Screening of cyanotoxin producing genes in Ecuadorian freshwater systems
Triagem de genes produtores de cianotoxinas em sistemas de água doce do Equador
Isabel Ballesteros; Sara de la Cruz; Michelle Rojas; Génesis Salazar; Miguel Martínez-Fresneda; Pablo Castillejo
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Referências
Abeysiriwardena, N.M., Gascoigne, S.J.L., & Anandappa, A., 2018. Algal bloom expansion increases cyanotoxin risk in food. YJBM 91(2), 129-142. PMid:29955218.
Adamski, M., Wołowski, K., Kaminski, A., & Hindáková, A., 2020. Cyanotoxin cylindrospermopsin producers and the catalytic decomposition process: A review. Harmful Algae 98, 101894. PMid:33129452.
Aguilera, A., Gómez, E.B., Kaštovský, J., Echenique, R.O., & Salerno, G.L., 2018. The polyphasic analysis of two native Raphidiopsis isolates supports the unification of the genera
Antunes, J.T., Leão, P.N., & Vasconcelos, V.M., 2015. Cylindrospermopsis raciborskii: review of the distribution, phylogeography, and ecophysiology of a global invasive species. Front. Microbiol. 6, 473. PMid:26042108.
Ballesteros, I., Terán, P., Guamán-Burneo, C., González, N., Cruz, A., & Castillejo, P., 2021. DNA barcoding approach to characterize microalgae isolated from freshwater systems of Ecuador. Neotrop. Biodivers. 7(1), 170-183.
Belykh, O.I., Tikhonova, I.V., Kuzmin, A.V., Sorokovikova, E.G., Fedorova, G.A., Khanaev, I.V., Sherbakova, T.A., & Timoshkin, O.A., 2016. First detection of benthic cyanobacteria in Lake Baikal producing paralytic shellfish toxins. Toxicon 121, 36-40. PMid:27569199.
Bittencourt-Oliveira, M.C., Oliveira, M.C., & Pinto, E., 2011. Diversity of microcystin-producing genotypes in Brazilian strains of
Carmichael, W.W., & Boyer, G.L., 2016. Health impacts from cyanobacteria harmful algae blooms: Implications for the North American Great Lakes. Harmful Algae 54, 194-212. PMid:28073476.
Carmichael, W.W., 2001. Health effects of toxin-producing cyanobacteria: “The CyanoHABs”. Hum. Ecol. Risk Assess. Int J 7(5), 1393-1407.
Carrillo, K.C., Drouet, J.C., Rodríguez-Romero, A., Tovar-Sánchez, A., Ruiz-Gutiérrez, G., & Viguri Fuente, J.R., 2021. Spatial distribution and level of contamination of potentially toxic elements in sediments and soils of a biological reserve wetland, northern Amazon region of Ecuador. J. Environ. Manage. 289, 112495. PMid:33831761.
Christiansen, G., Fastner, J., Erhard, M., Börner, T., & Dittmann, E., 2003. Microcystin biosynthesis in Planktothrix: Genes, evolution, and manipulation. J. Bacteriol. 185(2), 564-572. PMid:12511503.
Cirés, S., Wörmer, L., Ballot, A., Agha, R., Wiedner, C., Velázquez, D., Casero, M.C., & Quesada, A., 2014. Phylogeography of cylindrospermopsin and paralytic shellfish toxin-producing Nostocales cyanobacteria from Mediterranean Europe (Spain). Appl. Environ. Microbiol. 80(4), 1359-1370. PMid:24334673.
Corbel, S., Mougin, C., & Bouaïcha, N., 2014. Cyanobacterial toxins: modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere 96, 1-15. PMid:24012139.
Cuesta, F., Llambí, L.D., Huggel, C., Drenkhan, F., Gosling, W.D., Muriel, P., Jaramillo, R., & Tovar, C., 2019. New land in the Neotropics: a review of biotic community, ecosystem, and landscape transformations in the face of climate and glacier change. Reg. Environ. Change 19(6), 1623-1642.
de la Cruz, A.A., Hiskia, A., Kaloudis, T., Chernoff, N., Hill, D., Antoniou, M.G., He, X., Loftin, K., O’Shea, K., Zhao, C., Pelaez, M., Han, C., Lynch, T.J., & Dionysiou, D.D., 2013. A review on cylindrospermopsin: the global occurrence, detection, toxicity and degradation of a potent cyanotoxin. Environ. Sci. Process. Impacts 15(11), 1979-2003. PMid:24056894.
Echeverría-Almeida, J., & Athens, J.S., 2016. Investigación subacuática en las lagunas de Yahuarcocha, San Pablo, Mojanda, provincia de Imbabura, Ecuador. Rev. Arqueol. Am. 34, 125-142.
Fan, Z.Y., Li, X.R., Mao, D.P., Zhu, G.F., Wang, S.Y., & Quan, Z.X., 2009. Could nested PCR be applicable for the study of microbial diversity? World J. Microbiol. Biotechnol. 25(8), 1447-1452.
Gaget, V., Humpage, A.R., Huang, Q., Monis, P., & Brookes, J.D., 2017. Benthic cyanobacteria: A source of cylindrospermopsin and microcystin in Australian drinking water reservoirs. Water Res. 124, 454-464. PMid:28787682.
Gobler, C.J., 2020. Climate Change and Harmful Algal Blooms: insights and perspective. Harmful Algae 91, 101731. PMid:32057341.
Gómez Durañona, G.D., 2005. Estudio de los sedimentos de la Laguna De Limoncocha (Provincia De Sucumbios-Ecuador) (Doctoral Thesis in Edaphology). Quito-Ecuador: Universidad Internacional SEK.
Haddad, S.P., Bobbitt, J.M., Taylor, R.B., Lovin, L.M., Conkle, J.L., Chambliss, C.K., & Brooks, B.W., 2019. Determination of microcystins, nodularin, anatoxin-a, cylindrospermopsin, and saxitoxin in water and fish tissue using isotope dilution liquid chromatography tandem mass spectrometry. J. Chromatogr. A 1599, 66-74. PMid:30961962.
Hawkins, P.R., Runnegar, M.T., Jackson, A.R., & Falconer, I.R., 1985. Severe hepatotoxicity caused by the tropical cyanobacterium (blue-green alga)
Hercog, K., Maisanaba, S., Filipič, M., Jos, Á., Cameán, A.M., & Žegura, B., 2017. Genotoxic potential of the binary mixture of cyanotoxins microcystin-LR and cylindrospermopsin. Chemosphere 189, 319-329. PMid:28942258.
Hoff-Risseti, C., Dörr, F.A., Schaker, P.D.C., Pinto, E., Werner, V.R., & Fiore, M.F., 2013. Cylindrospermopsin and Saxitoxin Synthetase Genes in
Howard, M.D.A., Nagoda, C., Kudela, R.M., Hayashi, K., Tatters, A., Caron, D.A., Busse, L., Brown, J., Sutula, M., & Stein, E.D., 2017. Microcystin prevalence throughout lentic waterbodies in coastal southern California. Toxins (Basel) 9(7), 1-21. PMid:28737685.
Huguet, A., Lanceleur, R., Quenault, H., Le Hégarat, L., & Fessard, V., 2019. Identification of key pathways involved in the toxic response of the cyanobacterial toxin cylindrospermopsin in human hepatic HepaRG cells. Toxicol. In Vitro 58, 69-77. PMid:30905859.
Kobayasi, H., & Mayama, S., 1982. Most pollution-tolerant diatoms of severly polluted rivers in the vicinity of Tokyo. Jpn. J. Physiol. 30, 188-196.
Kokociński, M., Gagala, I., Jasser, I., Karosiene, J., Kasperovičiene, J., Kobos, J., Koreiviene, J., Soininen, J., Szczurowska, A., Woszczyk, M., & Mankiewicz-Boczek, J., 2017. Distribution of invasive
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K., 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35(6), 1547-1549. PMid:29722887.
Kurmayer, R., Christiansen, G., Fastner, J., & Börner, T., 2004. Abundance of active and inactive microcystin genotypes in populations of the toxic cyanobacterium
Lajeunesse, A., Segura, P.A., Gélinas, M., Hudon, C., Thomas, K., Quilliam, M.A., & Gagnon, C., 2012. Detection and confirmation of saxitoxin analogues in freshwater benthic
Lei, L., Lei, M., Lu, Y., Peng, L., & Han, B.P., 2019. Development of real-time PCR for quantification of
Loftin, K.A., Graham, J.L., Hilborn, E.D., Lehmann, S.C., Meyer, M.T., Dietze, J.E., & Griffith, C.B., 2016. Cyanotoxins in inland lakes of the United States: Occurrence and potential recreational health risks in the EPA National Lakes Assessment 2007. Harmful Algae 56, 77-90. PMid:28073498.
Lorenzi, A.S., Cordeiro-Araújo, M.K., Chia, M.A., & Bittencourt-Oliveira, M.C., 2018. Cyanotoxin contamination of semiarid drinking water supply reservoirs. Environ. Earth Sci. 77(16), 595.
Mankiewicz-Boczek, J., Kokociński, M., Gagała, I., Pawełczyk, J., Jurczak, T., & Dziadek, J., 2012. Preliminary molecular identification of cylindrospermopsin-producing Cyanobacteria in two Polish lakes (Central Europe). FEMS Microbiol Lett. 326(2), 173-179. PMid:22092753.
Mantzouki, E., Lürling, M., Fastner, J., de Senerpont Domis, L., Wilk-Woźniak, E., Koreivienė, J., Seelen, L., Teurlincx, S., Verstijnen, Y., Krztoń, W., Walusiak, E., Karosienė, J., Kasperovičienė, J., Savadova, K., Vitonytė, I., Cillero-Castro, C., Budzyńska, A., Goldyn, R., Kozak, A., Rosińska, J., Szeląg-Wasielewska, E., Domek, P., Jakubowska-Krepska, N., Kwasizur, K., Messyasz, B., Pełechaty, A., Pełechaty, M., Kokocinski, M., García-Murcia, A., Real, M., Romans, E., Noguero-Ribes, J., Duque, D.P., Fernández-Morán, E., Karakaya, N., Häggqvist, K., Demir, N., Beklioğlu, M., Filiz, N., Levi, E.E., Iskin, U., Bezirci, G., Tavşanoğlu, Ü.N., Özhan, K., Gkelis, S., Panou, M., Fakioglu, Ö., Avagianos, C., Kaloudis, T., Çelik, K., Yilmaz, M., Marcé, R., Catalán, N., Bravo, A.G., Buck, M., Colom-Montero, W., Mustonen, K., Pierson, D., Yang, Y., Raposeiro, P.M., Gonçalves, V., Antoniou, M.G., Tsiarta, N., McCarthy, V., Perello, V.C., Feldmann, T., Laas, A., Panksep, K., Tuvikene, L., Gagala, I., Mankiewicz-Boczek, J., Yağcı, M.A., Çınar, Ş., Çapkın, K., Yağcı, A., Cesur, M., Bilgin, F., Bulut, C., Uysal, R., Obertegger, U., Boscaini, A., Flaim, G., Salmaso, N., Cerasino, L., Richardson, J., Visser, P.M., Verspagen, J.M.H., Karan, T., Soylu, E.N., Maraşlıoğlu, F., Napiórkowska-Krzebietke, A., Ochocka, A., Pasztaleniec, A., Antão-Geraldes, A.M., Vasconcelos, V., Morais, J., Vale, M., Köker, L., Akçaalan, R., Albay, M., Špoljarić Maronić, D., Stević, F., Žuna Pfeiffer, T., Fonvielle, J., Straile, D., Rothhaupt, K.O., Hansson, L.A., Urrutia-Cordero, P., Bláha, L., Geriš, R., Fránková, M., Koçer, M.A.T., Alp, M.T., Remec-Rekar, S., Elersek, T., Triantis, T., Zervou, S.K., Hiskia, A., Haande, S., Skjelbred, B., Madrecka, B., Nemova, H., Drastichova, I., Chomova, L., Edwards, C., Sevindik, T.O., Tunca, H., Önem, B., Aleksovski, B., Krstić, S., Vucelić, I.B., Nawrocka, L., Salmi, P., Machado-Vieira, D., de Oliveira, A.G., Delgado-Martín, J., García, D., Cereijo, J.L., Gomà, J., Trapote, M.C., Vegas-Vilarrúbia, T., Obrador, B., Grabowska, M., Karpowicz, M., Chmura, D., Úbeda, B., Gálvez, J.Á., Özen, A., Christoffersen, K.S., Warming, T.P., Kobos, J., Mazur-Marzec, H., Pérez-Martínez, C., Ramos-Rodríguez, E., Arvola, L., Alcaraz-Párraga, P., Toporowska, M., Pawlik-Skowronska, B., Niedźwiecki, M., Pęczuła, W., Leira, M., Hernández, A., Moreno-Ostos, E., Blanco, J.M., Rodríguez, V., Montes-Pérez, J.J., Palomino, R.L., Rodríguez-Pérez, E., Carballeira, R., Camacho, A., Picazo, A., Rochera, C., Santamans, A.C., Ferriol, C., Romo, S., Soria, J.M., Dunalska, J., Sieńska, J., Szymański, D., Kruk, M., Kostrzewska-Szlakowska, I., Jasser, I., Žutinić, P., Gligora Udovič, M., Plenković-Moraj, A., Frąk, M., Bańkowska-Sobczak, A., Wasilewicz, M., Özkan, K., Maliaka, V., Kangro, K., Grossart, H.P., Paerl, H.W., Carey, C.C., & Ibelings, B.W., 2018. Temperature effects explain continental scale distribution of cyanobacterial toxins. Toxins (Basel) 10(4), 1-24. PMid:29652856.
Massey, I.Y., & Yang, F., 2020. A Mini Review on Microcystins and Bacterial Degradation. Toxins (Basel) 12(4), 268. PMid:32326338.
McGinnis, S., & Madden, T. L., 2004. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res. 32, 0305-1048.
Meriluoto, J., Blaha, L., Bojadzija, G., Bormans, M., Brient, L., Codd, G.A., Drobac, D., Faassen, E.J., Fastner, J., Hiskia, A., Ibelings, B.W., Kaloudis, T., Kokocinski, M., Kurmayer, R., Pantelić, D., Quesada, A., Salmaso, N., Tokodi, N., Triantis, T.M., Visser, P.M., & Svirčev, Z.., 2017. Toxic cyanobacteria and cyanotoxins in European waters - recent progress achieved through the CYANOCOST action and challenges for further research. AIOL J. 8(1), 161-178.
Metcalf, J.S., Banack, S.A., Powell, J.T., Tymm, F.J.M., Murch, S.J., Brand, L.E., & Cox, P.A., 2018. Public health responses to toxic cyanobacterial blooms: perspectives from the 2016 Florida event. Water Policy 20(5), 919-932.
Mihali, T.K., Kellmann, R., Muenchhoff, J., Barrow, K.D., & Neilan, B.A., 2008. Characterization of the gene cluster responsible for cylindrospermopsin biosynthesis. Appl. Environ. Microbiol. 74(3), 716-722. PMid:18065631.
Mikalsen, B., Boison, G., Skulberg, O.M., Fastner, J., Davies, W., Gabrielsen, T.M., Rudi, K., & Jakobsen, K.S., 2003. Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in
Milutinović, A., Sedmak, B., Horvat-Znidarsic, I., & Suput, D., 2002. Renal injuries induced by chronic intoxication with microcystins. Cell. Mol. Biol. Lett. 7(1), 139-141. PMid:11944069.
Mohamed, Z.A., El-Sharouny, H.M., & Ali, W.S.M., 2006. Microcystin production in benthic mats of cyanobacteria in the Nile River and irrigation canals, Egypt. Toxicon 47(5), 584-590. PMid:16564062.
Mowe, M.A.D., Mitrovic, S.M., Lim, R.P., Furey, A., & Yeo, D.C.J., 2015. Tropical cyanobacterial blooms: a review of prevalence, problem taxa, toxins and influencing environmental factors. J. Limnol. 74(2), 205-224.
Nishizawa, T., Ueda, A., Asayama, M., Fujii, K., Harada, K., Ochi, K., & Shirai, M., 2000. Polyketide synthase gene coupled to the peptide synthetase module involved in the biosynthesis of the cyclic heptapeptide microcystin. J Biochem 127(5), 779-789. PMid:10788786.
Nübel, U., Garcia-Pichel, F., & Muyzer, G., 1997. PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl. Environ. Microbiol. 63(8), 3327-3332. PMid:9251225.
Ohtani, I., Moore, R.E., & Runnegar, M.T.C., 1992. Cylindrospermopsin: a potent hepatotoxin from the blue-green alga
Orquera, E., & Cabrera, M., 2020. Caracterización del estado trófico de la laguna de Yambo mediante el análisis de fósforo. InfoANALITICA 8(1), 99-111.
Padisák, J., & Reynolds, C.S., 1998. Selection of phytoplankton associations in Lake Balaton, Hungary, in response to eutrophication and restoration measures, with special reference to the cyanoprokaryotes. Hydrobiologia 384(1-3), 41-53.
Padisák, J., 1997.
Percival, S.L., & Williams, D.W., 2013. Cyanobacteria. In: Percival, S.L., Yates, M.V., Williams, D., Chalmers, R., Gray, N. (Eds.), Microbiology of waterborne diseases: microbiological aspects and risks (2nd ed.). Cambridge: Academic Press.
Rasmussen, B., Fletcher, I.R., Brocks, J.J., & Kilburn, M.R., 2008. Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455(7216), 1101-1104. PMid:18948954.
Ríos-Touma, B., Villamarín, C., Jijón, G., Checa, J., Granda-Albuja, G., Bonifaz, E., & Guerrero-Latorre, L., 2022. Aquatic biodiversity loss in Andean urban streams. Urban Ecosyst.
Rodríguez Ayala, S., Flores, R., Rodríguez, M., & Andocilla, M., 2018. Quantitative determination of heavy metal hyperaccumulation in a macrophyte sample of
Schembri, M.A., Neilan, B.A., & Saint, C.P., 2001. Identification of genes implicated in toxin production in the cyanobacterium
Schutz, L., 2014. Survey of agricultural practices and alternatives to pesticide use to conserve water resources in the Mojanda Watershed, Ecuador. Future Food J. Food Agric. Soc. 2(1), 76-92.
Seawright, A.A., Nolan, C.C., Shaw, G.R., Chiswell, R.K., Norris, R.L., Moore, M.R., & Smith, M.J., 1999. The oral toxicity for mice of the tropical cyanobacterium
Seymour, M., 2019. Rapid progression and future of environmental DNA research. Commun. Biol. 2(1), 80. PMid:30820475.
Shalev-Alon, G., Sukenik, A., Livnah, O., Schwarz, R., & Kaplan, A., 2002. A novel gene encoding amidinotransferase in the cylindrospermopsin producing cyanobacterium
Smith, F.M.J., Wood, S.A., van Ginkel, R., Broady, P.A., & Gaw, S., 2011. First report of saxitoxin production by a species of the freshwater benthic cyanobacterium,
Stefanova, K., Radkova, M., Uzunov, B., Gärtner, G., & Stoyneva-Gärtner, M., 2020. Pilot search for cylindrospermopsin-producers in nine shallow Bulgarian waterbodies reveals nontoxic strains of
Štraser, A., Filipič, M., Gorenc, I., & Žegura, B., 2013. The influence of cylindrospermopsin on oxidative DNA damage and apoptosis induction in HepG2 cells. Chemosphere 92(1), 24-30. PMid:23601126.
Stüken, A., Rücker, J., Endrulat, T., Preussel, K., Hemm, M., Nixdorf, B., Karsten, U., & Wiedner, C., 2006. Distribution of three alien cyanobacterial species (Nostocales) in northeast Germany
Thomas, B., & Dittmann, E., 2005. Molecular biology of cyanobacterial toxins: genetic basis of microsystin production. In J. Huisman, H.C.P. Matthisj, P.M. Visser, eds. Harmful cyanobacteria. USA: Springer, 25-40.
Van Colen, W., Portilla, K., Oña, T., Wyseure, G., Goethals, P., Velarde, E., & Muylaert, K., 2017. Limnology of the neotropical high elevation shallow lake Yahuarcocha (Ecuador) and challenges for managing eutrophication using biomanipulation. Limnologica 67, 37-44.
Venegas, J., Castillejo Pons, P., Chamorro, S., Carrillo, I., & Lobo, E., 2018. Characterization and spatio-temporal dynamics of
Via-Ordorika, L., Fastner, J., Kurmayer, R., Hisbergues, M., Dittmann, E., Komarek, J., Erhard, M., & Chorus, I., 2004. Distribution of microcystin-producing and non-microcystin-producing Microcystis sp. in European freshwater bodies: detection of microcystins and microcystin genes in individual colonies. Syst. Appl. Microbiol. 27(5), 592-602. PMid:15490561.
Walter, J.M., Lopes, F.A.C., Lopes-Ferreira, M., Vidal, L.M., Leomil, L., Melo, F., de Azevedo, G.S., Oliveira, R.M.S., Medeiros, A.J., Melo, A.S.O., De Rezende, C.E., Tanuri, A., & Thompson, F.L., 2018. Occurrence of harmful cyanobacteria in drinking water from a severely drought-impacted semi-arid region. Front. Microbiol. 9, 176. PMid:29541063.
Whitton, B.A., & Potts, M., 2002. Introduction the Cyanobacteria. Bogotá. Kluwer Academic Publishers.
Wiedner, C., Rücker, J., Fastner, J., Chorus, I., & Nixdorf, B., 2008. Seasonal dynamics of cylindrospermopsin and cyanobacteria in two German lakes. Toxicon 52(6), 677-686. PMid:18725243.
Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S., & Madden, T.L., 2012. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13(1), 134. PMid:22708584.
Zhang, W., Lou, I., Ung, W.K., Kong, Y., & Mok, K.M., 2014. Application of PCR and real-time PCR for monitoring cyanobacteria,
Zhou, L., Yu, H., & Chen, K., 2002. Relationship between microcystin in drinking water and colorectal cancer. Biomed Environ Sci. 15(2), 166-171. PMid:12244757.
Zupančič, M., Kogovšek, P., Šter, T., Remec Rekar, Š., Cerasino, L., Baebler, Š., Krivograd Klemenčič, A., & Eleršek, T., 2021. Potentially toxic planktic and benthic cyanobacteria in slovenian freshwater bodies: detection by quantitative PCR. Toxins (Basel) 13(2), 1-19. PMid:33670338.
Submetido em:
09/03/2022
Aceito em:
28/09/2022
Publicado em:
11/10/2022
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