Biodegradation and Metabolic Pathway of Sulfamethoxazole by Sphingobacterium Mizutaii

doi:10.21203/rs.3.rs-778059/v1

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Biodegradation and Metabolic Pathway of Sulfamethoxazole by Sphingobacterium Mizutaii

https://doi.org/10.21203/rs.3.rs-778059/v1

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published 30 Nov, 2021

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Sulfamethoxazole (SMX) is the most commonly used antibiotics in China for inhibiting aquatic animal diseases. However, the residues of SMX are difficult to eliminate and may enter the food chain, leading to considerable threats on human health. The bacterial strain Sphingobacterium mizutaii LLE5 was isolated from activated sludge. This strain could utilize SMX as its sole carbon source and degrade it efficiently. Under optimal degradation conditions (30.8 °C, pH 7.2, and inoculum amount of 3.5 × 10⁷ cfu/mL), S. mizutaii LLE5 could degrade 93.87% of 50 mg/L SMX within 7 days. Four intermediate products from the degradation of SMX were identified: sulfanilamide, 4-aminothiophenol, 5-amino-3-methylisoxazole, and aniline, suggesting a possible degradation pathway based on these findings. This report is the first to confirm that Sphingobacteriumi could degrade SMX. Furthermore, S. mizutaii LLE5 could also degrade other sulfonamides. The degradation efficiencies of strain LLE5 for sulfadiazine, sulfaguanidine, sulfamisoxazole, and sulfadimidine were 59.85%, 51.68%, 46.95%, and 37.42%, respectively.

Agricultural Engineering

Food Science & Technology

Biodegradation

metabolic pathway

sulfamethoxazole

Sphingobacterium mizutaii

antibiotics

China

animal diseases

The amount of aquaculture in China ranks first in the world all year round. The huge output mainly depends on high-density aquaculture¹. This type of aquaculture leads to the risk of outbreaks of aquatic animal diseases. Sulfamethoxazole (SMX), which is the most commonly used antibiotics in China, can kill aquatic pathogens and can effectively inhibit aquatic animal diseases². However, SMX cannot be completely utilized and metabolized by aquatic animals because approximately 50% are excreted to the environment without modification. Consequently, SMX has become a widely distributed pollutant in aquatic and domestic waste waters³. Numerous studies have indicated that SMX has adverse ecological effects and may threaten human healthafter long-term exposure. The World Health Organization has classified SMX as a Category 3 carcinogen in 2017⁴. However, SMX has been proven to be difficult to eliminate by conventional water treatment processes⁵. The residues of SMX enter the food chain, leading to considerable threats to human health. Therefore, an efficient and reliable degradation method for removing SMX residue from the water environment must be developed ⁶.

SMX removal is mainly by physical, chemical, and microbial methods⁷. The physical and chemical methods mainly include anion exchange, nano-filtration, struvite precipitation, and electrodialysis⁸. However, for technical and economic reasons, physical and chemical techniques may not be feasible⁹. Microbial biodegradation has advantages in terms of its eco-friendliness, low cost, and scope of implementation and has been proven as an effective method for the remediation of SMX residues in aquaculture waters¹⁰. To date, more than 20 strains of SMX-degrading strains have been isolated from different environments, and all of them exhibit SXM-degrading ability under laboratory conditions. Liang et al. isolated Achromobacter sp. JL9, which can use SMX as the sole nitrogen source for growth. The degradation rate of SMX was 90.4%, and the highest reaction rate constant was 0.0384 min^{-1 11}. Gao et al. found that Phanerochaete chrysosporium has a strong tolerance to sulfamethoxazole in the concentration range of 10–30 mg/L¹². At 10 mg/L, the degradation rate reached 53% after 24 h and 74% after 10 days. Jia et al. reported that the sulfate-reducing bacteria (SRB) sludge system shows considerable ability to degrade SMX. When the initial concentration is 25, 50, 100, 150, and 200 mg/ L, the removal rates of SMX by SRB sludge through adsorption and biodegradation are 3.9, 5.6, 13.2, 15.9, and 21.3 mg/L/d¹³. Other bacteria, including Achromobacter denitrificans PR1¹⁴, P. chrysosporium¹⁵, Pseudomonas stutzeri¹⁶, and Acinetobacter sp.¹⁷, could serve as resources for the bioremediation of SMX from the polluted environment. Nevertheless, further studies are needed. Previous studies mainly isolated SMX-degrading bacteria through traditional methods, and the degradation efficiency was relatively low. The degradation mechanism of SMX and the metabolic pathway involved are also unclear.

The aims of this study were: (1) to isolate a bacterial strain that can highly degrade SMX by a novel method; (2) to optimize the environmental parameters to improve degradation efficiency; and (3) to deduce the possible degradation pathway of degrading strain and examine the mechanism underlying SMX degradation.

Chemicals and media. SMX (analytical standard, >99.5%), HPLC-grade methanol, and acetonitrile were purchased from Sinopharm Chemical Reagent Beijing Co., Ltd. All other reagents used in the present study were of analytical grade. Mineral salt medium (MSM) and Luria–Bertani (LB) medium were used as described by Song et al²³. Agar plates were prepared by adding 1.5% (w/v) agar into the liquid media.

Enrichment culture and high-throughput sequencing. Activated sludge samples were collected from the wastewater treatment pond of a pharmaceutical factory in Liaoyang City, Liaoning Province, China. 10.0 g of sample was suspended in 100 mL of MSM supplemented with 100 mg/L SMX. Then, the sample was incubated on a rotary incubator shaker at 30 °C and 100 r/min in the dark. After 7 days, 10 mL of the sample was transferred into fresh MSM supplemented with 200 mg/L of SMX and incubated for another 7 days. After repeating this process four times, the SMX concentration in the fourth generation increased to 500 mg/L. The activated sludge sample was designated as SMXY, and the four generations of SMX enrichment cultures were designated as SMX1, SMX2, SMX3, and SMX4. The total DNA of SMXY and SMX1-4 were extracted using a FastDNA SPIN kit for soil (MP, Biomedicals, USA). After purification, the 16S rRNA distinct regions V3–V4 were amplified with the following primers: 338F (5′-ACTCCTACGGGAGGCAGCA-3′) and 806R (5′-GGACTACHVGGGTWTCTAAT-3′). The polymerase chain reaction (PCR) system was designed as described by Li et al²⁴. The PCR product was sent to Biomark Gene Technology Company for library construction and high-throughput sequencing. The obtained sequence data were analyzed using Arch software (http://www.drive5.com/usearch/). The identity of sequences ≥97% was assigned to an operational taxonomic unit (OTU), and each OTU was considered to represent a species. The relative abundance of OTUs in the samples was statistically analyzed using R software (https://www.R-project.org)²⁵.

Isolation and identification of SMX-degrading bacteria

According to the results of high-throughput sequencing, the fourth-generation enrichment sample SMX4 containing the most Sphingobacterium cells was used for isolation of SMX-degrading bacteria. Then, 100 μL of SMX4 was spread on the MSM solid plate containing 100 mg/L SMX and incubated at 30 °C. The rapidly growing colonies on the plate with different morphologies were selected and restreaked three times to obtain pure cultures. The degradation efficiency of the isolates was determined by a high-performance liquid chromatography (HPLC) system (1260, Agilent, Santa Clara, CA) equipped with an eclipse Plus C₁₈ column. The elution comprised a mixture of methanol, formic acid (85/15/0.1, v/v/v), and distilled water, running at the flow rate of 1.0 mL/min. The injection volume was 10 μL, and the column temperature was 30 °C²⁶. The isolate with the highest degradation efficiency was selected for further analysis. The genomic DNA of the isolate was extracted and was used as a template for 16S rDNA amplification as described by Ruan et al²⁷. The universal primers were 27F (5′-AGAGTTTGATCCTGGCTCAG-3′) and 1492R (5′ACGGHTACCTTGTTTACGACTT-3′). The purified PCR product was sequenced by Bomad Technology (Beijing, China). The obtained sequence was deposited in GenBank. The strain was further identified by performing multiple sequence alignment using Clustal X sofware, and phylogenetic relationships were analyzed via the neighbor-joining (NJ) method with MEGA 6 software²⁸.

Inoculum preparation

Before the degradation experiment, strain activation was performed. S. mizutaii LLE-5 was inoculated into 100 mL of LB medium and incubated at 30 °C on a rotary shaker at 150 rpm. After 12 h, the bacterial cells were harvested by centrifugation at 4000 g for 10 min. The precipitate was washed two times by phosphate buffered saline (PBS) solution and suspended for subsequent studies²⁹.

Optimization of the SMX-degrading conditions

The effect of single environmental factors on the biodegradation efficiency was evaluated by analyzing the following parameters and their ranges³⁰: temperature (15 ℃, 20 ℃, 25 ℃, 30 ℃, 35 ℃,and 40 ℃); initial medium pH (4, 5, 6, 7, 8, and 9); inoculum amount (1.0 × 10⁷, 2.0 × 10⁷, 3.0 × 10⁷, 5.0 × 10⁷, 8.0 × 10⁷, and 10.0 × 10⁷ cfu/mL); and initial concentration (10, 50, 100, 200, 300 and 500 mg/L). The sterile distilled water was supplemented every 12 h according to the loss of weight. Selected single environmental factors and their interactions were further optimized via response surface methodology (RSM) analysis based on Box−Behnken design³¹. The second order polynomial equation is expressed as follows:

Y_i= b_o+ ∑b_iX_i+ ∑b_ijX_iX_j+ ∑b_iiX_i² (2)

where Y_i refers to the predicted response, X_i and X_j are variables, b_o is a constant, b_i denotes the linear coefficient, b_ii represents the quadratic coefficient, and b_ijcorresponds to the interaction coefficient.

Biodegradation tests

The SMX degradation test was performed under optimal conditions. S. mizutaii LLE-5 cells were inoculated into 100 mL of MSM supplemented with 50 mg/L of SMX. The residual of SMX and cell numbers of S. mizutaii LLE-5 were detected every day. The control was inoculated with killed cells of S. mizutaii LLE-5. Each test was conducted in triplicate³². The ability of S. mizutaii LLE-5 to degrade other structurally similar sulfonamides, including sulfadiazine, sulfaguanidine, sulfamisoxazole, and sulfadimidine, were evaluated. Analytical methods were the same as above described.

Identification of SMX biodegradation intermediates

Intermediates generated during SMX degradation by S. mizutaii LLE-5 in MSM were analyzed by HPLC-MS (AB Sciex QTRAP 5500, USA). Then, 10 mL of the culture and equal volume of methanol were added into a 50 mL centrifuge tube and mixed using a vortex mixer for 1 min. Then, the centrifuge tube was placed in a shaker, mixed at 220 r/min for 30 min, and centrifuged at 5000 g for 8 min. The upper phase was filtered with a 0.22 μm membrane for HPLC-MS analysis. The flow rate was 0.2 mL/min, the mobile phase A was 0.1% formic acid (V/V), and B was methanol. The targeted screening gradient elution program was: 0–2 min, 95% A; 2–25 min, 95%–5% A; 25–35 min, 5% A; and 35–40 min, 95% A. The sample injection volume was 20 μL, and the column temperature was 30 °C. The mass spectrometry conditions were: DuoSprayTM ion source, electrospray ionization (ESI), positive ion mode scanning, the ion source temperature was 550 ℃, the spray voltage was 5500 V, and curtain air (CUR) was 35 psi. The accumulation time was 0.25 s, and the collision voltage was (35±15) eV.

Community changes and diversity of SMX-degrading enrichment cultures

A total of 5978, 6012, 6048, 6005, and 6003 16S rRNA gene sequences of the distinct V3–V4 regions were obtained from sludge sample (SMXY) and four generations of enrichment cultures (SMX1–4) by high-throughput sequencing, respectively. After statistical analysis and annotation, the results (Fig. 1) showed that 5978 sequences in sludge sample SMXY were clustered into 166 OTUs. The highest abundance of OTUs belonged to bsv13, Lentimicrobium, Flaviolibacter, Ramlibacter, and Rhodoferax. After enrichment, the bacterial diversity of SMX1 rapidly decreased, 6012 sequences were clustered into only 23 OTUs. The main genera were Pseudomonas, Sphingobacterium, Escherichia-Shigella, Alcaligenes, and Sediminibacter. Pseudomonas became the highest abundance genus in SMX2. After the second passage, with the increase in the SMX concentration, the bacterial diversity of SMX2 decreased continuously, and 6048 sequences were clustered into 20 OTUs. The main genera were Sphingobacterium, Escherichia-Shigella, Alcaligenes, and Sediminibacter, Sphingobacterium replaced Pseudomonas as the genus with the highest abundance, and the proportion of Sphingobacterium reached 85.84%. The result indicates that Sphingobacterium can tolerate high concentrations of SMX that the other bacteria could not tolerate and thus, they died out. As a result, the diversity in the enrichment gradually declined with the increase in SMX concentrations and passage generations. After the third and fourth passages, the 6003 sequences of SMX4 were clustered into 16 OTUs, and the main genera were Sphingobacterium, Alcaligenes, and Sediminibacter. The proportion of Sphingobacterium reached 93.68% and became the dominant genera. This result provides strong evidence that Sphingobacterium contributed to SMX degradation. By contrast, the rapid reduction in the proportion of Pseudomonas and other bacteria indicates that they did not contribute to SMX degradation.

Isolation and identification of SMX-degrading strains. Five strains that showed SMX degradation ability were isolated from SMX4 and were named LLE1–5. Among them, LLE5 utilized SMX as the sole carbon source in MSM and degraded 91.3% of 50 mg/L SMX in 7 days. It was selected for further morphological physiological, and biochemical analyses. LLE5 colonies on LB plate had smooth surfaces and clear edges and were lemon yellow in color. Under the microscope, cells of LLE5 featured short rods that were 0.6–1.8 μm in length, 0.4–0.7 μm in width, and were gram negative and nonmotile. LLE5 could utilize dextran, D-maltose, D-trehalose, D-fiber, gentian disaccharide, disaccharide, sucrose, D-pinobiose, and stachyose but not D-sorbitol, D-mannitol, and D-arabinol. The 16S rRNA gene sequence of LLE5 was sequenced and submitted to GenBank with the accession number MW261785. Blast results showed that LLE5 belonged to the genus Sphingobacterium and clustered strongly with S. mizutaii NCTC 12149^T (99.09%, accession number LT906468) (Fig. 2). According to the results of morphological, physiobiochemical, and 16S rRNA evaluations, LLE5 was identified as a member of genus Sphingobacterium and named Sphingobacterium mizutaii. This is the first report that a Sphingobacterium species can degrade SMX. S. mizutaii LLE5 has been deposited in Guangdong Microbial Culture Collection of Center under number CGMCC 61038.

Optimization of the degradation conditions for LLE5

The influence of various environmental factors on the biodegradation efficiency was determined. S. mizutaii LLE5 can degrade SMX from 15 °C–40 °C (Fig. 3a), with an optimum temperature of 30 °C. Although the temperature decreased to 15 °C, the degradation efficiency was more than 42.32%. When the temperature rose to 40 ℃, the degradation efficiency was more than 58.65%, and these results showed that S. mizutaii LLE5 has an obvious temperature adaptability. pH is another key factor affecting the degradation efficiency of the strain. The results of different pH on the degradation of the strain (Fig. 3b) show that LLE5 can degrade SMX in the pH range 4.0–9.0. At the optimal pH of 7.0, the degradation of SMX was 91.77%. In addition, the degradation efficiency of LLE5 was more than 50% in the pH range 5.0–8.0, which indicated that the degradation efficiency of strain LLE5 was higher under neutral conditions. When the pH was reduced to 4.0, the degradation efficiency was still 48.64%, indicating that the strain was tolerant to acid conditions. When the pH was 9.0, the degradation efficiency was 38.70%, which indicated that LLE5 could be applied under neutral and acid conditions.The different initial inoculum amount on the degradation efficiency was analyzed (Fig. 3c). When the inoculation amount was 5×10⁷ cfu/mL, the degradation efficiency of S. mizutaii LLE5 was the highest, which was 92.89%. However, when the initial inoculation amount was 2.0×10⁷ –8.0×10⁷ cfu/mL, the degradation efficiency was more than 90%, indicating that the degradation efficiency of S. mizutaii LLE5 did not change significantly with the change in inoculation size. The initial concentration of SMX also influenced the degradation efficiency of S. mizutaii LLE5 (Fig. 3d). The degradation efficiency of S. mizutaii LLE5 with 10 mg/L SMX reached 95.14% and decreased to 83.42% when the SMX concentration reached 300 mg/L. These results indicate that high concentrations of SMX inhibit the growth of S. mizutaii LLE5.

The temperature, pH levels and inoculation size were further designed through the response surface method in accordance with the results of single-factor experiments, and 17 degradation tests were carried out (Table 1). By the statistical analysis of data, the following second-degree polynomial equation was obtained to explain SMX biodegradation by S. mizutaii LLE5:

Y₁ = 92.74 – 3.09A – 2.06B + 0.32C + 3.10AB – 1.07AC – 1.08BC – 9.40A² – 8.40B² – 0.12C² (1)

where Y₁ represents the SMX degradation efficiency, and A, B, and C are the coded values for temperature, pH level, and inoculation size respectively. Analysis of variance (ANOVA) for the fitted quadratic polynomial model is shown in Table 2.

The model was signifcant (P<0.05) with R²=0.9831 and Adj R²=0.9613. The results of regression analysis indicated that temperature and pH level were significant terms (P<0.05), whereas the inoculation amount was a nonsignificant term (P>0.05). The three-dimensional response surface was plotted to directly display the effects of the temperature and pH level on SMX biodegradation. At the theoretical maximum point of response surface(Fig. 4), the optimum conditions for SMX degradation by S. mizutaii LLE5 were 30.8 °C, pH 7.2, and inoculum amount of 3.5 × 10⁷ cfu/mL.

Degradation of SMX by strain LLE5. The degradation characteristics of SMX by S. mizutaii LLE5 under the optimal conditions were studied. The results indicated that the most efficient degradation was obtained during the first 3 days. On the third day, the degradation efficiency was 84.02%, and the cell concentration was 68.95% × 10⁷ cfu/mL(Fig. 5). The degradation efficiency was positively correlated with the cell growth density. At 5–7 days, the degradation efficiency of SMX gradually decreased and was accompanied by no further increase in S. mizutaii LLE5 cell density. Finally, the degradation efficiency of SMX with initial concentration of 50 mg/L was 93.87% after 7 days. This is the first report that Sphingobacterium mizutaii has a good degradation effect on SMX. S. mizutaii LLE5 can also degrade other sulfonamides, and the degradation efficiencies of strain LLE5 for sulfadiazine, sulfaguanidine, sulfamisoxazole, and sulfadimidine were 59.85%, 51.68%, 46.95%, and 37.42%, respectively (Fig. 6). These results show that although the degradation efficiency was relatively low, S. mizutaii LLE5 has a broad specificity for the degradation of sulfonamides and has considerable potential for processing sulfonamide pollution in the environment.

Metabolic pathways of SMX degradation by S. mizutaii LLE5. The metabolites of SMX degraded by S. mizutaii LLE5 in MSM liquid medium were detected by HPLC/MS. According to the chemical structure of SMX and the mass spectrum, four candidate products were identified. These products were sulfanilamide (171 m/z), 4-aminothiophenol (124 m/z), 5-amino-3-methylisoxazole (99 m/z), and aniline (92 m/z). None of these products were detected when the culture medium only contained SMX and without S. mizutaii LLE5, indicating that they are SMX biodegradation metabolites. A possible metabolic pathway for SMX biodegradation by LLE5 was proposed (Fig. 7). SMX is first transformed into sulfanilamide and 5-amino-3-methylisoxazole through hydrogenation. Then, sulfanilamide is degraded via desulfurization into aniline and via deamination into 4-aminothiophenol. Although the ring-opening products of hydroquinone were not detected, it is still the first report of the pathway of SMX degradation by a Sphingobacterium strain.

Sphingobacterium strains widely exist in natural environment¹⁸. Sphingobacterium is a kind of gram-negative bacteria and does not produce spores. Since the genus Sphingobacterium was proposed originally by Yabuuchi et alin 1983¹⁹, new species have been discovered from a variety of environments, such as soil, plants, animals, and even clinical samples of ventricular fluid and urine. Among them, Sphingobacterum thalpohilum and Sphingobacterum multivarum can degrade petroleum hydrocarbons. For example, S. multivorum SWH-2 has a strong ability to degrade petroleum²⁰. After ensuring optimal conditions, the normal growth and enzyme secretion and activity of S. multivorum SWH-2 will also change, which can further improve the oil degradation of the strain. In addition, most Sphingobacterium found thus far are resistant to a variety of antibiotics from microorganisms. However, there is no report on the direct degradation of antibiotics by Sphingobacterium. Sphingobacterium mizutaii isolated in this study is the first Sphingobacterium reported to degrade SMX. The discovery of this bacterium not only expanded the functional range of Sphingobacterium but also provided valuable microbial resources for the remediation of SMX contaminated aquaculture environment.

In recent years, a number of strains with good SMX degradation ability, such as Planococcus kocurii O516, Achromobacter sp. JL9, Phanerochaete chrysosporium, and Acinetobacter sp., have been isolated from soil, activated sludge, and aquaculture water. Compared with the reported strain, the strain LLE-5 had a better environmental range and tolerance. The study on the influence of environmental factors on the degradation effect indicates that strain LLE-5 can degrade SMX at the temperature range 15 ℃–40 ℃ and at pH 4–9. This finding provides a basis for the practical application of the strain in the future. The physiological and biochemical results showed that LLE-5 could use a variety of carbon sources. The bacteria have strong adaptability to the environment, rich types of nutrition metabolism, and potential to degrade other complex compounds.

The existing reports show that most strains of Sphingobacterium cannot produce antibiotics but are resistant to antibiotics, which is an important factor for the Sphingobacterium to adapt to extreme environments²¹. Antibiotics are compounds that inhibit the growth of microorganisms. Thus, degrading bacteria need to have antibiotic resistance. Some studies have shown that Klebsiella pneumoniae can use chloramphenicol as the sole carbon source for growth²². However, the drug sensitivity test showed that these strains were sensitive to chloramphenicol, which indicated that the drug resistance and drug degradation processes were two independent pathways. According to the degradation products of SMX by S. mizutaii LLE-5, the strain mainly transformed SMX into sulfanilamide and 5-amino-3-methylisoxazole through hydrogenation. Then, sulfanilamide is degraded via desulfurization into aniline and via deamination into 4-aminothiophenol. The results showed that the strain had a clear degradation function of sulfamethoxazole and had a good tolerance. However, SMX could not be completely mineralized in terms of degradation products. This work is the first to report the pathway of SMX degradation by a Sphingobacterium strain and provided a certain reference for the study of microbial degradation of SMX.

Acknowledgment

This work was supported by Open Research Fund of Key Laboratory of Healthy Freshwater Aquaculture, Ministry of Agriculture and Rural Affairs（ZJK202101） , Central Public-interest Scientific Institution Basal Research Fund, (CAFS, No. 2021A003).

Author Contributions

Y.M. and Z.R. conceived and designed research. J.S., G.H., L.L., H.Z., and D.Z. conducted experiments. J.X., X.L. and Z. Y. analyzed and discussed the data. J.S. wrote the manuscript. All authors read and approved the manuscript.

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Biodegradation and Metabolic Pathway of Sulfamethoxazole by Sphingobacterium Mizutaii

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References

Tables

Additional Declarations

Supplementary Files

Status:

Journal Publication

Version 1