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Pattern of multiresistant to antimicrobials and heavy metal tolerance in bacteria isolated from sewage sludge samples from a composting process at a recycling plant in southern Brazil

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Abstract

The composting process is a viable alternative for the recycling of household organic waste and sewage sludge generated during wastewater treatment. However, this technique can select microorganisms resistant to antimicrobials and heavy metals as a result of excess chemicals present in compost windrow. This study evaluates the antimicrobial multiresistant and tolerance to heavy metals in bacteria isolated from the composting process with sewage sludge. Fourteen antimicrobials were used in 344 strains for the resistance profile and four heavy metals (chromium, copper, zinc, and lead) for the minimum biocide concentration assay. The strains used were from the sewage sludge sample (beginning of the process) and the compost sample (end of the process). Strains with higher antimicrobial and heavy metal profile were identified by 16S rRNA gene sequencing. The results showed a multiresistant profile in 48 % of the strains, with the highest percentage of strains resistant to nitrofurantoin (65 %) and β-lactams (58 %). The strains isolated from the sewage sludge and the end of the composting process were more tolerant to copper, with a lethal dose of approximately 900 mg L−1 for about 50 % of the strains. The genera that showed the highest multiresistant profile and increased tolerance to the metals tested were Pseudomonas and Ochrobactrum. The results of this study may contribute to future research and the revision and regulation of legislation on sewage sludge reuse in soils.

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References

  • Alam, M. Z., Ahmad, S., & Malik, A. (2011). Prevalence of heavy metal resistance in bacteria isolated from tannery effluents and affected soil. Environmental Monitoring and Assessment, 178, 281–291.

    Article  CAS  Google Scholar 

  • Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.

    Article  CAS  Google Scholar 

  • Bauer, A. W., Kirby, W. M. M., Sherris, J. C., & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45, 493–496.

    CAS  Google Scholar 

  • Bruins, M. R., Kapil, S., & Oehme, F. W. (2000). Microbial resistance to metals in the environment. Ecotoxicology and Environmental Safety, 45, 198–207.

    Article  CAS  Google Scholar 

  • Bustamante, M. A., Restrepo, A. P., Albuquerque, J. A., Pérez-Murcia, M. D., Paredes, C., & Moral, R. (2013). Recycling of anaerobic digestates by composting: effect of the bulking agent used. Journal of Cleaner Production, 47, 61–69.

    Article  CAS  Google Scholar 

  • Cabral, L., Giovanella, P., Gianello, C., Bento, F. M., Andreazza, R., & Camargo, F. A. O. (2013). Isolation and characterization of bacteria from mercury contaminated sites in Rio Grande do Sul, Brazil, and assessment of methylmercury removal capability of a Pseudomonas putida V1 strain. Biodegradation, 24, 319–331.

    Article  CAS  Google Scholar 

  • Cheng, A. C., Turnidge, J., Collignon, P., Looke, D., Barton, M., & Gottlieb, T. (2012). Control of fluoroquinolone resistance through successful regulation. Emerging Infectious Diseases, 18, 1453–1460.

    Article  CAS  Google Scholar 

  • CLSI (2009). Clinical and laboratory standards institute. Performance standards for antimicrobial disk susceptibility tests; Approved standard. 10th ed. 29: M02-A10.

  • CONAMA – Conselho Nacional do Meio Ambiente. Resolution n° 375/2006, 29/8/2006. http://www.mma.gov.br/port/conama/legiano/. Accessed 10 December 2013.

  • Conklin, J. D. (1978). The pharmacokinetics of nitrofurantoin and its related bioavailability. Antibiotics and Chemotherapy, 25, 233–252.

    CAS  Google Scholar 

  • Ewing, B., & Green, P. (1998). Base-calling of automated sequencer traces using Phred. II, Error probabilities. Genome Research, 8, 186–194.

    Article  CAS  Google Scholar 

  • Ewing, B., Hillier, L., Wendl, M. C., & Green, P. (1998). Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Research, 8, 175–185.

    Article  CAS  Google Scholar 

  • Giovanella, P., Bento, F. M., Cabral, L., Gianello, C., & Camargo, F. A. O. (2011). Isolation and selection of microorganisms resistant and able to volatilize mercury. Quimica Nova, 34, 232–236.

    Article  CAS  Google Scholar 

  • Göbel, A., McArdell, C. S., Joss, A., Siegrist, H., & Giger, W. (2007). Fate of sulfonamides, macrolides, and trimethoprim in different wastewater treatment technologies. Science of the Total Environment, 372, 361–371.

    Article  Google Scholar 

  • Gordon, D., Abajian, C., & Green, P. (1998). Consed: a graphical tool for sequence finishing. Genome Research, 8, 195–202.

    Article  CAS  Google Scholar 

  • Gray, K. R., Sherman, K., & Biddlestone, A. J. (1971). A review of composting. Part I. Process Biochemistry, 6, 32–36.

    CAS  Google Scholar 

  • Guan, J., Wasty, A., Grenier, C., & Chan, M. (2007). Influence of temperature on survival and conjugative transfer of multiple antibiotic-resistant plasmids in chicken manure and compost microcosms. Poultry Science, 86, 610–613.

    Article  CAS  Google Scholar 

  • Hargreaves, J. C., Adl, M. S., & Warman, P. R. (2008). A review of the use of composted municipal solid waste in agriculture. Agriculture, Ecosystems & Environment, 123, 1–14.

    Article  Google Scholar 

  • Heck, K., De Marco, E. G., Hahn, A. B. B., Kluge, M., Spilki, F. R., & Van Der Sand, S. (2013). Evaluation of degradation temperature of compounds in a composting process and microbiological quality of the compost. Revista Brasileira de Engenharia Agrícola e Ambiental, 17, 54–59.

    Article  Google Scholar 

  • Heringa, S., Kim, J., Shepherd, M. W., Jr., Singh, R., & Jiang, X. (2010). The presence of antibiotic resistance and integrons in Escherichia coli isolated from compost. Foodborne Pathogens and Disease, 7, 1297–1304.

    Article  CAS  Google Scholar 

  • Higgins, C. S., Avison, M. B., Jamieson, L., Simm, A. M., Bennett, P. M., & Walsh, T. R. (2001). Characterization, cloning and sequence analysis of the inducible Ochrobactrum anthropi AmpC β-lactamase. Journal of Antimicrobial Chemotherapy, 47, 745–754.

    Article  CAS  Google Scholar 

  • Hirsch, R., Ternes, T., Haberer, K., & Kratz, K. (1999). Occurrence of antibiotics in the aquatic environment. Science of the Total Environment, 225, 109–118.

    Article  CAS  Google Scholar 

  • Hoffmeister, D., Germani, J. C., & Van Der Sand, S. T. (2005). Characterization of bacterial population during composting of municipal solid waste. Acta Scientiae Veterinariae, 33, 283–290.

    Google Scholar 

  • Hölzel, C. S., Schwaiger, K., Harms, K., Küchenhoff, H., Kunz, A., Meyer, K., Müller, C., & Bauer, J. (2010). Sewage sludge and liquid pig manure as possible sources of antibiotic resistant bacteria. Environmental Research, 110, 318–326.

    Article  Google Scholar 

  • Ju-Nam, Y., & Lead, J. R. (2008). Manufactured nanoparticles: an overview of their chemistry, interactions and potential environmental implications. Science of the Total Environment, 400, 396–414.

    Article  CAS  Google Scholar 

  • Kabala, C., Karczewska, A., Szopka, K., & Wilk, J. (2011). Copper, zinc, and lead fractions in soils long-term irrigated with municipal wastewater. Communications in Soil Science and Plant Analysis, 42, 905–919.

    Article  CAS  Google Scholar 

  • Kakimoto, T., Osawa, T., & Funamizu, N. (2007). Antibiotic effect of amoxicillin on the feces composting process and reactivation of bacteria by intermittent feeding of feces. Bioresource Technology, 98, 3555–3560.

    Article  CAS  Google Scholar 

  • Kaszab, E., Szoboszlay, S., Dobolyi, C., Háhn, J., Pék, N., & Kriszt, B. (2011). Antibiotic resistance profiles and virulence markers of Pseudomonas aeruginosa strains isolated from composts. Bioresource Technology, 102, 1543–1548.

    Article  CAS  Google Scholar 

  • Kim, J., Shepherd, M. W., Jr., & Jiang, X. (2009). Evaluating the effect of environmental factors on pathogen regrowth in compost extract. Microbial Ecology, 58, 498–508.

    Article  Google Scholar 

  • Kobya, M., Demirbas, E., Senturk, E., & Ince, M. (2005). Adsorption of heavy metal ions from aqueous solutions by activated carbon prepared from apricot stone. Bioresource Technology, 96, 1518–1521.

    Article  CAS  Google Scholar 

  • Lane, D. J. (1991). 16S/23S rRNA sequencing. In E. Stackebrandt & M. Goodfellwon (Eds.), Nucleic acid techniques in bacterial systematics (pp. 115–175). Chichester: John Wiley & Sons.

    Google Scholar 

  • Laura, D., De Socio, G., Frassnito, R., & Rotilio, D. (1996). Effects of atrazine on Ochrobactrum anthropi membrane fatty acids. Applied and Environmental Microbiology, 62, 2644–2646.

    CAS  Google Scholar 

  • Lin, S., Wu, Z., Yu, G., Zhu, M., Yu, B., & Li, R. (2010). Genetic diversity and molecular phylogeny of Planktothrix (Oscillatorailes, cyanobacteria) strains from China. Harmful Algae, 9, 87–97.

    Article  Google Scholar 

  • Luczkiewicz, A., Jankowska, K., Fudala-Ksiazek, S., & Olankzuk-Neyman, K. (2010). Antimicrobial resistance of fecal indicators in municipal wastewater treatment plant. Water Research, 44, 5089–5097.

    Article  CAS  Google Scholar 

  • Mashouf, R. Y., Babalhavaeji, H., & Yousef, J. (2009). Urinary tract infections: bacteriology and atibiotic resistance patterns. Indian Pediatrics, 46, 617–620.

    Google Scholar 

  • Matyar, F., Akkan, T., Uçak, Y., & Eraslan, B. (2010). Aeromonas and Pseudomonas: antibiotic and heavy metal resistance species from Iskenderun Bay, Turkey (Northeast Mediterranean Sea). Environmental Monitoring and Assessment, 167, 309–320.

    Article  CAS  Google Scholar 

  • McGrath, S. P., Chambers, B. J., Taylor, M. J., & Carlton-Smith, C. H. (2012). Biofortification of zinc in wheat grain by the application of sewage sludge. Plant and Soil, 361, 97–108.

    Article  CAS  Google Scholar 

  • Nagulapally, S. R., Ahmad, A., Henry, A., Marchin, G. L., Zurek, L., & Bhandari, A. (2009). Occurrence of ciprofloxacin-, trimethoprimesulfamethoxazole-, and vancomycin-resistant bacteria in a municipal wastewater treatment plant. Water Environment Research, 81, 82–90.

    Article  CAS  Google Scholar 

  • Neilan, B. A., Jacobs, D., Del Dot, T., Blackall, L. L., Hawkins, P. R., Cox, P. T., & Goodman, A. E. (1997). rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. International Journal of Systematic Bacteriology, 47, 693–697.

    Article  CAS  Google Scholar 

  • Ozdemir, G., Ozturk, T., Ceyhan, N., Isler, R., & Cosar, T. (2003). Heavy metal biosorption by biomass of Ochrobactrum anthropi producing exopolysaccharide in activated sludge. Bioresource Technology, 90, 71–74.

    Article  CAS  Google Scholar 

  • Palmisano, A. C., & Barlaz, M. A. (1996). Microbiology of solid waste. Boca Raton: CRC Press.

    Google Scholar 

  • Paterson, D. L., & Bonomo, R. A. (2005). Extended-Spectrum β-Lactamases: a clinical update. Clinical Microbiology Reviews, 18, 657–686.

    Article  CAS  Google Scholar 

  • Rebollido, R., Martínez, J., Aguilera, Y., Melchor, K., Koerner, I., & Stegmann, R. (2008). Microbial populations during composting process of organic fraction of municipal solid waste. Applied Ecology and Environmental Research, 6, 61–67.

    Article  Google Scholar 

  • Rigueiro-Rodríguez, A., Mosquera-Losada, M. R., & Ferreiro-Domínguez, N. (2012). Pasture and soil zinc evolution in forest and agriculture soils of Northwest Spain three years after fertilisation with sewage sludge. Agriculture, Ecosystems & Environment, 150, 111–120.

    Article  Google Scholar 

  • Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: A laboratory manual (2nd ed.). Cold Spring Harbor: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Silbergeld, E. K., Graham, J., & Price, L. B. (2008). Industrial food animal production, antimicrobial resistance, and human health. Annual Review of Public Health, 29, 151–169.

    Article  Google Scholar 

  • Soda, S., Otsuki, H., Inoue, D., Tsutsui, H., Sei, K., & Ike, M. (2008). Transfer of antibiotic multiresistant plasmid RP4 from Escherichia coli to activated sludge bacteria. Journal of Bioscience and Bioengineering, 106, 292–296.

    Article  CAS  Google Scholar 

  • United States Environmental Protection Agency (USEPA) (1995). Process design manual: Land application of sewage sludge and domestic septage. Cincinnati-Ohio. EPA/625/ R-95/001.

  • Vela-Cano, M., Castellano-Hinojosa, A., Vivas, A. F., & Toledo, M. V. M. (2014). Effect of heavy metals on the growth of bacteria isolated from sewage sludge compost tea. Advances in Microbiology, 4, 644–655.

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank Prof. Marli Fatima Fiore (Centro de Energia Nuclear, Universidade de São Paulo) for collaboration in the molecular analyses, Msc. Daniel Derrossi Meyer for comments on the manuscript and the Brazilian government by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for financial support.

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Correspondence to Sueli Van Der Sand.

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Heck, K., De Marco, É.G., Duarte, M.W. et al. Pattern of multiresistant to antimicrobials and heavy metal tolerance in bacteria isolated from sewage sludge samples from a composting process at a recycling plant in southern Brazil. Environ Monit Assess 187, 328 (2015). https://doi.org/10.1007/s10661-015-4575-6

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