氯霉素及其产物降解菌群在长期驯化过程中的微生物群落和关键基因演替模式

张家禹, 周开颜, 郭芳亮, 雷华新, 赵仁鑫, 林琳, 李晓岩, 李炳

工程（英文） ›› 2023, Vol. 31 ›› Issue (12) : 59-69.

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工程（英文） ›› 2023, Vol. 31 ›› Issue (12) : 59-69. DOI: 10.1016/j.eng.2023.07.009
研究论文

氯霉素及其产物降解菌群在长期驯化过程中的微生物群落和关键基因演替模式

作者信息 +

The Successional Pattern of Microbial Communities and Critical Genes of Consortia Subsisting on Chloramphenicol and Its Metabolites Through Long-Term Domestication

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Highlight

• Three domesticated consortia could degrade CAP, PNB, and DCA with high efficiencies.

• A successional pattern of the microbial community across domestication was revealed.

• Collaboration of Sph., Cab., and Cup. contributed to a high CAP mineralization rate.

• Dynamic changes in key genes involved in CAP, PNB and DCA metabolism were deciphered.

• Carbon source and pH had significant impacts on the biodegradation efficiency of CAP.

摘要

氯霉素（CAP）作为一种广泛存在的新污染物，对水环境中的生态群落产生了负面影响。生物处理广泛应用于水体污染物的去除，而功能微生物的性能决定了其效果。本研究从活性污泥中驯化了一个具有强大CAP降解能力的菌群。对硝基苯甲酸（PNB）和2,2-二氯乙酸（DCA）是CAP生物和化学处理过程中产生的主要产物，它们也分别作为菌群的唯一底物进行长期驯化。宏基因组分析揭示了2.5年驯化过程中微生物群落和关键功能基因的演替模式。经过长期驯化，Sphingomonas、Caballeronia和Cupriavidus分别成为CAP、PNB和DCA降解菌群中的优势菌属，并且它们分别是CAP、PNB和DCA的关键降解菌，它们之间的协同合作实现了CAP的高度矿化。PNB转化为原儿茶酸（PCA），然后通过间位和邻位裂解途径被矿化。通过长期驯化，参与CAP、PNB和DCA代谢的关键功能基因，包括CAP乙酰转移酶、CAP氧化还原酶、卤代酸脱卤酶和原儿茶酸双加氧酶，在菌群中显著富集。本研究还发现pH和碳源对CAP的生物降解效率有显著影响。本研究驯化的菌群和分离的菌株可用作加强CAP、PNB和DCA污染环境生物修复的微生物资源。

Abstract

As a widespread emerging contaminant, chloramphenicol (CAP) adversely impacts ecological communities in the water environment. Biological treatment is widely used for aquatic pollutant removal, and the performance of functional microbes determines its outcome. Herein, a consortium with a powerful CAP-degrading capacity was domesticated from activated sludge. As the common degradation products of CAP, 4-nitrobenzoic acid (PNB) and 2,2-dichloroacetic acid (DCA) were also used as the sole substrates for long-term domestication. The successional pattern of the microbial community and critical functional genes through the 2.5-year domestication was revealed by metagenomic analysis. Sphingomonas, Caballeronia, and Cupriavidus became the most dominant populations in the CAP-, PNB-, and DCA-degrading consortia, respectively, and they were crucial degraders of PNB and DCA. Their collaboration contributed to the high mineralization rate of CAP. PNB was transformed into protocatechuic acid (PCA) and then mineralized through meta-cleavage and ortho-cleavage pathways. Crucial functional genes involved in CAP, PNB, and DCA metabolism, including CAP acetyltransferase, CAP oxidoreductase, haloacid dehalogenases, and protocatechuate dioxygenases, were significantly enriched in consortia. pH and carbon source had significant impacts on CAP biodegradation efficiency. The domesticated consortia and isolated strains are necessary microbial resources to enhance the bioremediation of CAP-, PNB-, or DCA-polluted environments.

关键词

抗生素 / 生物降解 / 代谢作用 / 微生物群落演替 / 宏基因组

Keywords

Antibiotic / Biodegradation / Metabolism / Microbial community succession / Metagenome

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张家禹, 周开颜, 郭芳亮. 氯霉素及其产物降解菌群在长期驯化过程中的微生物群落和关键基因演替模式. Engineering. 2023, 31(12): 59-69 https://doi.org/10.1016/j.eng.2023.07.009

参考文献

原文顺序 | 文献年度倒序 | 文中引用次数倒序
[1]
M. Zhong, T. Wang, W. Zhao, J. Huang, B. Wang, L. Blaney, et al.. Emerging organic contaminants in Chinese surface water: identification of priority pollutants. Engineering, 11 ( 2022), pp. 111-125
[2]
W. Chu, S.W. Krasner, N. Gao, M.R. Templeton, D. Yin. Contribution of the antibiotic chloramphenicol and its analogues as precursors of dichloroacetamide and other disinfection byproducts in drinking water. Environ Sci Technol, 50 (1) ( 2016), pp. 388-396 DOI: 10.1021/acs.est.5b04856
[3]
X. Li, F. He, Z. Wang, B. Xing. Roadmap of environmental health research on emerging contaminants: inspiration from the studies on engineered nanomaterials. Eco-Environ Health, 1 (3) ( 2022), pp. 181-197
[4]
J. Zhang, J. Xu, H. Lei, H. Liang, X. Li, B. Li. The development of variation-based rifampicin resistance in Staphylococcus aureus deciphered through genomic and transcriptomic study. J Hazard Mater, 442 ( 2023), Article 130112
[5]
Y. Zhou, R. Farzana, S. Sihalath, S. Rattanavong, M. Vongsouvath, M. Mayxay, et al.. A one-health sampling strategy to explore the dissemination and relationship between colistin resistance in human, animal, and environmental sectors in Laos. Engineering, 15 ( 2022), pp. 45-56 DOI: 10.3934/jimo.2020142
[6]
Z. Han, H. Feng, X. Luan, Y. Shen, L. Ren, L. Deng, et al.. Three-year consecutive field application of erythromycin fermentation residue following hydrothermal treatment: cumulative effect on soil antibiotic resistance genes. Engineering, 15 ( 2022), pp. 78-88
[7]
N.H. Tran, H. Chen, M. Reinhard, F. Mao, K.Y. Gin. Occurrence and removal of multiple classes of antibiotics and antimicrobial agents in biological wastewater treatment processes. Water Res, 104 ( 2016), pp. 461-472
[8]
P.Y. Nguyen, G. Carvalho, M.A.M. Reis, A. Oehmen. A review of the biotransformations of priority pharmaceuticals in biological wastewater treatment processes. Water Res, 188 ( 2021), Article 116446
[9]
G. Wang, D. Wang, Y. Xu, Z. Li, L. Huang. Study on optimization and performance of biological enhanced activated sludge process for pharmaceutical wastewater treatment. Sci Total Environ, 739 ( 2020), Article 140166
[10]
D. Mosca Angelucci, E. Clagnan, L. Brusetti, M.C. Tomei. Anaerobic phenol biodegradation: kinetic study and microbial community shifts under high-concentration dynamic loading. Appl Microbiol Biotechnol, 104 (15) ( 2020), pp. 6825-6838 DOI: 10.1007/s00253-020-10696-8
[11]
X. Ma, M. Qi, Z. Li, Y. Zhao, P. Yan, B. Liang, et al.. Characterization of an efficient chloramphenicol-mineralizing bacterial consortium. Chemosphere, 222 ( 2019), pp. 149-155
[12]
X. Ma, B. Liang, M. Qi, H. Yun, K. Shi, Z. Li, et al.. Novel pathway for chloramphenicol catabolism in the activated sludge bacterial isolate Sphingobium sp. CAP-1. Environ Sci Technol, 54 (12) ( 2020), pp. 7591-7600 DOI: 10.1021/acs.est.9b07324
[13]
J. Zhang, W. Gan, R. Zhao, K. Yu, H. Lei, R. Li, et al.. Chloramphenicol biodegradation by enriched bacterial consortia and isolated strain Sphingomonas sp. CL5.1: the reconstruction of a novel biodegradation pathway. Water Res, 187 ( 2020), Article 116397
[14]
M. Sayed, A. Khan, S. Rauf, N.S. Shah, F. Rehman, A. Al-Kahtani, et al.. Bismuth-doped nano zerovalent iron: a novel catalyst for chloramphenicol degradation and hydrogen production. ACS Omega, 5 (47) ( 2020), pp. 30610-30624 DOI: 10.1021/acsomega.0c04574
[15]
H. Guo, N. Jiang, H. Wang, N. Lu, K. Shang, J. Li, et al.. Degradation of antibiotic chloramphenicol in water by pulsed discharge plasma combined with TiO2/WO3 composites: mechanism and degradation pathway. J Hazard Mater, 371 ( 2019), pp. 666-676
[16]
Z. Xin, T. Fengwei, W. Gang, L. Xiaoming, Z. Qiuxiang, Z. Hao, et al.. Isolation, identification and characterization of human intestinal bacteria with the ability to utilize chloramphenicol as the sole source of carbon and energy. FEMS Microbiol Ecol, 82 (3) ( 2012), pp. 703-712
CrossRef ADS Google scholar
[17]
T. Grummt, H.G. Wunderlich, A. Chakraborty, M. Kundi, B. Majer, F. Ferk, et al.. Genotoxicity of nitrosulfonic acids, nitrobenzoic acids, and nitrobenzylalcohols, pollutants commonly found in ground water near ammunition facilities. Environ Mol Mutagen, 47 (2) ( 2006), pp. 95-106 DOI: 10.1002/em.20172
[18]
Y. Liu, H. Li, R. Wang, Q. Hu, Y. Zhang, Z. Wang, et al.. Underlying mechanisms of promoted formation of haloacetic acids disinfection byproducts after indometacin degradation by non-thermal discharge plasma. Water Res, 220 ( 2022), Article 118701
[19]
H. Zhao, L. Yang, Y. Li, W. Xue, K. Li, Y. Xie, et al.. Environmental occurrence and risk assessment of haloacetic acids in swimming pool water and drinking water. RSC Adv, 10 (47) ( 2020), pp. 28267-28276 DOI: 10.1039/d0ra02389b
[20]
R. Zhao, K. Yu, J. Zhang, G. Zhang, J. Huang, L. Ma, et al.. Deciphering the mobility and bacterial hosts of antibiotic resistance genes under antibiotic selection pressure by metagenomic assembly and binning approaches. Water Res, 186 ( 2020), Article 116318
[21]
J. Zhang, X. Li, U. Klümper, H. Lei, T.U. Berendonk, F. Guo, et al.. Deciphering chloramphenicol biotransformation mechanisms and microbial interactions via integrated multi-omics and cultivation-dependent approaches. Microbiome, 10 (1) ( 2022), Article 180
[22]
R. Zhao, J. Feng, J. Huang, X. Li, B. Li. Reponses of microbial community and antibiotic resistance genes to the selection pressures of ampicillin, cephalexin and chloramphenicol in activated sludge reactors. Sci Total Environ, 755 (Pt 2) ( 2021), Article 142632
[23]
S. Chen, Y. Zhou, Y. Chen, J. Gu. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34 (17) ( 2018), pp. i884-i890 DOI: 10.1093/bioinformatics/bty560
[24]
D.E. Wood, J. Lu, B. Langmead. Improved metagenomic analysis with Kraken 2. Genome Biol, 20 (1) ( 2019), Article 257
[25]
J. Lu, F.P. Breitwieser, P. Thielen, S.L. Salzberg. Bracken: estimating species abundance in metagenomics data. PeerJ Comput Sci, 3(2017), Article e104 DOI: 10.7717/peerj-cs.104
[26]
S. Nurk, D. Meleshko, A. Korobeynikov, P.A. Pevzner. metaSPAdes: a new versatile metagenomic assembler. Genome Res, 27 (5) ( 2017), pp. 824-834 DOI: 10.1101/gr.213959.116
[27]
M. Kolmogorov, D.M. Bickhart, B. Behsaz, A. Gurevich, M. Rayko, S.B. Shin, et al.. metaFlye: scalable long-read metagenome assembly using repeat graphs. Nat Methods, 17 (11) ( 2020), pp. 1103-1110 DOI: 10.1038/s41592-020-00971-x
[28]
B.J. Walker, T. Abeel, T. Shea, M. Priest, A. Abouelliel, S. Sakthikumar, et al.. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One, 9 (11) ( 2014), Article e112963 DOI: 10.1371/journal.pone.0112963
[29]
Yu K, Qiu Z, Mu R, Qiao X, Zhang L, Lian CA, et al. Recovery of high-qualitied Genomes from a deep-inland Salt Lake Using BASALT. 2021. bioRxiv 2021.03.05.434042.
[30]
M.R. Olm, C.T. Brown, B. Brooks, J.F. Banfield. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J, 11 (12) ( 2017), pp. 2864-2868 DOI: 10.1038/ismej.2017.126
[31]
D.H. Parks, M. Imelfort, C.T. Skennerton, P. Hugenholtz, G.W. Tyson. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res, 25 (7) ( 2015), pp. 1043-1055 DOI: 10.1101/gr.186072.114
[32]
P.A. Chaumeil, A.J. Mussig, P. Hugenholtz, D.H. Parks. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics, 36 (6) ( 2019), pp. 1925-1927
[33]
D. Hyatt, G.L. Chen, P.F. Locascio, M.L. Land, F.W. Larimer, L.J. Hauser. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics, 11 (1) ( 2010), Article 119
[34]
T. Seemann. Prokka: rapid prokaryotic genome annotation. Bioinformatics, 30 (14) ( 2014), pp. 2068-2069 DOI: 10.1093/bioinformatics/btu153
[35]
T. Aramaki, R. Blanc-Mathieu, H. Endo, K. Ohkubo, M. Kanehisa, S. Goto, et al.. KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics, 36 (7) ( 2020), pp. 2251-2252 DOI: 10.1093/bioinformatics/btz859
[36]
T.A. Joseph, P. Chlenski, A. Litman, T. Korem, I. Pe’er. Accurate and robust inference of microbial growth dynamics from metagenomic sequencing reveals personalized growth rates. Genome Res, 32 (3) ( 2022), pp. 558-568 DOI: 10.1101/gr.275533.121
[37]
M.E. Ritchie, B. Phipson, D. Wu, Y. Hu, C.W. Law, W. Shi, et al.. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res, 43 (7) ( 2015), Article e47 DOI: 10.1093/nar/gkv007
[38]
E. Bolyen, J.R. Rideout, M.R. Dillon, N.A. Bokulich, C.C. Abnet, G.A. Al-Ghalith, et al.. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol, 37 (8) ( 2019), pp. 852-857 DOI: 10.1038/s41587-019-0209-9
[39]
Q. Wang, G.M. Garrity, J.M. Tiedje, J.R. Cole. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol, 73 (16) ( 2007), pp. 5261-5267
[40]
M. Nie, C. Yan, X. Xiong, X. Wen, X. Yang, Z. Lv, et al.. Degradation of chloramphenicol using a combination system of simulated solar light, Fe2+ and persulfate. Chem Eng J, 348 ( 2018), pp. 455-463
[41]
J. Chen, Y. Xia, Q. Dai. Electrochemical degradation of chloramphenicol with a novel Al doped PbO2 electrode: performance, kinetics and degradation mechanism. Electrochim Acta, 165 ( 2015), pp. 277-287
[42]
S. Chong, Y.L. Song, H. Zhao, G.M. Zhang, J. Li. Ultrasound/Zn0 for aqueous 4-nitrobenzoic acid degradation. Desalination Water Treat, 57 (52) (2016), pp. 24990-24998
CrossRef ADS Google scholar
[43]
M.A. Mazhar, N.A. Khan, S. Ahmed, A.H. Khan, A. Hussain, Rahisuddin, et al.. Chlorination disinfection by-products in municipal drinking water—a review. J Clean Prod, 273 ( 2020), Article 123159
[44]
J. Zhang, H. Zhang, X. Liu, F. Cui, Z. Zhao. Efficient reductive and oxidative decomposition of haloacetic acids by the vacuum-ultraviolet/sulfite system. Water Res, 210 ( 2022), Article 117974
[45]
K.Y. Park, S.Y. Choi, S.K. Ahn, J.H. Kweon. Disinfection by-product formation potential of algogenic organic matter from Microcystis aeruginosa: effects of growth phases and powdered activated carbon adsorption. J Hazard Mater, 408 ( 2021), Article 124864
[46]
X. Luan, H. Zhang, Z. Tian, M. Yang, X. Wen, Y. Zhang. Microbial community functional structure in an aerobic biofilm reactor: impact of streptomycin and recovery. Chemosphere, 255 ( 2020), Article 127032
[47]
R.A. Sorg, L. Lin, G.S. van Doorn, M. Sorg, J. Olson, V. Nizet, et al.. Collective resistance in microbial communities by intracellular antibiotic deactivation. PLoS Biol, 14 (12)( 2016), Article e2000631 DOI: 10.1371/journal.pbio.2000631
[48]
J. Zhang, X. Li, H. Lei, R. Zhao, W. Gan, K. Zhou, et al.. New insights into thiamphenicol biodegradation mechanism by Sphingomonas sp. CL5.1 deciphered through metabolic and proteomic analysis. J Hazard Mater, 426 (2022), Article 128101 DOI: 10.7498/aps.70.20220288
[49]
J. Zhang, C. Yang, J. Hu, Y. Zhang, Y. Lai, H. Gong, et al.. Deciphering a novel chloramphenicols resistance mechanism: oxidative inactivation of the propanediol pharmacophore. Water Res, 225 ( 2022), Article 119127
[50]
Y. Wang, Q. Xiang, Q. Zhou, J. Xu, D. Pei. Mini review: advances in 2-haloacid dehalogenases. Front Microbiol, 12 ( 2021), Article 758886
[51]
M. Meusel, H.J. Rehm. Biodegradation of dichloroacetic acid by freely suspended and adsorptive immobilized Xanthobacter autotrophicus GJ10 in soil. Appl Microbiol Biotechnol, 40 (1) ( 1993), pp. 165-171
[52]
B. Cao, K. Nagarajan, K.C. Loh. Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl Microbiol Biotechnol, 85 (2) ( 2009), pp. 207-228 DOI: 10.1007/s00253-009-2192-4
[53]
D. Kasai, T. Fujinami, T. Abe, K. Mase, Y. Katayama, M. Fukuda, et al.. Uncovering the protocatechuate 2,3-cleavage pathway genes. J Bacteriol, 191 (21) ( 2009), pp. 6758-6768
[54]
K.P. Barry, E.A. Taylor. Characterizing the promiscuity of LigAB, a lignin catabolite degrading extradiol dioxygenase from Sphingomonas paucimobilis SYK-6. Biochemistry, 52 (38) ( 2013), pp. 6724-6736 DOI: 10.1021/bi400665t
[55]
M.P. Valley, C.K. Brown, D.L. Burk, M.W. Vetting, D.H. Ohlendorf, J.D. Lipscomb. Roles of the equatorial tyrosyl iron ligand of protocatechuate 3,4-dioxygenase in catalysis. Biochemistry, 44 (33) ( 2005), pp. 11024-11039 DOI: 10.1021/bi050902i
[56]
H. Xu, L. Xiao, S. Zheng, Y. Zhang, J. Li, F. Liu. Reductive degradation of chloramphenicol by Geobacter metallireducens. Sci China Technol Sci, 62 (10) ( 2019), pp. 1688-1694 DOI: 10.1007/s11431-018-9415-2
[57]
T.S. Crofts, P. Sontha, A.O. King, B. Wang, B.A. Biddy, N. Zanolli, et al.. Discovery and characterization of a nitroreductase capable of conferring bacterial resistance to chloramphenicol. Cell Chem Biol, 26 (4) ( 2019), pp. 559-570
[58]
H. Chen, Q. Zhong. Antibacterial activity of acidified sodium benzoate against Escherichia coli O157:H7, Salmonella enterica, and Listeria monocytogenes in tryptic soy broth and on cherry tomatoes. Int J Food Microbiol, 274 ( 2018), pp. 38-44 DOI: 10.1117/12.2301006
[59]
M.J. Khoshnoud, A. Siavashpour, M. Bakhshizadeh, M. Rashedinia. Effects of sodium benzoate, a commonly used food preservative, on learning, memory, and oxidative stress in brain of mice. J Biochem Mol Toxicol, 32 (2) (2018), Article e22022
[60]
B. Liu, M. Terashima, N.T. Quan, N.T. Ha, L. Van Chieu, R. Goel, et al.. High nitrite concentration accelerates nitrite oxidising organism’s death. Water Sci Technol, 77 (11-12) ( 2018), pp. 2812-2822 DOI: 10.2166/wst.2018.272
[61]
J. Hrenović, Y. Orhan, H. Büyükgüngör, M. Horvatiček. Influence of ammonium, nitrate and nitrite on the performance of the pure culture of Acinetobacter junii. Biologia, 62 (5) ( 2007), pp. 517-522 DOI: 10.2478/s11756-007-0102-8
[62]
J.J. Rowe, J.M. Yarbrough, J.B. Rake, R.G. Eagon. Nitrite inhibition of aerobic bacteria. Curr Microbiol, 2 (1) ( 1979), pp. 51-54
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