Review

The divergence between the virus and cellular oxidative stress as separate environmental agents that trigger autoimmunity originates from their different procedural mechanisms of activating the same molecular entity: the transcription factor NF-kappa B

  • To happen, autoimmunity in man requires triggering by environmental factors: the viruses and cellular stress, in genetically primed individuals. The viruses and stress are operatives in this scene as stimuli for the activation of the transcription factor (TF), NF-ΚB. NF-ΚB is unusually activated: the viral activation occurs via serine residues-phosphorylation by IKKβ and IKKε, while the activation by oxidative stress occurs via tyrosine phosphorylation of IΚBα. The phosphorylation of particular amino acid residues of a given protein molecule modulates that protein’s polymorphic conformations, appropriately. For a TF, a given conformation influences its choice of cognate DNA sequence recognition as well as its interactions with neighboring molecules. The TF NF-ΚB performs a battery of regulatory functions. Because it is variously phosphorylated as seen above this implies that NF-ΚB is capable of assuming a multitude of polymorphic conformations that we refer to as “derivative isoforms”. Thus the virus activation of NF-ΚB occurring by phosphorylation at serines S536 and S468 is observed to generate the isoforms with the potential to activate the transcription of viral latency genes, hereby installing a latent infection. But oxidative stress activation of NF-ΚB occurs via phosphorylation of Tyr42 of IΚBα and this yields isoforms that activate the transcription of replication and transcription activator (RTA), the master lytic switch, which thereby abrogates the latency. The steps involved are that the stress-activated NF-ΚB and the viral miRNAs conjoin in a regulatory circuitry identified as feedback and feed-forward network motifs that co-accomplish the switching on of RTA which in turn activates the transcription of the immediate early genes BZLF1 and BRLF1. These two latter genes together mobilize the expression of the set of lytic genes, resulting in a lytic cascade and consequentially set in trend the viral journey to the triggering of autoimmunity (Figure 1).

    Citation: Norbert O. Temajo, Neville Howard. The divergence between the virus and cellular oxidative stress as separate environmental agents that trigger autoimmunity originates from their different procedural mechanisms of activating the same molecular entity: the transcription factor NF-kappa B[J]. AIMS Allergy and Immunology, 2017, 1(2): 50-61. doi: 10.3934/Allergy.2017.2.50

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  • To happen, autoimmunity in man requires triggering by environmental factors: the viruses and cellular stress, in genetically primed individuals. The viruses and stress are operatives in this scene as stimuli for the activation of the transcription factor (TF), NF-ΚB. NF-ΚB is unusually activated: the viral activation occurs via serine residues-phosphorylation by IKKβ and IKKε, while the activation by oxidative stress occurs via tyrosine phosphorylation of IΚBα. The phosphorylation of particular amino acid residues of a given protein molecule modulates that protein’s polymorphic conformations, appropriately. For a TF, a given conformation influences its choice of cognate DNA sequence recognition as well as its interactions with neighboring molecules. The TF NF-ΚB performs a battery of regulatory functions. Because it is variously phosphorylated as seen above this implies that NF-ΚB is capable of assuming a multitude of polymorphic conformations that we refer to as “derivative isoforms”. Thus the virus activation of NF-ΚB occurring by phosphorylation at serines S536 and S468 is observed to generate the isoforms with the potential to activate the transcription of viral latency genes, hereby installing a latent infection. But oxidative stress activation of NF-ΚB occurs via phosphorylation of Tyr42 of IΚBα and this yields isoforms that activate the transcription of replication and transcription activator (RTA), the master lytic switch, which thereby abrogates the latency. The steps involved are that the stress-activated NF-ΚB and the viral miRNAs conjoin in a regulatory circuitry identified as feedback and feed-forward network motifs that co-accomplish the switching on of RTA which in turn activates the transcription of the immediate early genes BZLF1 and BRLF1. These two latter genes together mobilize the expression of the set of lytic genes, resulting in a lytic cascade and consequentially set in trend the viral journey to the triggering of autoimmunity (Figure 1).


    Abbreviations:

    Cd Cadmium Co Cobalt
    CFU Colony Formation Unity Hg Mercury
    IAA Indole Acetic Acid NA Nutrient agar
    OD Optical density Pb Lead
    SE Solubilization Effiency
    YEM Yeast Extract Mannitol
    PGPR Plant Growth Promotion Rhizobacter
    NBRIP National Botanical Research Institute's Phosphate

    1. Introduction

    The Bombon plateu is located on the high Andes of Junin, Peru. It is known for its dry climate, extremely low temperatures and acidic soils (pH < 5) with relatively high concentration of toxic heavy metals. Among these, low temperatures and soil contamination are common problems which affect farmers of this region, together, these two factors diminish the yield of economically important crops such as maca (Lepidium meyenii Walp.) a Brassicaceae whose roots are used as food. Quality of the crop is also affected reducing its demand in international markets.

    The soil is a habitat for a wide variety of microorganisms. The rhizosphere, an area surrounding plant roots, is a special ecological niche that supports a vast group of metabolically versatile microorganisms [1]. Among these, plant growth promoting rhizobacteria (PGPR) are considered of great importance due to their ability to solubilize inorganic phosphates, transport iron, produce phytohormones like indole acetic acid (IAA) [2] and fix atmospheric nitrogen [3]. These attributes allow those microbes to induce plant growth and development. In this study, PGPRs can be considered as a biological alternative to improve the yield and growth of crops growing in the high Andes under harsh environmental conditions. In this context, the aims of this research were to select and characterize psychrotrophic bacteria isolated from maca rhizosphere by testing their plant growth promoting ability and tolerance to heavy metals. There are only few studies that explore the application of biofertilizers based on psychotrophic bacteria with PGPR characteristics, adapted to the harsh climatic conditions of the high Andean region and with potential to bioremediate soils contaminated with heavy metals.


    2. Materials and Methods


    2.1. Sampling and isolation of bacteria

    Soil samples were collected from fields in the Comunidad Campesina San Pedro de Cajas, Province of Tarma-Junin (located at 4100 meters above sea level). Maximum and minimum soil temperatures were 22 ℃ and 6 ℃, respectively, with a relative humidity of 55.2%. Three locations were sampled: Galpón Condorín (Length W 75°53'49.54'' Latitude S 11°15'12.18''), Acomachay (Length W 75°53'38.64'' Latitude S 11°14'15.24'') and Condorín (Lenght W 81°23'42'' Latitude S 82°7'32.01'') which were either at the stage of first harvest, second harvest and 10 years of land fallow (without planting any crop), respectively. Rhizosphere and soil samples were collected from different plants. Each plant was taken completely along with their associated soil. Moreover, 500 g of soil was also collected from the area lacking any plant material. Samples were processed later in accordance with the methodologies established by APHA (1998) [4] for isolation of viable aerobic bacteria. Temperature and time of incubation was modified to 6 ℃ for 7 days to obtain isolates with the ability to grow at low temperatures. Rhizosphere and soil samples were also characterized for their physico-chemical properties like pH, conductivity, texture, organic matter, nutrients, among others.


    2.2. Bacterial growth at different temperatures

    Isolates were grown in Nutrient Agar (NA) medium and incubated at 6 ℃, 12 ℃, 22 ℃ and 28 ℃ [5] in order to determine their nature as psychrotrophic or psychrophilic bacteria. Growth was evaluated after 7 days of incubation and results were expressed on a scale of 1 to 4 (where 4 represent the maximum colony growth).


    2.3. Characterization of IAA production

    IAA production was estimated using the colorimetric technique based on the Salkowski reagent [6]. Strains were grown in 5 ml of Yeast Extract Mannitol (YEM) broth suplemented with 5 mM L-tryptophan and were incubated at 6 ℃, 12 ℃ and 22 ℃ for 28, 19 and 11 days, respectively. Salkowski reagent (1:4) [7] was added to each culture media and the mix was kept in the dark for 30 min. Positive samples turned from shades of pink to intense rose. Optical density (OD) was registrated at 530 nm to measure IAA production. The amount of IAA in μg/ml was calculated by plotting a standard curve [8].


    2.4. Phosphate solubilization capacity of bacteria

    Isolates were grown in YEM broth and incubated at 6 ℃, 12 ℃ and, 22 ℃ for 28, 19 and 11 days, respectively. Five μl of each culture at a concentration of 108 CFU/ml [9] was inoculated in National Botanical Research Institute's Phosphate (NBRIP) basal medium plates supplemented with di-calcium (CaHPO4) or tri-calcium (Ca3(PO4)2) phosphate [10]. Plates were incubated at 6 ℃ and 12 ℃ for 36 days and at 22 ℃ for 8 days. Strains with a translucent halo around the colony were considered positive for phosphate solubilization.


    2.5. Seed germination assay

    Strains for this assay were selected according to positive results obtained on at least one of the in vitro PGPR traits. Red clover (Trifolium pratense) seeds were used as a model plant to evaluate the efficacy of the isolates on germination promotion. Disinfection and inoculation of seeds (106 UFC/ml) was carried out following the methodology described by Ogata and Zúñiga [12]. Seeds were incubated at 12 ℃ or 22 ℃ after inoculation. Inoculation with water was used as control. Each experimental unit consisted of 25 inoculated seeds in a water agar (0.75%) plate. Four replicates were used for each treatment. The percentage of germination was evaluated with the following formula:

    %G=NumberofgerminatedseedsTotalnumberofseeds×100

    2.6. Heavy metal resistance

    All strains tested in the germination assay were also evaluated for their ability to grow in the presence of four heavy metals: Pb (lead trihydrate), Cd (cadmium chloride), Co (cobalt chloride) and Hg (mercury chloride Ⅱ). The assay was conducted following the method described by Lalitha [13] using 0.5 mM Cd, Pb or Co and 0.01 mM Hg [14]. In addition, a mixture of all metals at 0.5 mM was also used. Strains resistant to the different metals tested were further evaluated for their minimum inhibitory concentration (MIC) using Pb and Cd separately. The assay was conducted using 8 concentrations (0.005, 0.01, 0.05, 0.1, 0.5, 1, 2.5 and 5 mM) of each heavy metal on NA medium adjusted to pH 5 [14] and incubated at 6 ℃ for 30 days.


    2.7. Molecular identification and phylogenetic analysis

    Molecular identification was carried out using 16S rDNA gene polymerase chain reaction (PCR) amplification and sequencing by using primer pair fD1 (5'-CCGAATTCGTCGACAACAGAGTTTGATCCTGGCTCAG-3') and rD1 (5'-CCCGGGATCCAAGCTTAAGGAGGTGATCCAGCC-3') [15]. The ClustalX2 software [16] was used for alignment of sequences generated in this study along with sequences obtained from databases. Phylogenetic relationships were established with the neighbor-joining (NJ) method and distances calculated according to the Kimura-2 parameter model using the MEGA6 software [17].


    3. Results and Discussion


    3.1. Isolation of PGPR

    Physicochemical characterization of the soils samples revealed that they were non-saline, moderately thick with sandy loam consistency and acidic (pH values ranging from 4 to 5). Concentrations of the metals such as B, Fe, Mn, Cu, Zn and Cr were in the range of 13.86–18.87 ppm. The concentration of lead (Pb) was in the range of 33.92–56.14 ppm while that of cadmium (Cd) was between 1.43–1.98 ppm. Based on the Environmental Quality Standards of agricultural soils, the samples slightly exceded the maximum permissible values of Cd but not of Pb. According to the Peruvian normative, concentrations under 70 ppm and 1.4 ppm of Pb and Cd, respectively, are allowed for agricultural soil.

    A total of 44 bacterial strains were isolated: 8 from Galpón Condorín (1st year of harvest), 30 from Acomachay (2nd year of harvest) and 6 from Condorin (10 years of rest). Twenty three were isolated from the rhizosphere and 21 from non-rhizospheric soil. Growth at different temperatures, showed that more than 59% of the strains have a growth level of 4 when they were incubated at 12 ℃, 22 ℃ and 28 ℃ (Figure 1). All isolates grew at 12 ℃ and 6 ℃. These results may be related to their origin in the high andean zone, where soils reach very low temperatures (close to 0 ℃) during the freezing season. Their versatility to grow at different temperatures indicated that the strains belong to the psychrotrophic group (Przemieniecki et al., 2014). It is worth noting that strains obtained in this study took 7 days to grow under low temperatures while Calvo and Zúñiga (2010) reported that strains belonging to the genus Bacillus took only 4 days to grow under the same conditions.

    Figure 1. Percentage of strains showing different growth levels (1–4) at different temperatures (6 ℃, 12 ℃, 22 ℃, 28 ℃).

    3.2. IAA production assays

    Strains were tested for their ability to produce IAA at three temperatures i.e. 22 ℃, 12 ℃ and 6 ℃ (Table 1). Among the tested strains, LMTK39 was able to produce the maximum amount of the phytohormone at 22 ℃ and 12 ℃, 60.6 μg/ml and 31.1 μg/ml, respectively. Whereas strain LMTK11 showed the highest ability to produce IAA at 6 ℃ (14.1 μg/ml). It was observed that the number of strains having the ability to produce IAA at 6 ℃ were higher than that of those at 22 and 12 ℃. The above finding was not unexpected due to the fact that the amount of IAA biosynthesis varies as per the nature of the strain and environmental factors like altitude, temperature, drought conditions etc. In addition, a number of other factors related to stress conditions affecting these microbes are also known to influence with IAA biosynthesis [2,20]. Subramanian et al. (2016) [21] reported that bacterial strains isolated from soils collected in regions with an average temperature of about 2 ℃, have the ability to produce IAA at 5 ℃. IAA production by these strains was found to be in the range of 0.3 to 17 μg/ml, values which are similar to those found in this study at 6 ℃. A similar test was also performed by Zúñiga et al. (2011) [22] with strains isolated from maca rhizosphere at 28 ℃ showing less IAA production ability (0.3–11.9 μg/ml) at 5 ℃ than those reported in this study.

    Table 1. PGPR traits of the strains used in this study. IAA (μg/ml) production and halo of phosphate solubilization (mm).
    STRAINS IAA (μg/ml) CaHPO4 (mm) Ca3(PO4)2 (mm)
    22 ℃ 12 ℃ 6 ℃ 22 ℃ 12 ℃ 6 ℃ 22 ℃ 12 ℃ 6 ℃
    LMTK1 3.6
    LMTK4 3.3
    LMTK5 4.0
    LMTK6 2.9 3.2 1.25 5.25 2
    LMTK7 7.0 3.0 3.2
    LMTK10 1.8 4.8 3.2
    LMTK11 5.4 15.1 14.1 11.5 23.5 18 2 2.5 2.75
    LMTK15 4.5
    LMTK25 1.8 0.9 6.9
    LMTK28 3.7 0.9 8 20.5 11.25 2.5
    LMTK32 2.0 1.1 8 19.25 11 2.5 2.5
    LMTK34 12.3 4.7 7 20.5 10 2 4.5
    LMTK36 9 17 12.5 2 1
    LMTK37 12.8 6.0 12.1
    LMTK39 60.6 31.1 12.5
    LMTK42 0.4 1.5 12.6 8 16.25 12.25 1.25 1
    LMTK43 3.0 9.8 9.5 3 6.25 3.25 1.25 1.5
     | Show Table
    DownLoad: CSV

    3.3. Phosphate solubilization ability

    Eight strains were able to solubilize di-calcium and tri-calcium phosphate. Strain LMTK11 was the only one which had the ability to solubilize tri-calcium phosphate at 22 ℃. This strain showed a solubilization halo of 2 mm, while in a di-calcium phosphate media it was capable to produce a halo size of 11.5 mm. Solubilization halo of the strains from this study varied from 5.25 mm to 23.5 mm at 12 ℃. Strains LMTK11, LMTK28 and LMTK34 showed the maximum ability to solubilize di-calcium phosphate at this temperature. The ability of the strains to solubilize di-calcium at 6 ℃ was lower than at 12 ℃ and higher than at 22 ℃. At this temperature (6 ℃), strains LMTK11, LMTK28 and LMTK34 displayed solubilization halos of 18, 11.3 and 10 mm respectively (Table 1). In a similar study, strains isolated from the Himalayas and living at harsh conditions of low temperature and high altitude, showed a range of solubilization efficiency between 25.8–375.4 and 31.7–456.5 at incubation temperatures of 4 and 10 ℃, respectively [23]. From all the strains tested, Pseudomonas sp. showed high ability to solubilize di-calcium and tri-calcium phosphates. Mishra et al. (2015) [24] also reported Pseudomonas sp. as the bacterial genus with the highest solubilization activity. In contrast, Zúñiga et al. (2011) [22] found that free-living diazotrophs showed the best solubilization halos in di-calcium and tri-calcium media at temperatures of 5, 14 and 28 ℃.


    3.4. Promotion of seed germination

    Sixteen from the seventeen strains tested in the red clover germination assay at 22 ℃ significantly increased the percentage of germination compared to the non-inoculated control (Figure 2A). LMTK11 strain showed the best performance in the germination assay at this temperature. These results are consistent with those reported by Kloepper et al. (1991) [25], which emphasize the role of PGPR in improving seed germination rates through the production of plant growth regulating substances such as auxins, cytokinins or gibberellins [26]. The majority of the strains able to increase the germination percentage were also positive for both IAA production and phosphate solubilization. Although, some of the strains did not show high values in all PGPR traits, they were able to improve seed germination in comparison to the non-inoculated control. At 12 ℃, strains LMTK25 and LMTK28 showed better ability to increase the germination rate (42 and 41%, respectively) than the control (26%) (Figure 2b). A study conducted by Acosta et al. (2012) [27] also higlighted the importance of incubation temperature for the induction of seed germination.

    Figure 2. Effect of inoculation with different bacterial strains on red clover seed germination. A. 22 ℃; B. 12 ℃.

    3.5. Bacterial growth at different heavy metal concentrations

    Eleven out of the seventeen strains tested were able to grow in the presence of different heavy metals (0.5 mM Pb, Cd and Co; 0.01 mM Hg). It was shown that the strains were able to better tolerate the heavy metals when they were cultivated at pH 5 rather than 4 (Table 2). Other studies show a variable effect of heavy metals such as lead and cadmium in different organisms, demonstrating that the toxicity depends not only on pH but also on the concentration and organism evaluated. [28,29,30]. Strain LMTK11 was the only one able to grow at both pH 4 and 5 in a culture media supplemented with Hg; while in media supplemented with Co at pH 5, the growth of strains LMTK11, LMTK32 and LMTK36 was the only observed. Interestingly, strain LMTK11 was able to grow in NA plates supplemented with a mixture of heavy metals (Pb, Cd, Co and Hg). Mechanisms reported for heavy metal resistance in bacteria are: (1) exclusion of metal by a permeable barrier, (2) exclusion by active transport of the metal from the inside of the cell outwards, (3) intracellular physical sequestration of the metal using a polymer to prevent metal cellular damage, (4) extracellular sequestration, (5) enzymatic detoxification of the metal to a less toxic form, and (6) cell reduction of the sensitivity to metals [31].

    Table 2. Growth ability of eleven strains in the presence of different heavy metals at pH 4 and 5.
    STRAINS pH 4 pH 5
    Cd Pb Co Hg MIX Cd Pb Co Hg MIX
    LMTK5 x x x
    LMTK11 x x x x x x x x
    LMTK28 x x x
    LMTK32 x x x x
    LMTK33 x x x
    LMTK34 x x x
    LMTK36 x x x x
    LMTK37 x
    LMTK39 x
    LMTK42 x x x
    LMTK43 x x x x
    x, Growth ability; MIX, mixture of different heavy metals.
     | Show Table
    DownLoad: CSV

    3.6. Minimum inhibitory concentration assay

    Minimum inhibitory concentration (MIC) assays was performed using Pb and Cd. Based on the results obtained, MIC values of the 11 selected strains were calculated to be 0.5 mM and 0.05 mM for Pb and Cd, respectively (Table 3). Kumar et al. (2015) [32] reported two Bacillus strains with MIC values of 250 and 1000 ppm for Pb. On this kind of assay, reduction in colony size is common. This reduction is attributed to the toxic effects that both metals exert on bacterial cell affecting its metabolism, causing a blockage of enzymes and polynucleotides activities [33,34]. These heavy metals are also known to interfere with the transport of essential nutrients and ions. They also affect organisms by either substitution or displacement of essential ions in the cell or through denaturation and inactivation of key enzymes. In addition, heavy metals are able to affect bacterial membrane integrity [31]. Although high concentrations of heavy metals inhibit bacterial growth, there are some species which are resistant and could grow up to 5000 ppm of Pb [35]. In course of the assays, it was noticed that some bacterial colony sizes increased as the concentration of the metals were increased. Strain LMTK43 showed an increase in colony size in comparison to the control devoid of heavy metals. Some studies have described the ability of certain strains to use these metals as growth enhancers. For instance, in a study conducted by Azario et al. 2010 [36], significant increase in growth of E. coli ATCC 35218 was observed when it was cultivated in a media supplemented with Cr, Cd and Pb separately or together, as a cocktail.

    Table 3. Strain tolerance percentages to different concentrations (mM) of lead and cadmium.
    Heavy metals lead and cadmium concentrations (mM)
    0.005 0.01 0.05 0.1 0.5 1 2.5 5
    Pb 100 100 100 100 72.7 0 0 0
    Cd 100 100 72.7 63.6 63.6 54.5 0 0
     | Show Table
    DownLoad: CSV

    3.7. Phylogenetic analysis of the strains

    The NJ phylogenetic tree (Figure 4) showed that the studied strains were clustered in 8 groups distributed in the Pseudomonas, Bacillus, Paenibacillus, Sporosarcina, Cupriavidus and Paenarthrobacter genera. The majority of strains belonged to Bacillus and Pseudomonas. Bacillus and Pseudomonas genera are usually reported as PGPR and are found to be dominant in bacterial-plant studies [37]. Among the Firmicutes, five strains were clustered within the Bacillus simplex group and two strains were grouped with Paenibacillus sinodophylli. One strain of Actinobacteria grouped with Paenathrobacter nitroguajacolicus. Proteobacteria were represented by one strain related to Cupriavidus gilardii, one strain to Pseudomonas taiwanensis while five strains were grouped with Pseudomonas constaninii. The comparison of the 16S rDNA gene sequence of all the isolates against type strains of bacterial species recorded in the EzCloud database is shown in Table 4.

    Table 4. Comparison of 16S rDNA sequences obtained from strains isolated in this study and related type strains.
    Strains Molecular identification using 16S rDNA gen Accession number Similarity (%)
    LMTK1 Bacillus simplex NBRC 15720T BCVO01000086 99.8
    LMTK4 Bacillus simplex NBRC 15720T BCVO01000086 99.8
    LMTK5 Bacillus simplex NBRC 15720T BCVO01000086 99.8
    LMTK6 Paenarthrobacter nitroguajacolicus G2-1T AJ512504 99.8
    LMTK7 Bacillus butanolivorans DSM 18926T LGYA01000001 99.8
    LMTK10 Bacillus butanolivorans DSM 18926T LGYA01000001 99.8
    LMTK11 Pseudomonas fluorescens DSM 50090T LHVP01000014 99.5
    LMTK15 Bacillus simplex NBRC 15720T BCVO01000086 99.8
    LMTK25 Bacillus simplex NBRC 15720T BCVO01000086 99.8
    LMTK28 Pseudomonas trivialis DSM 14937T JYLK01000002 99.2
    LMTK32 Pseudomonas simiae OLiT AJ936933 99
    LMTK34 Pseudomonas simiae OLiT AJ936933 99
    LMTK36 Pseudomonas simiae OLiT AJ936933 99.5
    LMTK37 Paenibacillus sinopodophylli TEGR-3T KX009022 98.2
    LMTK39 Paenibacillus sinopodophylli TEGR-3T KX009022 96
    LMTK42 Cupriavidus gilardii LMG 5886T AF076645 99.5
    LMTK43 Pseudomonas baetica a390T FM201274 99.5
     | Show Table
    DownLoad: CSV
    Figure 3. Phylogenetic tree based on 16S rDNA sequences. Strains obtained in this study are indicated in bold. Only bootstrap values greater than 60% are shown (1, 000 pseudoreplicates). Type strains of related species were obtained from Ez-biocloud.

    4. Conclusions

    The results obtained in this study demonstrate the PGPR potential of these strains; as well as their ability to grow in the presence of heavy metals such as lead and cadmium under in vitro conditions. This study provides first experimental evidence highlighting the potential of these strains as biofertilizers and bioremediators for the high Andean soils, due to their ability promote plant growth, ability to grow at low temperatures and to tolerate heavy metal toxicity.


    Acknowledgment

    This research was funded by PROCYT 309-2009-CONCYTEC, Peru Biodiverso-2009-GTZ-CONCYTEC and ECOANDINO S.A.C. We thank Dr. Ernesto Ormeño Orrillo for his suggestions and critical editing of the manuscript.


    Conflict of Interest

    The authors declare no conflict of interest in this research.


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