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Proteolytic Enzyme Activity and Its Relationship with Physicochemical and Microbiological Indicators in Freshwater Ecosystems of Western Cuba

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Abstract

The enzymatic reactions of microbial communities are rapid and adequate to changes in the composition of organic matter and environmental factors; therefore, they can be used as descriptors of biological responses in freshwater systems. The objective of this work was to determine the proteolytic enzymatic activity in the Almendares and San Juan rivers (western Cuba) and their relationship with physicochemical and microbiological indicators. The Almendares River (Havana, Cuba) presented water quality index between very poor and unusable for consumption, which makes impossible for recreational uses. In contrast, the waters of the San Juan River (Artemisa, Cuba) are classified as excellent and good in most of the sampling stations during the study period. The greatest proteolytic activities were detected in the San Juan River compared to the Almendares River, which indicates that in more contaminated ecosystems, the proteolytic enzyme activity decreases compared to another less impacted system. In addition, the annual variation in the proteolytic activity of both rivers was evidenced. In the San Juan River, a correlation was observed among proteolytic activity, the concentration of proteolytic bacteria and the physicochemical indicators of water quality, suggesting that proteolytic activity is related to naturally occurring contaminants. In contrast, in the Almendares River, this relationship was not observed, which suggests that the proteolytic activity is not directly affected by the indicators measured in this study.

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References

  • Admiraal, W., & Tubbing, G. M. J. (1991). Extracellular enzyme activity associated with suspended matter in the River Rhine. Freshwater Biology, 26, 507–517. https://doi.org/10.1111/j.1365-2427.1991.tb01415.x.

    Article  CAS  Google Scholar 

  • AFNOR (2009). Qualité de l’eau. Analyses biochimiques et biologiques – analyses microbiologiques. Norme NF EN ISO 16061. Paris: Association Française de Normalisation.

  • Afroz, R., & Rahman, A. (2017). Health impact of river water pollution in Malaysia. International Journal of Advanced and Applied Science, 4, 78–85. https://doi.org/10.21833/ijaas.2017.05.014.

    Article  Google Scholar 

  • Alquicira, L. (2003). Determinación de la especificidad de proteasas fúngicas en la hidrólisis de proteína. México D. F. Tesis en opción al grado de Especialista en Biotecnología, México DF.

  • APHA. (2012). Standard methods for the analysis of water and wastewater. 20nd ed. edited by E. W. Rice, R. B. Baird, A. D.Eaton and L. S. Clesceri. American Public Health Association (APHA), American Water Works Association (AWWA) and Water Environment Federation (WEF), Washington, D.C., EUA.

  • Arpajón, Y., Romeu, B., Rodríguez, A., Heydrich, M., Rojas, M. and Lugo, D. (2011). Impacto de los nutrientes inorgánicos sobre la comunidad bacteriana en el río Almendares (Cuba) Hig. Sanid. Ambient., 11, 731-738. ISSN: 1579-1734. Depósito legal GR-22/2002.

  • Arpajón, Y., Larrea, J. A., Rojas, N., Heydrich, M. and Lugo, D. (2012). Efectividad de los programas de preservación de ecosistemas dulceacuícolas de Sierra del Rosario, Pinar del Río. Memorias Convención Internacional de Salud Pública. Cuba Salud 2012. La Habana 3-7 de diciembre de 2012. ISBN: 978-959-212-811-8.

  • Cunha, A., Almeida, A., Coelho, F. J. R. C., Gomes, N. C. M., Oliveira, V. and Santos, A. L. (2010). Bacterial extracellular enzymatic activity in globally changing aquatic ecosystems. Current research, technology and education topics in applied microbiology and microbial Biotecnology, A. Mñendez-Vilas (Ed.) 124-135.

  • Díaz, O., Olivares, S., Gelen, A., D’Alessandro, K., Lima-Carzola, L., García, D., Casanova, A. O., García, C., & Manduca, M. (2019). Estudios de contaminación ambiental en La Habana mediante técnicas nucleares conexas. Nucleus., 66, 58–65 ISSN 0864-084X.

    Google Scholar 

  • Franco-Anaya, P., López-Gutiérrez, L., & Orozco-Ugarriza, M. E. (2016). Calidad microbiológica del agua envasada comercializada en el área turística de Cartagena, Colombia. Agronomia Colombiana, 34(1), 1319–1321. https://doi.org/10.15446/agron.colomb.v34n1supl.58432.

    Article  Google Scholar 

  • Gandolfi, C.B., Peralta R.M., (2000). Production of extracellular protease by Aspergillus tamarii. Journal of Basic Microbiology 40(2), 75-81

  • Giraldo, L. C., Palacio, C. A., & Aguirre, N. J. (2014). Temporal variation of the extracelular enzimatic activity (EEA): case of study: Aburra- Medellín River, in the Valle de Aburra in Medellín, Antioquia, Colombia. International Journal of Enviromental Protection., 4(5), 58–67. https://doi.org/10.5963/IJEP.

    Article  Google Scholar 

  • Halliday, S. J., Skeffington, A., Bowes, M. J., Gozzard, E., Newman, J. R., Loewenthal, M., Palmer-Felgate, E. J., Jarvie, H. P., & Wade, A. J. (2014). The water quality of the river Enborne, UK: observations from high-frequency monitoring in a rural, Lowland River System. Water., 6, 150–180. https://doi.org/10.3390/w6010150.

    Article  CAS  Google Scholar 

  • Huang, D., Xu, J., Zeng, G., Lai, C., Yuan, X., Luo, X., Wang, C., Xu, P., & Huang, C. (2015). Influence of exogenous lead pollution on enzyme activities and organic matter degradation in the surface of river sediment. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-015-4375-0.

  • Ilie, M., Marinescu, F., Ghita, G., Anghel, A. M., Deák, G., & Raischi, M. (2017). Assessment of nutrients- chlorophyll-a relationship in the lower Danube river. Int’l Journal of Advances in Chemical Engineering, & Biological Sciences, 4(1), 15–20. https://doi.org/10.15242/IJACEBS.C0117029.

    Article  Google Scholar 

  • INSMET (Instituto Nacional de Meteorología). www.met.inf.cu. Consultado: 15-2-2018.

  • Jaramillo, M. T., Aguirre, N. J., & Galvis, J. H. (2016). Using extracelularenzime activity as pollutant indicator: a field estudy in Chinchiná River, Caldas- Colombia. International Journal of Enviromental Protection., 6(1), 47–59. https://doi.org/10.5963/IJEP0601004.

    Article  Google Scholar 

  • Jeffrey, S. W., & Humphrey, G. F. (1975). New spectrophotometric - equations for determining chIorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen, 167(2), 191–194. https://doi.org/10.1016/S0015-3796(17)30778-3.

    Article  CAS  Google Scholar 

  • Kalwasińska, A., & Brzezinsk, M. S. (2013). Extracellular enzymatic activities in subsurface water of eutrophic Lake Chełmżyńskie, Poland. Journal of Freshwater Ecology, 28(4), 517–527. https://doi.org/10.1080/02705060.2013.793220.

    Article  CAS  Google Scholar 

  • Koffi, N., García-Armisen, T., Anzil, A., Brion, N., & Servais, P. (2014). Impact of wastewater release on the faecal contamination of a small urban river: the Zenne River in Brussels (Belgium). Water, Air, and Soil Pollution, 225(2043), 1–12. https://doi.org/10.1007/s11270-014-2043-5.

    Article  CAS  Google Scholar 

  • Kutvirt, S. (2013). The microbial link in ecosystem processing in the east fork of the Jemez river: extracellular enzyme response to habitat, seasonal fluctuations, and wildfire disturbance. 1-31. http://digitalrepository.unm.edu/wr_sp/13

  • Larrea, J. A., Rojas, M., Heydrich, M., Romeu, B., Rojas, N., & Lugo, D. (2009). Evaluación de la calidad microbiológica de las aguas del Complejo Turístico “Las Terrazas”, Pinar del Río (Cuba). Hig Sanid Ambient, 9, 492–504.

    Google Scholar 

  • Larrea, J. A., Rojas, M. M., Bacchetti, T., Lugo, D., Heydrich, M., Estéve, A., & Boltes, K. (2014). Influencia de la contaminación química y fecal sobre la estructura de las comunidades bacterianas del Río Almendares, La Habana, Cuba. Revista Investigación y Saberes., 3(3), 1–11.

    Google Scholar 

  • Larrea, J. A., Rojas, M. M., García, I., Romeu, B., Bacchetti, T., Gillis, A., Boltes, A. K., Heydrich, M., Lugo, D., & Mahillon, J. (2018). Diversity and enzymatic potentialities of Bacillus sp. strains isolated from a polluted freshwater ecosystem in Cuba. World J. Microb. Biot., 34(28), 1–11. https://doi.org/10.1007/s11274-018-2411-1.

    Article  CAS  Google Scholar 

  • Li, Y., Wu, C., Zhou, M., Wang, E. T., Zhang, Z., Liu, W., Ning, J., & Xie, Z. (2017). Diversity of cultivable protease-producing Bacteria in Laizhou Bay sediments, Bohai Sea, China. Frontiers in Microbiology, 8(405), 1–10. https://doi.org/10.3389/fmicb.2017.00405.

    Article  Google Scholar 

  • Li, Y., Sun, L.-L., Sun, Y.-Y., Cha, Q.-Q., Li, C.-Y., Zhao, D.-L., Song, X.-Y., Wang, M., McMinn, A., Chen, X.-L., Zhang, Y.-Z., & Qin, Q.-L. (2019). Extracellular enzyme activity and its implications for organic matter cycling in northern Chinese marginal seas. Frontiers in Microbiology, 10, 2137. https://doi.org/10.3389/fmicb.2019.02137.

    Article  Google Scholar 

  • Malaver, N., Rodríguez, M., Montero, R., Aguilar, V. H., & Salas, M. (2014). Cambios espaciales y temporales en las características fisicoquímicas y microbiológícas del agua de la laguna de Tacarigua, Estado Miranda, Venezuela. Acta Biologica Venezuelica, 34(1), 117–151.

    Google Scholar 

  • Martínez, A., Cruz, M., Veranes, O., Carballo, M. E., Salgado, I., Olivares, S., Lima, L., & Rodríguez, D. K. (2010). Antibiotic and metals resistance in bacteria isolates from Almendares River. Revista CENIC Ciencias Biológicas., 41, 1–10.

    Google Scholar 

  • Mullen, L., Malcolm X Shabazz High School Aquatic Biogeochemistry Team, Boerrigter, K., Ferriero, N., Rosalsky, J., Barrett, A. B., Murray, P. J., & Steen, A. D. (2018). Potential activities of freshwater exo-and endo-acting extracellular peptidases in East Tennessee and the Pocono Mountains. Frontiers in Microbiology, 9, 368. https://doi.org/10.3389/fmicb.2018.00368.

    Article  Google Scholar 

  • National Institute of Hydraulic Resources. (2010). Informe técnico Cuencas Hidrográficas de la Habana. Situación del saneamiento ambiental de la Habana, Cuba.

  • Nayar R. (2020). Assessment of water quality index and monitoring of pollutants by physico-chemical analysis in water bodies: a review. IJERT. 9 (01). ISSN: 2278-0181, ID: IJERTV9IS010046.

  • Pandey, A., Germano, S., Osaku, C. A., Rocha, N. S., & Soccol, C. R. (2003). Characterization and stability of proteases from Penicillium sp. produced by solid state fermentation. Enzyme and Microbial Technology, 32(2), 246–251. https://doi.org/10.1016/S0141-0229(02)00283-1.

    Article  Google Scholar 

  • Quiroz, S., Izquierdo-Kulich, E. and Menéndez, C. (2018). Impacto ambiental del vertimiento de aguas sobre la capacidad de autodepuración del río Portoviejo. Revista Centro Azúcar. 45 (1), 73. ISSN: 2223–486 https://www.researchgate.net/deref/http%3A%2F%2Fcentroazucar.uclv.edu.cu%2F.

  • Romeu, B.. Lugo, D.. and Rojas, N. M. (2011). Riesgo biológico asociado al empleo de las aguas contaminadas del río Almendares en la zona del Gran Parque Metropolitano de La Habana (Cuba). Hig. Sanid. Ambient. 11, 715-724. ISSN 1579-1734. Depósito legal GR-222/2002.

  • Romeu, B., Quintero, H., Larrea, J. A., Rojas, N. and Heydrich, M. (2015). Calidad química y microbiológica de las aguas del río San Juan, Artemisa (Cuba). Hig. Sanid. Ambient. 15 (4), 1367-1374. ISSN 1579-1734. Depósito legal GR-222/2002.

  • Roy, K., Chari, M. S., Gaur, S. R., & Thakur, A. (2014). Ecological dynamics and hydrobiological correlations in freshwater ponds – recent researches and application. International Journal Environmental Biology., 4(2), 112–118 ISSN: 2277-386X.

    Google Scholar 

  • Sabater, S., Guasch, H., Ricart, M., Romani, A., Vidal, G., & Klünder, C. (2016). Monitoring the effect of chemicals on biological communities. The biofilm as an interface. Anal. Bioanal., 378, 1425–1434. https://doi.org/10.1007/s00216-006-1051-8.

    Article  CAS  Google Scholar 

  • Samboni, N. E., Carvajal, Y., & Escobar, J. C. (2007). Revisión de parámetros físicoquímicos como indicadores de calidad y contaminación del agua. Revista de Ingienería e Investigación, 27(3), 172–181 ISN: 0120–5609.

    Google Scholar 

  • Schneider I. and Topalova Y. (2009). Structural and functional changes in river microbial communities after dairy wastewater discharge. Biotechnol Biotec. Eq. 23 (2), 1210–1216. https://doi.org/10.1080/13102818.2009.10817640.

  • Singh, R., Singh, T. and Pandey, A. (2019). Microbial enzymes—an overview. En: Advances in enzyme technology: a volume in biomass, biofuel, biochemicals. (R. S. Singh, R. R. Singhania, A. Pandey, Ch. Larroche, Ed.). Elsevier, Amsterdam, pp. 1–40. https://doi.org/10.1016/B978-0-444-64114-4.00001-7.

  • Sosa-Avalos, R., Gaxiola-Castro, G., Olivos-Ortiz, A., & Silva-Iñiguez, L. (2013). Nutrientes Inorgánicos y producción del fitoplancton en una laguna costera subtropical de México. Revista de Biología Marina y Oceanografía, 48(1), 143–154. https://doi.org/10.4067/S0718-19572013000100012.

    Article  Google Scholar 

  • StatSoft. (2007). STATISTICA (data analysis software system), version 8.0. from www. statsoft.com 10/03/2018.

  • Tanor, E. B., Ts’enoli, S., & George, M. J. (2014). Physico-chemical assessment of pollution in the Caledon River around Maseru city, Lesotho. European Chemical Bulletin, 3(8), 776–782. https://doi.org/10.17628/ecb.2014.3.776-782.

    Article  CAS  Google Scholar 

  • Tiquia, S. M. (2011). Extracellular hydrolytic enzyme activities of the heterotrophic microbial communities of the Rouge River: an approach to evaluate ecosystem response to urbanization. Microbial Ecology, 62(3), 679–689. https://doi.org/10.1007/s00248-011-9871-2.

    Article  CAS  Google Scholar 

  • Tirkey, P., Bhattacharya, T., & Chakraborty, S. (2013). Water quality indices- important tools for water quality assessment: a review. International Journal of Advances in Chemestry, 1(1).

  • Traving, S. J., Bentzon-Tilia, M., Knudsen-Leerbeck, H., Mantikci, M., Hansen, J. L. S., Stedmon, C. A., Sørensen, H., Markager, S., & Riemann, L. (2016). Coupling bacterioplankton populations and environment to community function in coastal temperate waters. Frontiers in Microbiology, 7(1533), 1–13. https://doi.org/10.3389/fmicb.2016.01533.

    Article  Google Scholar 

  • Traving, S. J., Rowe, O., Jakobsen, N. M., Sørensen, H., Dinasque, J., Stedmon, C. A., Andersson, A. A., & Riemann, L. (2017). The effect of increased loads of dissolved organic matter on estuarine microbial community composition and function. Frontiers in Microbiology, 8(351), 1–15. https://doi.org/10.3389/fmicb.2017.00351.

    Article  Google Scholar 

  • Tsuboi, S., Yamamura, S., Imai, A., Satou, T., & Iwasaki, K. (2014). Linking temporal changes in bacterial community structures with the detection and phylogenetic analysis of neutral metalloprotease genes in the sediments of a hypereutrophic lake. Microbes and Environments, 29(3), 314–321. https://doi.org/10.1264/jsme2.ME14064.

    Article  Google Scholar 

  • Wang, Z., Wang, Z., Chen, C., & Wu, Q. (2017). Abundance of microorganisms and enzyme activity in the rapid-pool-benchland systems in natural Douliu River of China. Journal of Earth Sciences and Environmental Studies., 4(6), 749–762. https://doi.org/10.7287/peerj.preprints.2712v2.

    Article  Google Scholar 

  • Ward, O., Rao, M. B., & Kulkarni, A. (2009). Proteases, Production. Encyclopedia of Microbiology, 495–511. https://doi.org/10.1016/B978-012373944-5.00172-3.

  • Wei, C., Malfatti, F., Azam, F., Obayashi, Y., & Suzuki, S. (2010). The effect of zinc exposure on the bacteria abundance and proteolytic activity in seawater. Interdisciplinary Studies on Environmental Chemistry — Biological Responses to Contaminants., 3, 57–63.

    Google Scholar 

  • WHO. (2018). Guidelines for drinking-water quality: fourth edition incorporating first addendum. Ginebra: Licencia: CC BY-NC-SA 3.0 IGO. pp. 636 ISBN 978–92-4- 354995-8.

  • Yisa, J., & Jimoh, T. (2010). Analytical studies on water quality index of river Landzu. American Journal of Applied Sciences, 7(4), 453–458. https://doi.org/10.3844/ajassp.2010.453.458.

    Article  CAS  Google Scholar 

  • Young, R. G. (2008). Organic matter breakdown and ecosystem metabolism: functional indicators for assessing river ecosystem health. Journal of the North American Benthological Society, 27(3), 605–625. https://doi.org/10.1899/07-121.1.

    Article  Google Scholar 

  • Zhang, X. Y., Han, X. X., Chen, X. L., Dang, H. Y., Xie, B. B., Qin, Q. L., Shi, M., Zhou, B. C., & Zhang, Y. Z. (2015). Diversity of cultivable protease-producing bacteria in sediments of Jiaozhou Bay, China. Frontiers in Microbiology, 6(1021), 1–9. https://doi.org/10.3389/fmicb.2015.01021.

    Article  Google Scholar 

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  1. Department of Microbiology and Virology, Biology Faculty, Havana University, 25 No. 455 between J e I, Vedado, Havana, Cuba

    Katherin Izquierdo Fiallo, Jeny Adina Larrea Murrell, Daysi Lugo Moya & Marcia M. Rojas Badía

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  1. Katherin Izquierdo Fiallo
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Distribution of the isolated proteolytic bacteria in the Almendares River (February 2016–June 2017) according to their morphological characteristics (PNG 169 kb)

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Distribution of the isolated proteolytic bacteria in the San Juan River (February 2016–June 2017) according to their morphological characteristics (PNG 216 kb)

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Fiallo, K.I., Murrell, J.A.L., Moya, D.L. et al. Proteolytic Enzyme Activity and Its Relationship with Physicochemical and Microbiological Indicators in Freshwater Ecosystems of Western Cuba. Water Air Soil Pollut 231, 540 (2020). https://doi.org/10.1007/s11270-020-04909-z

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