Skip to main content

Advertisement

SpringerLink
Log in

Marine fungi isolated from Chilean fjord sediments can degrade oxytetracycline

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Salmon farming is the main economic activity in the fjords area of Southern Chile. This activity requires the use of antibiotics, such as oxytetracycline, for the control and prevention of diseases, which have a negative impact on the environment. We analyzed the abilities of endemic marine fungi to biodegrade oxytetracycline, an antibiotic used extensively in fish farming. We isolated marine fungi strains from sediment samples obtained from an area of fish farming activity. The five isolated strains showed an activity on oxytetracycline and were identified as Trichoderma harzianum, Trichoderma deliquescens, Penicillium crustosum, Rhodotorula mucilaginosa, and Talaromyces atroroseus by a scanning electron microscopy and characterized by molecular techniques. Results showed significant degradation in the concentration of oxytetracycline at the first 2 days of treatment for all strains analyzed. At 21 days of treatment, the concentration of oxytetracycline was decreased 92 % by T. harzianum, 85 % by T. deliquescens, 83 % by P. crustosum, 73 % by R. mucilaginosa, and 72 % by T. atroroseus, all of which were significantly higher than the controls. Given these results, we propose that fungal strains isolated from marine sediments may be useful tools for biodegradation of antibiotics, such as oxytetracycline, in the salmon industry.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahumada-Rudolph, R., Cajas-Madriaga, D., Rudolph, A., Reinoso, R., Torres, C., Silva, M., & Becerra, J. (2014). Variation of sterols and fatty acids as an adaptive response to changes in temperature, salinity and pH of a marine fungus Epicoccum nigrum isolated from the Patagonian fjords. Revista de Biología Marina y Oceanografía, 49, 293–305.

    Article  Google Scholar 

  • Andrade, V. da C., Zampieri, B. del B., Ballesteros, E. R., Pinto A. B., de Oliveira, A. J. (2015) Densities and antimicrobial resistance of Escherichia coli isolated from marine waters and beach sands. Environmental Monitoring and Assessment, 187:342 doi: 10.1007/s10661-015-4573-8.

  • Alcock, R. E., Sweetman, A., & Jones, K. C. (1999). Assessment of organic contaminant fate in wastewater treatment plants I. Selected compounds and physiochemical properties. Chemosphere, 38, 2247–2262.

    Article  CAS  Google Scholar 

  • Baćmaga, M., Kucharski, J., & Wyszkowska, J. (2015). Microbial and enzymatic activity of soil contaminated with azoxystrobin. Environmental Monitoring and Assessment. doi:10.1007/s10661-015-4827-5.

    Google Scholar 

  • Bannister, R. J., Valdemarsen, T., Hansen, P. K., Holmer, M., & Ervik, A. (2014). Changes in benthic sediment conditions under an Atlantic salmon farm at a deep, well-flushed coastal site. Aquaculture Environment Interactions, 5, 29–47.

    Article  Google Scholar 

  • Baldrian, P. (2003). Interactions of heavy metals with white-rot fungi. Enzyme and Microbial Technology, 32, 78–91.

    Article  CAS  Google Scholar 

  • Bugni, T. S., & Ireland, C. M. (2004). Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Natural Product Reports, 21, 143–163.

    Article  CAS  Google Scholar 

  • Burridge, L., Weis, J. S., Cabello, F., Pizarro, J., & Bostick, K. (2010). Chemical use in salmon aquaculture: a review of current practices and possible environmental effects. Aquaculture, 306, 7–23.

    Article  CAS  Google Scholar 

  • Buschmann, A. H., Riquelme, V. A., Hernández-González, M. C., Varela, D., Jiménez, J. E., Henríquez, L. A., Vergara, P. A., Guíñez, R., & Filún, L. (2006). A review of the impacts of salmon farming on marine coastal ecosystems in the Southeast Pacific. ICES Journal of Marine Science, 63, 1338–1345.

    Article  Google Scholar 

  • Buschmann, A. H., Tomova, A., López, A., Maldonado, M. A., & Henríquez, L. A. (2012). Salmon aquaculture and antimicrobial resistance in the marine environment. PloS One, 7, e42724. doi:10.1371/journal.pone.0042724.

    Article  CAS  Google Scholar 

  • Buschmann, A. H. & Muñoz J. L. P. 2016. Salmon faring. Reference module in Earth systems and environmental sciences. Amsterdam, Elsevier. doi: 10.1016/B978–0–12-409548-9.09580-4.

  • Cabello, F. C., Godfrey, H. P., Tomova, A., Ivanova, L., Dölz, H., Millanao, A., & Buschmann, A. H. (2013). Antimicrobial use in aquaculture re-examined: its relevance to antimicrobial resistance and to animal and human health. Environmental Microbiology, 15, 1917–1942.

    Article  Google Scholar 

  • Cabello, F. C. (2004). Antibióticos y acuicultura en Chile: consecuencias para la salud humana y animal. Revista Médica Chile, 132, 1001–1006.

    Article  CAS  Google Scholar 

  • Cabello, F. C. (2006). Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environmental Microbiology, 8, 1137–1144.

    Article  CAS  Google Scholar 

  • Chen, G., Fan, J., Liu, R., Zeng, G., Chen, A., & Zou, Z. (2012). Removal of Cd(II), Cu(II) and Zn(II) from aqueous solutions by live Phanerochaete chrysosporium. Environmental Technology, 33, 2653–2659.

    Article  CAS  Google Scholar 

  • Costa-Pierce, B. A. (2010). Sustainable ecological aquaculture systems: the need for a new social contract for aquaculture development. Marine Technology Society, 44, 88–112.

    Article  Google Scholar 

  • Coyne, R., Smith, P., & Moriarty, C. (2001). The fate of oxytetracycline in the marine environment of a salmon cage farm. Marine Environment and Health Series, 3, 1–24.

    Google Scholar 

  • Drummond, A. J., Ashton, B., Burton, S., Cheung, M., Cooper, A., Heled, J., Moir, R., Stones-Havas, S., Sturrock, S., & Thierer, T. (2011) Geneious v5.4. Biomatters, Auckland. http://www.geneious.com/. Accessed 30 Oct 2015

  • Fester, T. (2012). Arbuscular mycorrhizal fungi in a wetland constructed for benzene-, methyl tert-butyl ether- and ammonia-contaminated groundwater bioremediation. Microbial Biotechnology, 6, 80–84.

    Article  Google Scholar 

  • Fortt, Z. A., Cabello, F., & Buschmann, A. (2007). Residuos de tetraciclina y quinolonas en peces silvestres en una zona costera donde se desarrolla la acuicultura del salmón en Chile. Revista Chilena de Infectología, 24, 14–18.

    Article  Google Scholar 

  • Gadd, G. M. (2007). Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycological Research, 111, 3–49.

    Article  CAS  Google Scholar 

  • Guzmán-Dávalos, L., & Álvarez-Barajas, I. (2014). Hongos y líquenes como bioindicadores y micorremediacion. In C. A. González, A. Vallarino, J. C. Pérez, & A. M. Low (Eds.), Bioindicadores: guardianes de nuestro futuro ambiental (pp. 579–603). México: El Colegio de la Frontera Sur e Instituto Nacional de Ecología y Cambio Climático.

    Google Scholar 

  • Halling-Sørensen, B. (2001). Inhibition of aerobic growth and nitrification of bacteria in sewage sludge by antibacterial agents. Archives of Environmental Contamination and Toxicology, 40, 451–460.

    Article  Google Scholar 

  • Hargrave, B. T., Holmer, M., & Newcombe, C. P. (2008) Towards a classification of organic enrichment in marine sediments based on biogeochemical indicators. Marine Pollution Bulletin, 56:810–824

  • Harms, H., Schlosser, D., & Wick, L. Y. (2011). Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nature Reviews Microbiology, 9, 177–191.

    Article  CAS  Google Scholar 

  • Hektoen, H., Berge, J. A., Hormazábal, V., & Yndestad, M. (1995). Persistence of antibacterial agents in marine sediments. Aquaculture, 133, 175–184.

    Article  CAS  Google Scholar 

  • Heuer, O. E., Kruse, H., Grave, K., Collignon, P., & Karunasagar, I. (2009). Human health consequences of use of antimicrobial agents in aquaculture. Clinical Infectious Diseases, 49, 1248–1253.

    Article  Google Scholar 

  • Holmer, M. (2010). Environmental issues of fish farming in offshore waters: perspectives, concerns and research needs. Aquaculture Environment Interactions, 1, 57–70.

    Article  Google Scholar 

  • Instituto Nacional de Estadísticas (INE). 2014. Compendio estadístico 2014. http://www.ine.cl/canales/menu/publicaciones/calendario_de_publicaciones/pdf/compendio_2014.pdf. Accessed 27 Dec 2015.

  • Keeley, N. B., Cromey, C. J., Goodwin, E. O., Gibbs, M. T., & Macleod, C. M. (2013). Predictive depositional modelling (DEPO-MOD) of the interactive effect of current flow and resuspension on ecological impacts beneath salmon farms. Aquaculture Environment Interactions, 3, 275–291.

    Article  Google Scholar 

  • Krause, E., Wichels, A., Giménez, L., & Gerdts, G. (2013). Marine fungi may benefit from ocean acidification. Aquatic Microbial Ecology, 69, 59–67.

    Article  Google Scholar 

  • Kutti, T., Hansen, K. P., Ervik, A., Høisæter, T., & Johannessen, P. (2007). Effects of organic effluents from a salmon farm on a fjord system. II. Temporal and spatial patterns in infauna community composition. Aquaculture, 262, 355–366.

    Article  CAS  Google Scholar 

  • Kümmerer, K. (2009). Antibiotics in the aquatic—a review—part I. Chemosphere, 75, 417–434.

    Article  Google Scholar 

  • Manohar, C. S., & Raghukumar, C. (2013). Fungal diversity from various marine habitats deduced through culture-independent studies. FEMS Microbiology Letters, 341, 69–78.

    Article  CAS  Google Scholar 

  • Marshall, B. M., & Levy, S. B. (2011). Food animals and antimicrobials: impacts on human health. Clinical Microbiology Reviews, 24, 718–733.

    Article  CAS  Google Scholar 

  • Millanao, B. A., Barrientos, H. M., Gomez, C. C., Tomova, A., & Buschmann, A. (2011). Uso inadecuado y excesivo de antibióticos: salud pública y salmonicultura en Chile. Revista Médica Chile, 139, 107–118.

    Article  Google Scholar 

  • Miranda, C., & Zemelman, R. (2002). Bacterial resistance to oxytetracycline in Chilean salmon farming. Aquaculture, 212, 31–47.

    Article  CAS  Google Scholar 

  • Nnenna, F. P., Lekiah, P., & Obemeata, O. (2011). Degradation of antibiotics by bacteria and fungi from the aquatic environment. Toxicology and Environmental Health Sciences, 3, 275–285.

    CAS  Google Scholar 

  • Rhodes, G., Huys, G., Swings, J., McGann, P., & Hiney, M. (2000). Distribution of oxytetracycline resistance plasmids between aeromonads in hospital and aquaculture environments: implication of Tn1721 in dissemination of the tetracycline resistance determinant Tet A. Applied and Environmental Microbiology, 66, 3883–3890.

    Article  CAS  Google Scholar 

  • Rudolph, A., Medina, P., Urrutia, C., & Ahumada, R. (2009). Ecotoxicological sediment evaluations in marine aquaculture areas of Chile. Environmental Monitoring and Assessment, 155, 419–429.

    Article  CAS  Google Scholar 

  • Rudolph, A., Medina, P., Ahumada, R., & Novoa, V. (2011). Ecotoxicological quality of sediments in fiords in Southern Chile (44–46.5° LS). Revista de Biología Marina y Oceanografía, 46, 79–84.

    Article  Google Scholar 

  • Samuelsen, O. B. (1989). Degradation of oxytetracycline in seawater at two different temperatures and light intensities, and the persistence of oxytetracycline in the sediment from a fish farm. Aquaculture, 83, 7–16.

    Article  CAS  Google Scholar 

  • Sarmah, A. K., Meyer, M. T., & Boxall, A. B. A. (2006). A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere, 65, 725–759.

    Article  CAS  Google Scholar 

  • Schmitt, H., Haapakangas, H., & Van Beelen, P. (2005). Effects of antibiotics on soil microorganisms; time and nutrients influence pollution-induced community tolerance. Soil Biology and Biochemistry, 37, 1882–1892.

    Article  CAS  Google Scholar 

  • Servicio Nacional de Pesca y Acuicultura (SERNAPESCA) (2014) Informe sobre uso de antimicrobianos en la salmonicultura nacional 2013. Unidad de salud animal. Ministerio de Economía, Fomento y Turismo. Valparaíso, Chile. 19 pp.

  • Silva, N., & Guzmán, D. (2006). Condiciones oceanográficas físicas y químicas, entre boca del Guafo y fiordo Aysén (Crucero Cimar 7 Fiordos). Ciencia Tecnología del Mar, 29, 25–44.

    Google Scholar 

  • Sowmya, H. V., Ramalingappa, B., Nayanashree, G., Thippeswamy, B., & Krishnappa, M. (2014). Degradation of polyethylene by Trichoderma harzianum—SEM, FTIR, and NMR analyses. Environmental Monitoring and Assessment, 186(10), 6577–6586.

    Article  CAS  Google Scholar 

  • Sørum, H. (2006). Antimicrobial drug resistance in fish pathogens. In F. M. Aarestrup (Ed.), Antimicrobial resistance in bacteria of animal origin (pp. 213–238). Washington: ASM Press.

    Google Scholar 

  • Subsecretaría de Pesca y Acuicultura (SUBPESCA) (2014) Informe sectorial de pesca y acuicultura. Valparaíso, Chile p 19.

  • Subsecretaría de Pesca y Acuicultura (SUBPESCA) (2015) Subsecretaría de Pesca y Acuicultura. Valparaíso, Chile http://www.subpesca.cl/prensa/601/w3-article-88821.html. Accessed 27 Dec 2015.

  • Tedersoo, L., Suvi, T., Jairus, T., & Kõljalg, H. (2009). Forest microsite effects on community composition of ectomycorrhizal fungi on seedlings of Picea abies and Betula pendula. Environmental Microbiology, 10, 1189–1201.

    Article  Google Scholar 

  • Valdemarsen, T., Kristensen, E., & Holmer, M. (2009). Metabolic threshold and sulfide-buffering in diffusion controlled marine sediments impacted by continuous organic enrichment. Biogeochemistry, 95, 335–353.

    Article  CAS  Google Scholar 

  • Vidaver, A. (2002). Uses of antimicrobials in plant agriculture. Clinical Infectious Diseases, 34, 107–110.

    Article  Google Scholar 

  • Williams, A. J., Deck, J., Freeman, J. P., Chiarelli, M. P., Adjej, M. D., Heinze, T. M., & Sutherland, J. D. (2007). Biotransformation of flumequine by the fungus Cunninghamella elegans. Chemosphere, 67, 240–243.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank financial support of the “CONICYT + PAI (Comisión nacional de Investigación Científica y Tecnológica + Programa de Atracción e Inserción) Concurso Nacional Tesis de Doctorado en la Industria, Convocatoria 2013 + Folio 783110001” and the project partner Blumar Salmones S.A and Project FONDECYT 1151028. Special thanks to Sr. Nicos Nicolaides for his help in presenting the project.

Author information

Authors and Affiliations

  1. Departamento de Geografía, Facultad de Arquitectura, Urbanismo y Geografía, Universidad de Concepción, Víctor Lamas 1290, PO Box 160-C, Concepción, Chile

    R. Ahumada-Rudolph & V. Novoa

  2. Estudiantes de Doctorado en Ciencias Ambientales, Facultad de Ciencias Ambientales, Universidad de Concepción, Víctor Lamas 1290, PO Box 160-C, Concepción, Chile

    R. Ahumada-Rudolph & V. Novoa

  3. Laboratorio de Química de Productos Naturales, Departamento de Botánica, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Víctor Lamas 1290, PO Box 160-C, Concepción, Chile

    R. Ahumada-Rudolph & J. Becerra

  4. Departamento de Estadística, Facultad de Ciencias Físicas y Matemáticas, Universidad de Concepción, Víctor Lamas 1290, PO Box 160-C, Concepción, Chile

    K. Sáez

  5. Laboratorio de Microbiología Básica y Bioremediación, Facultad de Ciencias Biológicas, Universidad de Concepción, Víctor Lamas 1290, PO Box 160-C, Concepción, Chile

    M. Martínez

  6. Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Alonso de Ribera 2850, PO Box 297, Concepción, Chile

    A. Rudolph

  7. Laboratorio de Genómica & Biodiversidad (LGB), Departamento de Ciencias Naturales, Universidad del Bío-Bío, Dieciocho de Septiembre 580, PO Box 447, Chillán, Chile

    C. Torres-Diaz

Authors
  1. R. Ahumada-Rudolph
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. Novoa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Sáez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Rudolph
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Torres-Diaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. Becerra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Ahumada-Rudolph.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahumada-Rudolph, R., Novoa, V., Sáez, K. et al. Marine fungi isolated from Chilean fjord sediments can degrade oxytetracycline. Environ Monit Assess 188, 468 (2016). https://doi.org/10.1007/s10661-016-5475-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-016-5475-0

Keywords

Search

Navigation