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Mesophilic and thermophilic anaerobic digestion of swine manure with sulfamethoxazole and norfloxacin: Dynamics of microbial communities and evolution of resistance genes

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Abstract

The role of norfloxacin (NOR) and sulfamethoxazole (SMX) in mesophilic and thermophilic anaerobic digestion (AD) of pig manure, with respect to methane production and variations in the microbial community and resistance genes, including antibiotic resistance genes (ARGs), class I integrase (intIl), and heavy metal resistance genes (MRGs), was investigated. The results indicated that NOR exerted little influence on the microbial community, whereas SMX negatively affected the acetoclastic methanogens. The abundance of two sulfonamide resistance genes (sul1 and sul2), three quinolone resistance genes (qnrS, parC, and aac(6′)-Ib-cr), and intI1 decreased by 2–3 orders of magnitude at the end of thermophilic AD. In contrast, mesophilic AD was generally ineffective in reducing the abundance of resistance genes. According to the results of redundancy analysis, the abundance of ARGs was affected primarily by microbial community dynamics (68.5%), rather than the selective pressure due to antibiotic addition (13.3%). Horizontal gene transfer (HGT) through intI1 contributed to 26.4% of the ARG variation. The archaeal community also influenced the changes in the resistance genes, and ARG reduction was significantly correlated with enhanced methane production. Thermophilic AD presented a higher methane production potential and greater reduction in resistance gene abundance.

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References

  • An X L, Chen Q L, Zhu D, Zhu Y G, Gillings M R, Su J Q (2018). Impact of wastewater treatment on the prevalence of integrons and the genetic diversity of integron gene cassettes. Applied and Environmental Microbiology, 84(9): e02766–02717

    Article  CAS  Google Scholar 

  • Chen Q, An X, Li H, Su J, Ma Y, Zhu Y G (2016). Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environment International, 92–93: 1–10

    Article  Google Scholar 

  • Chen Z Q, Li M, Wen Q X (2017). Comprehensive evaluation of three sets of advanced wastewater treatment trains for treating secondary effluent: Organic micro-pollutants and bio-toxicity. Chemosphere, 189: 426–434

    Article  CAS  Google Scholar 

  • Duan M L, Li H C, Gu J, Tuo X X, Sun W, Qian X, Wang X J (2017). Effects of biochar on reducing the abundance of oxytetracycline, antibiotic resistance genes, and human pathogenic bacteria in soil and lettuce. Environmental Pollution, 224: 787–795

    Article  CAS  Google Scholar 

  • Gaze W H, Zhang L, Abdouslam N A, Hawkey P M, Calvo-Bado L, Royle J, Brown H, Davis S, Kay P, Boxall ABA, Wellington E M H (2011). Impacts of anthropogenic activity on the ecology of Class 1 integrons and integron-associated genes in the environment. ISME Journal, 5(8): 1253–1261

    Article  CAS  Google Scholar 

  • Grabowski A, Tindall B J, Bardin V, Blanchet D, Jeanthon C (2005). Petrimonas sulfuriphila gen. nov., sp. nov., amesophilic fermentative bacterium isolated from a biodegraded oil reservoir. International Journal of Systematic and Evolutionary Microbiology, 55(3): 1113–1121

    Article  CAS  Google Scholar 

  • Hatamoto M, Imachi H, Fukayo S, Ohashi A, Harada H (2007). Syntrophomonaspalmitatica sp. nov., an anaerobic, syntrophic, long-chain fatty-acid-oxidizing bacterium isolated from methanogenic sludge. International Journal of Systematic and Evolutionary Microbiology, 57(9): 2137–2142

    Article  CAS  Google Scholar 

  • Hu J, Xu Q, Li X, Wang D, Zhou Y, Zhao J, Zhang D, Yang Q, Zeng G (2018). Sulfamethazine affects fermentative short-chain fatty acids production from waste activated sludge. Science of the Total Environment, 639: 1471–1479

    Article  CAS  Google Scholar 

  • Jang H M, Lee J, Choi S, Shin J, Kan E, Kim Y M (2018). Response of antibiotic and heavy metal resistance genes to two different temperature sequences in anaerobic digestion of waste activated sludge. Bioresource Technology, 267: 303–310

    Article  CAS  Google Scholar 

  • Kaplan E, Ofek M, Jurkevitch E, Cytryn E (2013). Characterization of fluoroquinolone resistance and qnr diversity in Enterobacteriaceae from municipal biosolids. Frontiers in Microbiology, 4: 144

    Article  Google Scholar 

  • Larrañaga O, Brown-Jaque M, Quirós P, Gómez-Gómez C, Blanch A, Rodríguez-Rubio L, Muniesa M (2018). Phage particles harboring antibiotic resistance genes in fresh-cut vegetables and agricultural soil. Environment International, 115: 133–141

    Article  Google Scholar 

  • Li L H, Li Y, Sun Y M, Yuan Z H, Kang X H, Zhang Y, Yang G X (2018a). Effect of bioaugmentation on the microbial community and mono-digestion performance of Pennisetum hybrid. Waste Management (New York, N.Y.), 78: 741–749

    Article  CAS  Google Scholar 

  • Li Y, Sun Y M, Li L H, Yuan Z H (2018b). Acclimation of acid-tolerant methanogenic propionate-utilizing culture and microbial community dissecting. Bioresource Technology, 250: 117–123

    Article  CAS  Google Scholar 

  • Ma Y, Wilson C A, Novak J T, Riffat R, Aynur S, Murthy S, Pruden A (2011). Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline resistance genes and Class 1 integrons. Environmental Science & Technology, 45(18): 7855e7861

    Article  Google Scholar 

  • Palmer A C, Kishony R (2013). Understanding, predicting and manipulating the genotypic evolution of antibiotic resistance. Nature Reviews. Genetics, 14(4): 243–248

    CAS  Google Scholar 

  • Selvam A, Zhao Z, Wong J W C (2012). Composting of swine manure spiked with sulfadiazine, chlortetracycline and ciprofloxacin. Bioresource Technology, 126: 412–417

    Article  CAS  Google Scholar 

  • Song W, Wang X J, Gu J, Zhang S Q, Yin Y N, Li Y, Qian X, Sun W (2017). Effects of different swine manure to wheat straw ratios on antibiotic resistance genes and the microbial community structure during anaerobic digestion. Bioresource Technology, 231: 1–8

    Article  CAS  Google Scholar 

  • Wang H T, Chi Q Q, Zhu D, Li G, Ding J, An X L, Zheng F, Zhu Y G, Xue X M (2019). Arsenic and sulfamethoxazole increase the incidence of antibiotic resistance genes in the gut of earthworm. Environmental Science & Technology, 53(17): 10445–10453

    Article  CAS  Google Scholar 

  • Wen Q X, Chen Z Q, Wang C Y, Ren N Q (2012). Bulking sludge for PHA production: Energy saving and comparative storage capacity with well-settled sludge. Journal of Environmental Sciences-China, 24(10): 1744–1752

    Article  CAS  Google Scholar 

  • Xiong X, Li Y X, Li W, Lin C Y, Han W, Yang M (2010). Copper content in animal manures and potential risk of soil copper pollution with animal manure use in agriculture. Resources, Conservation and Recycling, 54(11): 985–990

    Article  Google Scholar 

  • Xu R, Yang Z H, Zheng Y, Liu J B, Xiong W P, Zhang Y R, Lu Y, Xue W J, Fan C Z (2018). Organic loading rate and hydraulic retention time shape distinct ecological networks of anaerobic digestion related microbiome. Bioresource Technology, 262: 184–193

    Article  CAS  Google Scholar 

  • Xu R, Yang Z H, Zheng Y, Wang Q P, Bai Y, Liu J B, Zhang Y R, Xiong W P, Lu Y, Fan C Z (2019). Metagenomic analysis reveals the effects of long-term antibiotic pressure on sludge anaerobic digestion and antimicrobial resistance risk. Bioresource Technology, 282: 179–188

    Article  CAS  Google Scholar 

  • Yang Z M, Shi X S, Dai M, Wang L, Xu X H, Guo R B (2018). Promoting degradation of 2,4-dichlorophenoxyacetic acid with fermentative effluents from hydrogen-producing reactor. Chemosphere, 201: 859–863

    Article  CAS  Google Scholar 

  • Yi J, Dong B, Jin J W, Dai X H (2014). Effect of increasing total solids contents on anaerobic digestion of food waste under mesophilic conditions: Performance and microbial characteristics analysis. PLoS One, 9(7): e102548

    Article  Google Scholar 

  • Zhang J Y, Sui Q W, Tong J, Buhe C, Wang R, Chen M X, Wei Y S (2016). Sludge bio-drying: Effective to reduce both antibiotic resistance genes and mobile genetic elements. Water Research, 106: 62–70

    Article  Google Scholar 

  • Zhang J Y, Sui Q W, Zhong H, Meng X S, Wang Z Y, Wang Y W, Wei Y S (2018). Impacts of zero valent iron, natural zeolite and Dnase on the fate of antibiotic resistance genes during thermophilic and mesophilic anaerobic digestion of swine manure. Bioresource Technology, 258: 135–141

    Article  CAS  Google Scholar 

  • Zhang J Y, Wang Z Y, Lu T D, Liu J B, Wang Y W, Shen P H, Wei Y S (2019). Response and mechanisms of the performance and fate of antibiotic resistance genes to nano-magnetite during anaerobic digestion of swine manure. Journal of Hazardous Materials, 366: 192–201

    Article  CAS  Google Scholar 

  • Zhang T, Yang Y, Pruden A (2015). Effect of temperature on removal of antibiotic resistance genes by anaerobic digestion of activated sludge revealed by metagenomic approach. Applied Microbiology and Biotechnology, 99(18): 7771–7779

    Article  CAS  Google Scholar 

  • Zhao L, Ji Y, Sun P Z, Deng J H, Wang H Y, Yang Y K (2019). Effects of individual and combined zinc oxide nanoparticle, norfloxacin, and sulfamethazine contamination on sludge anaerobic digestion. Bioresource Technology, 273: 454–461

    Article  CAS  Google Scholar 

  • Zheng J, Gao R X, Wei Y Y, Chen T, Fan J Q, Zhou Z C, Makimilua T B, Jiao Y N, Chen H (2017). High-throughput profiling and analysis of antibiotic resistance genes in east Tiaoxi River. China. Environmental Pollution, 230: 648–654

    Article  CAS  Google Scholar 

  • Zhou X, Wang J, Lu C, Liao Q, Gudda F O, Ling W (2020). Antibiotics in animal manure and manure-based fertilizers: Occurrence and ecological risk assessment. Chemosphere, 255: 127006

    Article  CAS  Google Scholar 

  • Zwietering M H, Jongenburger I, Rombouts F M, Van’t Riet K (1990). Modeling of the bacterial growth curve. Applied and Environmental Microbiology, 56(6): 1875–1881

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 51878214) and the National Key Research and Development Program of China (No. 2019YFD1100200).

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Correspondence to Zhiqiang Chen.

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Highlights

• SMX addition had negative effect on acetoclastic methanogens in mesophilic AD.

• Thermophilic AD was more effective in eliminating resistance genes than mesophilic.

• ARGs variations in AD were mainly affected by succession of microbial community.

• Methane production was significant associated to ARGs reduction.

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Wen, Q., Yang, S. & Chen, Z. Mesophilic and thermophilic anaerobic digestion of swine manure with sulfamethoxazole and norfloxacin: Dynamics of microbial communities and evolution of resistance genes. Front. Environ. Sci. Eng. 15, 94 (2021). https://doi.org/10.1007/s11783-020-1342-x

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  • DOI: https://doi.org/10.1007/s11783-020-1342-x

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