.

    Article  CAS  PubMed  Google Scholar 

  40. Ma G. Diversity and phylogenetic analyses of nicotine-degrading bacteria isolated from tobacco plantation soils. Afr Microbiol Res. 2012;6:6392–8.

    CAS  Google Scholar 

  41. Raman G, Mohan K, Manohar V, Sakthivel N. Biodegradation of nicotine by a novel nicotine-degrading bacterium, Pseudomonas plecoglossicida TND35 and its new biotransformation intermediates. Biodegradation. 2014;25:95–107.

    Article  CAS  PubMed  Google Scholar 

  42. Chen B, Sun L, Zeng G, Shen Z, Wang K, Yin L, Xu F, Wang P, Ding Y, Nie Q, Wu Q, Zhang Z, Xia J, Lin J, Luo Y, Cai J, Krausz KW, Zheng R, Xue Y, Zheng MH, Li Y, Yu C, Gonzalez FJ, Jiang C. Gut bacteria alleviate smoking-related NASH by degrading gut nicotine. Nature. 2022;610:562–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Liu J, Ma G, Chen T, Hou Y, Yang S, Zhang KQ, Yang J. Nicotine-degrading microorganisms and their potential applications. Appl Microbiol Biotechnol. 2015;99:3775–85.

    Article  CAS  PubMed  Google Scholar 

  44. Huang C, Shan L, Chen Z, He Z, Li J, Yang Y, Shu M, Pan F, Jiao Y, Zhang F, Linhardt RJ, Zhong W. Differential effects of homologous transcriptional regulators NicR2A, NicR2B1, and NicR2B2 and endogenous ectopic strong promoters on nicotine metabolism in Pseudomonas sp. Strain JY-Q. Appl Environ Microbiol. 2021;87:e02457-e2520.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Chiribau CB, Sandu C, Igloi GL, Brandsch R. Characterization of PmfR, the transcriptional activator of the pAO1-borne purU-mabO-folD operon of Arthrobacter nicotinovorans. J Bacteriol. 2005;187:3062–270.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Shu NW, Zhen L, Hong ZT, Jing M, Ping X. Characterization of environmentally friendly nicotine degradation by biotype A strain S16. Microbiology-Sgm. 2007;153:1556–65.

    Article  Google Scholar 

  47. Ganas P, Sachelaru P, Mihasan M, Igloi GL, Brandsch R. Two closely related pathways of nicotine catabolism in Arthrobacter nicotinovorans and Nocardioides sp. strain JS614. Arch Microbiol. 2008;189:511–7.

    Article  CAS  PubMed  Google Scholar 

  48. Tang H, Wang L, Meng X, Ma L, Wang S, He X, Geng W, Ping X. A novel gene, encoding a nicotine oxidoreductase, involved in nicotine degradation by Pseudomonas putida Strain S16. Appl Environ Microbiol. 2008;74:1567–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Tang H, Wang L, Meng X, Ma L, Wang S, He X, Wu G, Xu P. Novel nicotine oxidoreductase-encoding gene involved in nicotine degradation by Pseudomonas putida strain S16. Appl Environ Microbiol. 2009;75:772–8.

    Article  CAS  PubMed  Google Scholar 

  50. Mihasan M, Brandsch R. pAO1 of Arthrobacter nicotinovorans and the spread of catabolic traits by horizontal gene transfer in gram-positive soil bacteria. J Mol Evol. 2013;77:22–30.

    Article  CAS  PubMed  Google Scholar 

  51. Meng XJ, Lu LL, Gu GF, Xiao M. A novel pathway for nicotine degradation by Aspergillus oryzae 112822 isolated from tobacco leaves. Res Microbiol. 2010;161:626–33.

    Article  CAS  PubMed  Google Scholar 

  52. Grether-Beck S, Igloi GL, Pust S, Schilz E, Decker K, Brandsch R. Structural analysis and molybdenum-dependent expression of the pAO1-encoded nicotine dehydrogenase genes of Arthrobacter nicotinovorans. Mol Microbiol. 1994;13:929–36.

    Article  CAS  PubMed  Google Scholar 

  53. Chiribau CB, Sandu C, Fraaije M, Schiltz E, Brandsch R. A novel gamma-N-methylaminobutyrate demethylating oxidase involved in catabolism of the tobacco alkaloid nicotine by Arthrobacter nicotinovorans pAO1. Eur J Biochem. 2004;271:4677–84.

    Article  CAS  PubMed  Google Scholar 

  54. Sachelaru P, Schiltz E, Igloi GL, Brandsch R. An alpha/beta-fold C-C bond hydrolase is involved in a central step of nicotine catabolism by Arthrobacter nicotinovorans. J Bacteriol. 2005;187:8516–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Zhao-Shea R, Liu L, Soll LG, Improgo MR, Meyers EE, McIntosh JM, Grady SR, Marks MJ, Gardner PD, Tapper AR. Nicotine-mediated activation of dopaminergic neurons in distinct regions of the ventral tegmental area. Neuropsychopharmacology. 2011;36:1021–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Wada E, Yamasaki K. Degradation of nicotine by soil bacteria. J Am Chem Soc. 1954;76:155–7.

    Article  CAS  Google Scholar 

  57. Tang H, Yao Y, Zhang D, Meng X, Wang L, Yu H, Ma L, Xu P. A novel NADH-dependent and FAD-containing hydroxylase is crucial for nicotine degradation by Pseudomonas putida. J Biol Chem. 2011;286:39179–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Tang H, Yao Y, Wang L, Yu H, Ren Y, Wu G, Xu P. Genomic analysis of Pseudomonas putida: genes in a genome island are crucial for nicotine degradation. Sci Rep. 2012;2:377.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Xue S, Schlosburg JE, Janda KD. A new strategy for smoking cessation: characterization of a bacterial enzyme for the degradation of nicotine. J Am Chem Soc. 2015;137:10136–9.

    Article  CAS  PubMed  Google Scholar 

  60. Thisted T, Biesova Z, Walmacq C, Stone E, Rodnick-Smith M, Ahmed SS, Horrigan SK, Van Engelen B, Reed C, Kalnik MW. Optimization of a nicotine degrading enzyme for potential use in treatment of nicotine addiction. BMC Biotechnol. 2019;19:56.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Zhang H, Zhao R, Huang C, Li J, Shao Y, Xu J, Shu M, Zhong W. Selective and faster nicotine biodegradation by genetically modified Pseudomonas sp. JY-Q in the presence of glucose. Appl Microbiol Biotechnol. 2019;103:339–48.

    Article  CAS  PubMed  Google Scholar 

  62. Su Y, Xian H, Shi S, Zhang C, Manik SM, Mao J, Zhang G, Liao W, Wang Q, Liu H. Biodegradation of lignin and nicotine with white rot fungi for the delignification and detoxification of tobacco stalk. BMC Biotechnol. 2016;16:81.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Frankenburg WG. Transformation products of nicotine in fermented leaves. Science. 1948;107:427–8.

    Article  CAS  PubMed  Google Scholar 

  64. Frankenburg WG, Vaitekunas AA. Chemical studies on nicoine degradation by microorganism derived from the surface of tobacco seeds. Croesta. 1957;1:1–34.

    Google Scholar 

  65. Briški F, Horgas N, Vuković M, Gomzi Z. Aerobic composting of tobacco industry solid waste—simulation of the process. Clean Technol Environ Policy. 2003;5:295–301.

    Article  Google Scholar 

  66. Ruan A, Min H, Peng X, Huang Z. Isolation and characterization of Pseudomonas sp. strain HF-1, capable of degrading nicotine. Res Microbiol. 2005;156:700–6.

    Article  CAS  PubMed  Google Scholar 

  67. Xia ZY, Lei LP, Wu YP, Guo RJ. Isolation and identification of degrading nicotine bacteria-Arthrobacter nicotianae strain K9. Chin Tob Sci. 2006;2:1–4.

    Google Scholar 

  68. Zhao M, Wang B, Li F, Qiu L, Li F, Wang S, Cui J. Analysis of bacterial communities on aging flue-cured tobacco leaves by 16S rDNA PCR-DGGE technology. Appl Microbiol Biotechnol. 2007;73:1435–40.

    Article  CAS  PubMed  Google Scholar 

  69. English CF, Bell EJ, Berger AJ. Isolation of thermophiles from broadleaf tobacco and effect of pure culture inoculation on cigar aroma and mildness. Appl Microbiol. 2007;15:117–9.

    Article  Google Scholar 

  70. Wang SN. Green route to 6-Hydroxy-3-succinoyl-pyridine from (S)-Nicotine of tobacco waste by whole cells of a Pseudomonas sp. Environ Sci Technol. 2005;39:6877–80.

    Article  CAS  PubMed  Google Scholar 

  71. Kaelin P, Morel P, Gadani F. Isolation of Bacillus thuringiensis from stored tobacco and Lasioderma serricorne (F.). Appl Environ Microbiol. 1994;60:19–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. El Hajjouji H, Ait Baddi G, Yaacoubi A, Hamdi H, Winterton P, Revel JC, Hafidi M. Optimisation of biodegradation conditions for the treatment of olive mill wastewater. Bioresour Technol. 2008;99:5505–10.

    Article  PubMed  Google Scholar 

  73. Hung YJ, Peng CC, Tzen JT, Chen MJ, Liu JR. Immobilization of neocallimastix patriciarum xylanase on artificial oil bodies and statistical optimization of enzyme activity. Bioresour Technol. 2008;99:8662–6.

    Article  CAS  PubMed  Google Scholar 

  74. Yus Azila Y, Mashitah MD, Bhatia S. Process optimization studies of lead (Pb(II)) biosorption onto immobilized cells of Pycnoporus sanguineus using response surface methodology. Bioresour Technol. 2008;99:8549–52.

    Article  CAS  PubMed  Google Scholar 

  75. Wang HH, Yin B, Peng XX, Wang JY, Xie ZH, Gao J, Tang XK. Biodegradation of nicotine by newly isolated Pseudomonas sp. CS3 and its metabolites. J Appl Microbiol. 2012;112:258–68.

    Article  CAS  PubMed  Google Scholar 

  76. Wang M, Yang G, Wang X, Yao Y, Lu ZM. Nicotine degradation by two novel bacterial isolates of Acinetobacter sp. TW and Sphingomonas sp. TY and their responses in the presence of neonicotinoid insecticides. World J Microbiol Biotechnol. 2010;27:1633–40.

    Article  Google Scholar 

  77. Xu P, Yu B, Li FL, Cai XF, Ma CQ. Microbial degradation of sulfur, nitrogen and oxygen heterocycles. Trends Microbiol. 2006;14:398–405.

    Article  CAS  PubMed  Google Scholar 

  78. Yuan YJ, Lu ZX, Huang LJ, Li Y, Lu FX, Bie XM, Teng YQ, Lin Q. Biodegradation of nicotine from tobacco waste extract by Ochrobactrum intermedium DN2. J Ind Microbiol Biotechnol. 2007;34:567–70.

    Article  CAS  PubMed  Google Scholar 

  79. Zhao L, Zhu C, Gao Y, Wang C, Li X, Shu M, Shi Y, Zhong W. Nicotine degradation enhancement by Pseudomonas stutzeri ZCJ during aging process of tobacco leaves. World J Microbiol Biotechnol. 2012;28:2077–86.

    Article  CAS  PubMed  Google Scholar 

  80. Ruan A, Min H, Zhu W. Studies on biodegradation of nicotine by Arthrobacter sp. strain HF-2. J Environ Sci Health B. 2006;41:1159–70.

    Article  CAS  PubMed  Google Scholar 

  81. Zhong W, Zhu C, Shu M, Sun K, Zhao L, Wang C, Ye Z, Chen J. Degradation of nicotine in tobacco waste extract by newly isolated Pseudomonas sp. ZUTSKD Bioresour Technol. 2010;101:6935–41.

    Article  CAS  PubMed  Google Scholar 

  82. Huang J, Yang J, Duan Y, Gu W, Gong X, Zhe W, Su C, Zhang KQ. Bacterial diversities on unaged and aging flue-cured tobacco leaves estimated by 16S rRNA sequence analysis. Appl Microbiol Biotechnol. 2010;88:553–62.

    Article  CAS  PubMed  Google Scholar 

  83. Schievelbein H. Nicotine, resorption and fate. Pharmacol Ther. 1982;18:233–48.

    Article  CAS  PubMed  Google Scholar 

  84. Payne RB, May HD, Sowers KR. Enhanced reductive dechlorination of polychlorinated biphenyl impacted sediment by bioaugmentation with a dehalorespiring bacterium. Environ Sci Technol. 2011;45:8772–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Schenk S, Decker K. Horizontal gene transfer involved in the convergent evolution of the plasmid-encoded enantioselective 6-hydroxynicotine oxidases. J Mol Evol. 1999;48:178–86.

    Article  CAS  PubMed  Google Scholar 

  86. Sandu C, Chiribau CB, Brandsch R. Characterization of HdnoR, the transcriptional repressor of the 6-hydroxy-D-nicotine oxidase gene of Arthrobacter nicotinovorans pAO1, and its DNA-binding activity in response to L- and D-nicotine derivatives. J Biol Chem. 2003;278:51307–15.

    Article  CAS  PubMed  Google Scholar 

  87. Mihasan M, Chiribau CB, Friedrich T, Artenie V, Brandsch R. An NAD(P)H-nicotine blue oxidoreductase is part of the nicotine regulon and may protect Arthrobacter nicotinovorans from oxidative stress during nicotine catabolism. Appl Environ Microbiol. 2007;73:2479–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Shuning W, Haiyan H, Kebo X, Ping XJ. Identification of nicotine biotransformation intermediates by Agrobacterium tumefaciens strain S33 suggests a novel nicotine degradation pathway. Appl Microbiol Biotechnol. 2015;95:1567–78.

    Google Scholar 

  89. Li H, Xie K, Huang H, Wang S. 6-Hydroxy-3-succinoylpyridine hydroxylase catalyzes a central step of nicotine degradation in Agrobacterium tumefaciens S33. PLoS ONE. 2014;9: e103324.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Deborah AR, Bruce NC. Microbial transformation of alkaloids. Curr Opin Microbiol. 2002;5:274–81.

    Article  Google Scholar 

  91. Nakano H, Wieser M, Hurh B, Kawai T, Yoshida T, Yamane T, Nagasawa T. Purification, characterization and gene cloning of 6-hydroxynicotinate 3-monooxygenase from Pseudomonas fluorescens TN5. Eur J Biochem. 1999;260:120–6.

    Article  CAS  PubMed  Google Scholar 

  92. Wang MZ, Zheng X, He HZ, Shen DS, Feng HJ. Ecological roles and release patterns of acylated homoserine lactones in Pseudomonas sp. HF-1 and their implications in bacterial bioaugmentation. Bioresour Technol. 2012;125:119–26.

    Article  CAS  PubMed  Google Scholar 

  93. Zhang K, Zheng X, Shen DS, Wang MZ, Feng HJ, He HZ, Wang S, Wang JH. Evidence for existence of quorum sensing in a bioaugmented system by acylated homoserine lactone-dependent quorum quenching. Environ Sci Pollut Res Int. 2015;22:6050–6.

    Article  CAS  PubMed  Google Scholar 

  94. Yu H, Tang H, Xu P. Green strategy from waste to value-added-chemical production: efficient biosynthesis of 6-hydroxy-3-succinoyl-pyridine by an engineered biocatalyst. Sci Rep. 2014;4:5397.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Wang JH, He HZ, Wang MZ, Wang S, Zhang J, Wei W. Bioaugmentation of activated sludge with Acinetobacter sp. TW enhances nicotine degradation in a synthetic tobacco wastewater treatment system. Bioresour Technol. 2013;142:445–53.

    Article  CAS  PubMed  Google Scholar 

  96. Hongjuan L, Yanqing D, Guanghui M, Liping L, Keqin Z. Isolation and characterization of Acinetobacter sp. ND12 capable of degrading nicotine. Afr J Microbiol Res. 2011;5:1335–41.

    Article  Google Scholar 

  97. Wang M, Yang G, Wang X, Yao Y, Min H, Lu Z. Nicotine degradation by two novel bacterial isolates of Acinetobacter sp. TW and Sphingomonas sp. TY and their responses in the presence of neonicotinoid insecticides. World J Microbiol Biotechnol. 2011;27:1633–40.

    Article  CAS  Google Scholar 

  98. Ruan A, Zhu HM. Studies on biodegradation of nicotine by Arthrobacter sp. Strain HF-2. J Environ Sci Health B. 2006;41:1159–70.

    Article  CAS  PubMed  Google Scholar 

  99. Yao Y, Tang H, Ren H, Yu H, Wang L. Genome sequence of a nicotine-degrading strain of Arthrobacter. J Bacteriol. 2012;194:5714–4715.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Ruan A, Gao Y, Fang C, Xu Y. Isolation and characterization of a novel nicotinophilic bacterium, Arthrobacter sp. aRF-1 and its metabolic pathway. Biotechnol Appl Biochem. 2018;65:848–56.

    Article  CAS  PubMed  Google Scholar 

  101. Deng NN, Luo D, Zhong J, Zhou JY, Tan H. Identification and degradation optimization of a high nicotine endurance strain Arthrobacter sp. AH14. J Agric Sci Technol. 2016;18:62–71.

    CAS  Google Scholar 

  102. Jiang Y, Gong J, Chen Y, Hu B, Sun J, Zhu Y, Xia Z, Zou C. Biodegradation of nicotine and TSNAs by Bacterium sp. Strain J54. J Agric Sci Tech. 2021;18:62–71.

    Google Scholar 

  103. Lei L, Zhang W, Wei H, Xia Z, Liu XZ. Characterization of a novel nicotine-degrading Ensifer sp. strain N7 isolated from tobacco rhizosphere. Ann Microbiol. 2009;59:247–52.

    Article  CAS  Google Scholar 

  104. Yu H, Tang H, Zhu X, Li Y, Xu P. Molecular mechanism of nicotine degradation by a newly isolated strain, Ochrobactrum sp. strain SJY1. Appl Environ Microbiol. 2015;81:272–81.

    Article  PubMed  Google Scholar 

  105. Civilini M, Domenis C, Sebastianutto N. Nicotine decontamination of tobacco agro-industrial waste and its degradation by microorganisms. Waste Manag Res. 1997;15:349–58.

    Article  CAS  Google Scholar 

  106. Gong XW, Yang JK, Duan YQ, Dong JY, Zhe W, Le W, Li QH, Zhang K. Isolation and characterization of Rhodococcus sp. Y22 and its potential application to tobacco processing. Res Microbiol. 2009;160:200–4.

    Article  CAS  PubMed  Google Scholar 

  107. Weihong Z, Chenjing Z, Ming S, Kedan S, Lei Z, Chang W, Zhijuan Y, Jianmeng C. Degradation of nicotine in tobacco waste extract by newly isolated Pseudomonas sp. ZUTSKD. Bioresour Technol. 2015;101:6935–41.

    Google Scholar 

  108. Qiu J, Ma Y, Chen L, Wu L, Wen Y, Liu W. A sirA-like gene, sirA2, is essential for 3-succinoyl-pyridine metabolism in the newly isolated nicotine-degrading Pseudomonas sp. HZN6 strain. Appl Microbiol Biotechnol. 2011;92:1023–32.

    Article  CAS  PubMed  Google Scholar 

  109. Li J, Qian S, Xiong L, Zhu C, Shu M, Wang J, Jiao Y, He H, Zhang F, Linhardt RJ, Zhong W. Comparative genomics reveals specific genetic architectures in nicotine metabolism of Pseudomonas sp. JY-Q. Front Microbiol. 2017;8:2085.

    Article  PubMed  PubMed Central  Google Scholar 

  110. Pan D, Sun M, Wang Y, Lv P, Wu X, Li QX, Cao H, Hua R. Characterization of nicotine catabolism through a novel pyrrolidine pathway in Pseudomonas sp. S-1. J Agric Food Chem. 2018;66:7393–401.

    Article  CAS  PubMed  Google Scholar 

  111. Li A, Qiu J, Chen D, Ye J, Wang Y, Tong L, Jiang J, Chen J. Characterization and genome analysis of a nicotine and nicotinic acid-degrading strain Pseudomonas putida JQ581 isolated from marine. Mar Drugs. 2017;15:1023–32.

    Article  Google Scholar 

  112. Liu R, Bao ZX, Zhao PJ, Li GH. Advances in the study of metabolomics and metabolites in some species interactions. Molecules. 2021;26:3311.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Xia ZY, Yu Q, Lei LP, Wu YP, Ren K, Li Y, Zou CM. A novel nicotine-degrading bacterium Pseudomonas fluorescens strain 1206. Appl Biochem Microbiol. 2019;55(2):123–8.

    Article  CAS  Google Scholar 

  114. Ma Y, Wen R, Qiu J, Hong J, Liu M, Zhang D. Biodegradation of nicotine by a novel strain Pusillimonas. Res Microbiol. 2015;166:67–71.

    Article  CAS  PubMed  Google Scholar 

  115. Wei H, Lei L, Xia Z. Characterisation of a novel aerobic nicotine-biodegrading strain of Pseudomonas putida. Ann Microbiol. 2008;58:41–5.

    Article  CAS  Google Scholar 

  116. Jiang HJ, Wu FL, Chen SL, Qiu GJ, Ma Y. Biodegradation of nicotine by a novel strain Shinella sp. HZN1 isolated from activated sludge. J Environ Sci Health B. 2011;46:703–8.

    CAS  PubMed  Google Scholar 

  117. Uchida S, Maeda S, Kisaki TJA, Chemistry B. Conversion of nicotine into nornicotine and N-methylmyosmine by fungi. Agric Biol Chem. 1983;47:1949–53.

    CAS  Google Scholar 

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  1. School of Life Sciences, Taizhou University, Taizhou, 318000, Zhejiang, People’s Republic of China

    Jie Huang, Yi-Qian Chi, You-Xuan Lu & Feng-Wei Yin

  2. School of Food Science and Pharmaceutical Engineering, Nanjing Normal University, Nanjing, 210000, People’s Republic of China

    Zi-Jia Li, Dong-Dong Yang & Zhi-Yun Wei

  3. Taizhou Key Laboratory of Biomass Functional Materials Development and Application, Taizhou University, Taizhou, 318000, Zhejiang, People’s Republic of China

    Feng-Wei Yin

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FW.Y designed the work; ZJ.L,DD.Y and ZY.W wrote the main manuscript text; J.H,YQ.C and YX.L prepared the figures. All authors reviewd the manuscript.

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Li, ZJ., Yang, DD., Wei, ZY. et al. Reduction of nicotine content in tobacco through microbial degradation: research progress and potential applications. Biotechnol Biofuels 17, 144 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13068-024-02593-3

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Biotechnology for Biofuels and Bioproducts

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