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Journal of Environmental Science and Health, Part A
Toxic/Hazardous Substances and Environmental Engineering
Volume 58, 2023 - Issue 9
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Articles

Fate of antimicrobial resistance genes (ARG) and ARG carriers in struvite production process from human urine

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Pages 783-792 | Received 12 Jan 2023, Accepted 26 Jun 2023, Published online: 19 Jul 2023

References

  • Antonini, S.; Paris, S.; Eichert, T.; Clemens, J. Nitrogen and Phosphorous Recovery from Human Urine by Struvite Precipitation and Air Stripping in Vietnam. Clean Soil Air Water 2011, 39, 1099–1104. DOI: 10.1002/clen.201100036.
  • Decrey, L.; Udert, K. M.; Tilley, E.; Pecson, B. M.; Kohn, T. Fate of the Pathogen Indicators Phage ΦX174 and Ascaris Suum Eggs during the Production of Struvite Fertilizer from Source-Separated Urine. Water Res. 2011, 45, 4960–4972. DOI: 10.1016/j.watres.2011.06.042.
  • Etter, B.; Tilley, E.; Khadka, R.; Udert, K. M. Low Cost Struvite Production Using Source Separated Urine in Nepal. Water Res. 2011, 45, 852–862. DOI: 10.1016/j.watres.2010.10.007.
  • Liu, Z. G.; Zhao, Q. L.; Wang, K.; Lee, D. J.; Qiu, W.; Wang, J. F. Urea Hydrolysis and Recovery of Nitrogen and Phosphrous as MAP from Stale Human Urine. J. Environ. Sci. (China) 2008, 20, 1018–1024. DOI: 10.1016/s1001-0742(08)62202-0.
  • Liu, Z. G.; Zhao, Q. L.; Wang, K.; Qiu, W.; Li, W.; Wang, J. F. Comparison between Complete and Partial Recovery of N and P from Stale Human Urine with MAP Crystallization. J. Environ. Eng. Sci. 2008, 7, 223–228. DOI: 10.1139/S07-053.
  • Rahman, M.; Salleh, M. A. M.; Rashid, U.; Ahsan, A.; Hossain, M. M.; Ra, S. C. Production of Slow Release Crystal Fertilizer from Wastewaters through Struvite Crystallization – A Review. Arabian J. Chem. 2014, 7, 139–155. DOI: 10.1016/j.arabjc.2013.10.007.
  • Wilsenach, J. A.; Schuurbiers, M. C. M.; Loosdrecht, V. Phospahte and Potassium Recovery from Source Separated Urine through Struvite Precipitation. Water Res. 2007, 41, 458–466. DOI: 10.1016/j.watres.2006.10.014.
  • Winker, M.; Vinneras, B.; Muskolus, A.; Arnold, U.; Clemens, J. Fertilizer Products from New Sanitation Systems: Their Potential Values and Risks. Bioresour. Technol. 2009, 100, 4090–4096. DOI: 10.1016/j.biortech.2009.03.024.
  • Ackerman, A. L.; Chai, T. C. The Bladder is Not Sterile: An Update on the Urinary Microbiome. Curr. Bladder Dysfunct. Rep. 2019, 14, 331–341. DOI: 10.1007/s11884-019-00543-6.
  • Pearce, M. M.; Hilt, E. E.; Rosenfeld, A. B.; Zilliox, M. J.; White, K. T.; Fok, C.; Stephanie, K.; Schreckenberger, P. C.; Brubaker, L.; Gai, X.; Wolfe, A. J. The Female Urinary Microbiome: A Comparison of Women With and Without Urgency Urinary Incontinence. mBio 2014, 5, e01283-14. DOI: 10.1128/mBio.01283-14.
  • Fricke, W. F.; Maddox, C.; Song, Y.; Bromberg, J. S. Human Microbiota Characterization in the Course of Renal Transplantation. Am. J. Transplant. 2014, 14, 416–427. DOI: 10.1111/ajt.12588.
  • Maskell, R.; Pead, L.; Allen, J. The Puzzle of “Urethral Syndrome”: A Possible Answer? Lancet 1979, 1, 1058–1059. DOI: 10.1016/s0140-6736(79)92953-2.
  • Nelson, D. E.; Dong, Q.; Van Der Pol, B.; Toh, E.; Fan, B.; Katz, B. P.; Mi, D.; Rong, R.; Weinstock, G. M.; Sodergren, E.; Fortenberry, J. D. Bacterial Communities of the Coronal Sulcus and Distal Urethra of Adolescent Males. PLoS One 2012, 7, e36298. DOI: 10.1371/journal.pone.0036298.
  • Siddiqui, H.; Nederbragt, A. J.; Lagesen, K.; Jeansson, S. L.; Jakobsen, K. S. Assessing Diversity of the Female Urine Microbiota by High Throughput Sequencing of 16S rDNA Amplicons. BMC Microbiol. 2011, 11, 244. DOI: 10.1186/1471-2180-11-244.
  • Siddiqui, H.; Lagesen, K.; Nederbragt, A. J.; Jeansson, S. L.; Jakobsen, K. S. Alterations of Microbiota in Urine from Women with Interstitial Cystitis. BMC Microbiol. 2012, 12, 205. DOI: 10.1186/1471-2180-12-205.
  • Fane, S. Life Cycle Microbial Risk Analysis of Sustainable Sanitation Alternatives. In Ecosan- Closing the Loop. Proceedings of the 2nd International Symposium on Ecological Sanitation. Incorporating the 1st IWA Specialist Group Conference on Sustainable Sanitation, GTZ. Germany, 2004; pp. 389–396.
  • Lahr, R. H.; Goetsch, H. E.; Haig, S. J.; Hays, A. N.; Love, N. G.; Aga, D. S.; Bott, C. B.; Foxman, B.; Jimenez, J.; Luo, T.; et al. Urine Bacterial Community Convergence through Fertilizer Production: Storage, Pasteurization, and Struvite Precipitation. Environ. Sci. Technol. 2016, 50, 11619–11626. DOI: 10.1021/acs.est.6b02094.
  • Goetsch, H. E.; Love, N. G.; Wigginton, K. R. Fate of Extracellular DNA in the Production of Fertilizers from Source-Separated Urine. Environ. Sci. Technol. 2020, 54, 1808–1815. DOI: 10.1021/acs.est.9b04263.
  • Li, H.; Zheng, X.; Tan, L.; Shao, Z.; Cao, H.; Xu, Y. The Vertical Migration of Antibiotic-Resistant Genes and Pathogens in Soil and Vegetables after the Application of Different Fertilizers. Environ. Res. 2022, 203, 111884. DOI: 10.1016/j.envres.2021.111884.
  • Jadeja, N. B.; Worrich, A. From Gut to Mud: Dissemination of Antimicrobial Resistance between Animal and Agricultural Niches. Environ. Microbiol. 2022, 24, 3290–3306. DOI: 10.1111/1462-2920.15927.
  • Yang, Y.; Ashworth, A.; DeBruyn, J. M.; Durso, L. M.; Savin, M.; Cook, K.; Moore, P. A.; Jr.; Owens, P. R. Antimicrobial Resistant Gene Prevalence in Soils Due to Animal Manure Deposition and Long-Term Pasture Management. Peer J. 2020, 8, e10258. DOI: 10.7717/peerj.10258. PMID: 33194426; PMCID: PMC7646296.
  • Haaber, J.; Leisner, J. J.; Cohn, T. M.; Catalan-Moreno, A.; Nielsen, B. J.; Westh, H.; Penadés, J. R.; Ingmer, H. Bacterial Viruses Enable their Host to Acquire Antibiotic Resistance Genes from Neighbouring Cells. Nat. Commun. 2016, 7, 1–8. DOI: 10.1038/ncomms13333.
  • Malachowa, N.; DeLeo, F. R. Mobile Genetic Elements of Staphylococcus aureus. Cell. Mol. Life Sci. 2010, 67, 3057–3071. DOI: 10.1007/s00018-010-0389-4.
  • Muniesa, M.; García, A.; Miró, E.; Mirelis, B.; Prats, G.; Jofre, J.; Navarro, F. Bacteriophages and Diffusion of Beta-Lactamase Genes. Emerg. Infect. Dis. 2004, 10, 1134–1137. DOI: 10.3201/eid1006.030472.
  • Witte, W. International Dissemination of Antibiotic Resistant Strains of Bacterial Pathogens. Infect. Genet. Evol. 2004, 4, 187–191. DOI: 10.1016/j.meegid.2003.12.005.
  • Brabban, A. D.; Hite, E.; Callaway, T. R. Evolution of Foodborne Pathogens via Temperate Bacteriophage-Mediated Gene Transfer. Foodborne Pathog. Dis. 2005, 2, 287–303. DOI: 10.1089/fpd.2005.2.287.
  • Piddock, L. J. V. Reflecting on the Final Report of the O’Neill Review on Antimicrobial Resistance. Lancet Infect. Dis. 2016, 16, 767–768. DOI: 10.1016/S1473-3099(16)30127-X.
  • Moon, K.; Jeon, J. H.; Kang, I.; Park, K. S.; Lee, K.; Cha, C. J.; Lee, S. H.; Cho, J. C. Freshwater Viral Metagenome Reveals Novel and Functional Phage-Borne Antibiotic Resistance Genes. Microbiome 2020, 8, 75. DOI: 10.1186/s40168-020-00863-4.
  • World Health Organization (WHO). Global Antimicrobial Resistance Surveillance System (GLASS) Report: Early Implementation 2017-2018; WHO: Geneva; 2018.
  • Tsai, Y. L.; Olson, B. H. Rapid Method for Separation of Bacterial DNA from Humic Substances in Sediments for Polymerase Chain Reaction. Appl. Environ. Microbiol. 1992, 58, 2292–2295. DOI: 10.1128/aem.58.7.2292-2295.1992.
  • Silva, M. A. L.; Medeiros, Z.; Cynthia , Soares, C. R. P.; Silva, E. D.; Miranda-Filho, D. B.; Melo, F. L. A Comparison of Four DNA Extraction Protocols for the Analysis of Urine from Patients with Visceral Leishmaniasis. Rev. Soc. Bras. Med. Trop. 2014, 47, 193–197. DOI: 10.1590/0037-8682-0233-2013.
  • Geissler, M.; Isabel, S.; Voisin, B.; Fauvel, C.; Boissinot, M.; Bergeron, M. G.; Veres, T. Modular Ultrasonic Lysis System for Rapid Nucleic Acid Extraction and Sample Transfer of Bacillus Spores. J. Bioterr. Biodef. 2012, 03, 119. DOI: 10.4172/2157-2526.1000119.
  • Kleinheinz, K. A.; Joensen, K. G.; Larsen, M. V. Applying the ResFinder and Virulence Finder Web-Services for Easy Identification of Acquired Antibiotic Resistance and E. coli Virulence Genes in Bacteriophage and Prophage Nucleotide Sequences. Baceriophage 2014, 4, e27943. DOI: 10.4161/bact.27943.
  • van der Graaf-van Bloois, L.; Wagenaar, J. A.; Zomer, A. L. RFPlasmid: Predicting Plasmid Sequences from Short Read Assembly Data Using Machine Learning. Microb. Genomics 2021, 7, DOI: 10.1099/mgen.0.000683. PMID: 34846288; PMCID: PMC8743549.
  • Wojciuk, B.; Salabura, A.; Grygorcewicz, B.; Kędzierska, K.; Ciechanowski, K.; Dołęgowska, B. Urobiome: In Sickness and in Health. Microorganisms 2019, 7, 548. DOI: 10.3390/microorganisms7110548.
  • Żaczek, M.; Weber-Dąbrowska, B.; Międzybrodzki, R.; Górski, A. Phage Prevalence in the Human Urinary Tract—Current Knowledge and Therapeutic Implications. Microorganisms 2020, 8, 1802. DOI: 10.3390/microorganisms8111802.
  • Yildirim, Z.; Sakin, T.; Akçelik, M.; Akçelik, N. Identification and Characterization of Lytic Bacteriophages Specific to Foodborne Pathogenic Escherichia coli O157:H7. Food Sci. Technol. Int. 2021, 27, 56–72. DOI: 10.1177/1082013220929836.
  • Peng, Q.; Yuan, Y. Characterization of a Newly Isolated Phage Infecting Pathogenic Escherichia coli and Analysis of Its Mosaic Structural Genes. Sci Rep 2018, 8, 8086. DOI: 10.1038/s41598-018-26004-4.
  • Lukman, C.; Yonathan, C.; Magdalena, S.; Waturangi, D. E. Isolation and Characterization of Pathogenic Escherichia coli Bacteriophages from Chicken and Beef Offal. BMC Res Notes 2020, 13, 8. DOI: 10.1186/s13104-019-4859-y.
  • Muniesa, M.; Colomer-Lluch, M.; Jofre, J. Potential Impact of Environmental Bacteriophages in Spreading Antibiotic Resistance Genes. Future Microbiol 2013, 8, 739–751. DOI: 10.2217/fmb.13.32.
  • Muniesa, M.; Colomer-Lluch, M.; Jofre, J. Could Bacteriophages Transfer Antibiotic Resistance Genes from Environmental Bacteria to Human-Body Associated Bacterial Populations? Mob. Genet. Elements 2013, 3, e25847. DOI: 10.4161/mge.25847. Epub 2013 Aug 2. PMID: 24195016; PMCID: PMC3812792.
  • Evans, T. J.; Crow, M. A.; Williamson, N. R.; Orme, W.; Thomson, N. R.; Komitopoulou, E.; Salmond, G. P. C. Characterization of a Broad-Host-Range Flagellum-Dependent Phage That Mediates High-Efficiency Generalized Transduction in, and between, Serratia and Pantoea. Microbiology (Reading) 2010, 156, 240–247. DOI: 10.1099/mic.0.032797-0.
  • Petrovski, S.; Seviour, R. J.; Tillett, D. Characterization of the Genome of the Polyvalent Lytic Bacteriophage GTE2, Which Has Potential for Biocontrol of Gordonia-, Rhodococcus-, and Nocardia-Stabilized Foams in Activated Sludge Plants. Appl. Environ. Microbiol. 2011, 77, 3923–3929. DOI: 10.1128/AEM.00025-11.
  • Souza, K. A.; Ginoza, H. S.; Haight, R. D. Isolation of a Polyvalent Bacteriophage for Escherichia coli, Klebsiella pneumoniae, and Aerobacter Aerogenes. J. Virol. 1972, 9, 851–856. DOI: 10.1128/JVI.9.5.851-856.1972.
  • Colomer-Lluch, M.; Jofre, J.; Muniesa, M. Antibiotic Resistance Genes in the Bacteriophage DNA Fraction of Environmental Samples. PLoS One. 2011, 6, e17549. DOI: 10.1371/journal.pone.0017549.
  • Colomer-Lluch, M.; Jofre, J.; Muniesa, M. Quinolone Resistance Genes (qnrA and qnrS) in Bacteriophage Particles from Wastewater Samples and the Effect of Inducing Agents on Packaged Antibiotic Resistance Genes. J. Antimicrob. Chemother. 2014, 69, 1265–1274. DOI: 10.1093/jac/dkt528.
  • American Academy of Microbiology. Antibiotic Resistance: An Ecological Perspective on an Old Problem. This report is based on a colloquium, sponsored by the American Academy of Microbiology, convened October 12–14, 2008, at the conference center of the Fondation Mérieux in Annecy, American Society for Microbiology: France. Washington (DC), 2009. PMID: 32644325.
  • Starliper, C. E.; Watten, B. J.; Iwanowicz, D. D.; Green, P. A.; Bassett, N. L.; Adams, C. R. Efficacy of pH Elevation as a Bactericidal Strategy for Treating Ballast Water of Freight Carriers. J. Adv. Res. 2015, 6, 501–509. DOI: 10.1016/j.jare.2015.02.005.
  • La Rosa, R.; Johansen, H. K.; Molin, S. Persistent Bacterial Infections, Antibiotic Treatment Failure, and Microbial Adaptive Evolution. Antibiotics 2022, 11, 419. DOI: 10.3390/antibiotics11030419.
  • Vermeulen, A.; Gysemans, K. P. M.; Bernaerts, K.; Geeraerd, A. H.; Van Impe, J. F.; Debevere, J.; Devlieghere, F. Influence of pH, Water Activity and Acetic Acid Concentration on Listeria monocytogenes at 7 °C: Data Collection for the Development of a Growth/No Growth Model. Int. J. Food Microbiol. 2007, 114, 332–341. DOI: 10.1016/j.ijfoodmicro.2006.09.023.
  • Havenga, B.; Ndlovu, T.; Clements, T.; Reyneke, B.; Waso, M.; Khan, W. Exploring the Antimicrobial Resistance Profiles of WHO Critical Priority List Bacterial Strains. BMC Microbiol 2019, 19, 303. DOI: 10.1186/s12866-019-1687-0.
  • Bischel, H. N.; Schindelholz, S.; Schoger, M.; Decrey, L.; Buckley, C. A.; Udert, K. M.; Kohn, T. Bacteria Inactivation during the Drying of Struvite Fertilizers Produced from Stored Urine. Environ. Sci. Technol. 2016, 50, 13013–13023. DOI: 10.1021/acs.est.6b03555.
  • Bayer, A. S.; Schneider, T.; Sahl, H. G. Mechanisms of Daptomycin Resistance in Staphylococcus aureus: Role of the Cell Membrane and Cell Wall. Ann. NY Acad. Sci. 2013, 1277, 139–158. DOI: 10.1111/j.1749-6632.2012.06819.x.
  • Gundogdu, A.; Ulu-Kilic, A.; Kilic, H.; Ozhan, E.; Altun, D.; Cakir, O.; Alp, E. Could Frequent Carbapenem Use Be a Risk Factor for Colistin Resistance? Microb. Drug Resist. 2018, 24, 774–781. DOI: 10.1089/mdr.2016.0321.
  • Schürmann, B.; Everding, W.; Montag, D.; Pinnekamp, J. Fate of Pharmaceuticals and Bacteria in Stored Urine during Precipitation and Drying of Struvite. Water Sci. Technol. 2012, 65, 10.
  • Colomer-Lluch, M.; Imamovic, L.; Jofre, J.; Muniesa, M. Bacteriophages Carrying Antibiotic Resistance Genes in Fecal Waste from Cattle, Pigs, and Poultry. Antimicrob. Agents Chemother. 2011, 55, 4908–4911. DOI: 10.1128/AAC.00535-11.

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