Abstract
In tropical countries, the control of the mosquito Aedes aegypti is a public health priority due to its role as a vector of important viral diseases. Marine cyanobacteria are recognized as abundant sources of bioactive compounds, and they constitute a potential source of insecticides useful for controlling mosquito populations and preventing epidemic outbreaks. We collected 30 benthic cyanobacterial mats in Providencia and Rosario islands (in the Colombian Caribbean) belonging to the genera Phormidium, Symploca, Oscillatoria, Lyngbya, Pseudoanabaena, Leptolyngbya, Moorea, and Dapis. Fractions of organic extracts from the most abundant environmental samples were evaluated in three bioassays, assessing (i) larvicidal activity against A. aegypti, (ii) toxicity against the brine shrimp (Artemia salina) nauplii, and (iii) acetylcholinesterase inhibition. Non-polar fractions exhibited larvicidal activity. The polar fraction from one Dapis pleuosa extract showed larvicidal activity without being toxic against A. salina nauplii. Extracts from Moorea producens exhibited the greatest toxicity against A. aegypti larvae and A. salina nauplii. From 23 cultured cyanobacterial samples, only five grew under laboratory conditions and produced enough biomass to yield organic extracts. Of these, three extracts showed strong larvicidal activity, but only the extract from Phormidium tenue showed reduced toxicity against A. salina nauplii. We detected variation among the chemical profiles and larvicidal activity of cyanobacterial consortia depending on sites and dates of collection. Our findings suggest that despite variation in chemical profiles, extracts of marine benthic cyanobacteria can be further developed as effective control agents against insect vectors, in their larval stages. The culture of marine benthic cyanobacteria needs to be further explored to provide enough biomass leading to the identification of bioactive compounds with public health applications.
https://www.who.int/denguecontrol/mosquito/en/
http://www.who.int/mediacentre/factsheets/zika/en/
http://www.who.int/mediacentre/factsheets/fs327/en/
http://www.ncbi.nlm.nih.gov/pubmed/28403438
http://apps.who.int/irisbitstream/10665/75303/1/9789241504034_eng.pdf
Tan L. Bioactive natural products from marine cyanobacteria for drug discovery, Phytochemistry, 68(7): 954-979, 2007.
doi: 10.1016/j.phytochem.2007.01.012
Berry J, Gantar M, Perez M, Berry G, Noriega F. Cyanobacterial toxins as allelochemicals with potential applications as algaecides, herbicides and insecticides, Marine Drugs, 6(2): 117-146, 2008.
doi: 10.3390/md20080007
Harada K, Suomalainen M, Uchida H, Masui H, Ohmura K, Kiviranta J, Ikemoto T. Insecticidal compounds against mosquito larvae from Oscillatoria agardhii Strain 27, Environmental Toxicology, 15: 114-119, 1999.
doi: 10.1002/(SICI)1522-7278(2000)15:2<114::AIDTOX7>3.0.CO;2-P
Berry GA. Mosquito Larvicides from Cyanobacteria. FIU Electronic Theses and Dissertations. 1449.
doi: 10.25148/etd.FI14071114
Castenholz RW. Culturing methods for cyanobacteria, Methods in Enzymology, 167: C 68-93, 1988.
doi: 10.1016/0076-6879(88)67006-6
Puyana M, Acosta A, Bernal-Sotelo K, Velásquez-Rodríguez T, Ramos F. Spatial scale of cyanobacterial blooms in Old Providence Island, Colombian Caribbean, Universitas Scientiarum,
(1): 83-105, 2014.
doi: 10.11144/Javeriana.SC20-1.sscb
Baker JA, Neilan BA, Entsch B, Mckay DB. Identification of cyanobacteria and their toxigenicity in environmental samples by rapid molecular analysis, Environmental Toxicology, 16(6): 472- 482, 2001.
doi: 10.1002/tox.10010
DeLong EF. The microbial ocean from genomes to biomes, Nature, 459: (7244) 200-206, 2009.
doi: 10.1038/nature08059
Tan LT. Pharmaceutical agents from filamentous marine cyanobacteria, Drug Discovery Today, 18: (17) 863-871, 2013.
doi: 10.1016/j.drudis.2013.05.010
Martins A, Vieira H, Gaspar H, Santos S. Marketed marine natural products in the pharmaceutical and cosmeceutical industries: Tips for success, Marine Drugs, 12: (2) 1066-1101, 2014.
doi: 10.3390/md12021066
Engene N, Rottacker E, Kaštovský J, Byrum T, Choi H, Ellisman M, Komárek J, Gerwick W. Moorea producens gen. nov., sp. nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites, Internationa Journal of Systematic and Evolutionary Microbiology, 62: (5) 1171-1178, 2012.
doi: 10.1099/ijs.0.033761-0
Gerwick L, Gerwick W, Coates R, Engene N, Grindberg R, Jones A, Sorrels C. Giant marine cyanobacteria produce exciting potential pharmaceutical, American Society for Microbiology, 3: 277- 284, 2008.
doi: 10.1128/microbe.3.277.1
Thacker R, Paul V. Are benthic cyanobacteria indicators of nutrient enrichment? Relationships between cyanobacterial abundance and environmental factors on the reef flats of Guam, Bulletin of Marine Science, 69: 497-508, 2001.
Abed R, Dobrestov S, Al-Kharusi S, Schramm A, Jupp B, Golubic S. Cyanobacterial diversity and bioactivity of inland hypersaline microbial mats from a desert stream in the Sultanate of Oman, Fottea, 11: (1) 215-224, 2011.
doi: 10.5507/fot.2011.020
Palinska K, Abed R, Wendt K, Charpy L, Lotocka M, Golubic S. Opportunistic Cyanobacteria in benthic microbial mats of a tropical lagoon, Tikehau Atoll, Tuamotu Archipelago: minor in natural populations, major in cultures, Fottea, 12: 127-140, 2012.
doi: 10.5507/fot.2012.010
Tan LT. Bioactive natural products from marine cyanobacteria for drug discovery, Phytochemistry, 68: (7) 954-979, 2007.
doi: 10.1016/j.phytochem.2007.01.012
Guezennec J, Moppert X, Raguenes G, Richert L, Costa B, Simon-Colin C. Microbial mats in French Polynesia and their biotechnological applications, Process Biochemestry, 46: (1) 16-22, 2011.
doi: 10.1016/j.procbio.2010.09.001
Quintana J, Bayona LM, Castellanos L, Puyana M, Camargo P, Aristizábal F, Edwards C, Tabudravu JN, Jaspars M, Ramos FA. Almiramide D, cytotoxic peptide from the marine cyanobacterium Oscillatoria nigroviridis, Bioorganic & Medicinal Chemistry, 22: (24) 6789-6795, 2014.
doi: 10.1016/j.bmc.2014.10.039
Gutiérrez C, Marrugo M, Lozano P, Sierra P, Andrade C. El Entorno Ambiental del Parque Nacional Natural Corales del Rosario Y de San Bernardo. Parque Nacional Natural Corales del Rosario y de San Bernardo. Cartagena de Indias 2011.
Gómez D, Segura C, Sierra P, Garai J. Atlas de la Reserva de Biósfera Seaflower. Archipiélago de San Andrés, Old Providence y Santa Catalina. Instituto de Investigaciones Marinas y Costeras “José Benito Vives De Andréis” –INVEMAR y Corporación para el Desarrollo Sostenible del Archipiélago de San Andrés, Old Providence y Santa Catalina-CORALINA, Serie Publicaciones Especiales N°28. Santa Marta 2012.
Bolañoz N, Acosta A. ¿Qué perdió Colombia con el fallo de la Haya?, Revista Javeriana, 742: 56-62, 2013.
Geister J. The influence of wave exposure on the ecological zonation of Caribbean coral reefs, p. 23-29. In: D.L. Taylor (ed.) Proceedings of Third International Coral Reef Symposium Vol. 2: Geology. Rosenstiel School of Marine and Atmospheric Science, Miami, Florida.
Geister J. Recent coral reefs and geologic history of Old Providence island (western Caribbean sea, Colombia), Geología Colombiana, 15: 115 134, 1986.
Diaz JM, Barrios LM, López-Victoria M. Áreas Coralinas de Colombia. N° 5. Santa Marta: Invemar, Serie Publicaciones Especiales N°5, Santa Marta 2000.
Alvarado E, Pizarro V, Sarmiento A. El Entorno Ambiental del Parque Nacional Natural Corales del Rosario y de San Bernardo. Parques Nacionales Naturales de Colombia. Dirección Territorial Caribe. Parque Nacional Natural Corales del Rosario y de San Bernardo. Cartagena de Indias 2011.
Komárek J, Kaštovský J, Mareš J, Johansen JR. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) using a polyphasic approach, Preslia, 86: (4) 295-335, 2014.
doi: 10.1049/iet-ipr.2009.0392
Komárek J. A polyphasic approach for the taxonomy of cyanobacteria: principles and applications, European Journal of Phycology, 51: (3) 346-353, 2016.
doi: 10.1080/09670262.2016.1163738
Engene N, Choi H, Esquenazi E, Rottacker E, Ellisman M, Dorrestein P, Gerwick W. Underestimated biodiversity as a major explanation for the perceived rich secondary metabolite capacity of the cyanobacterial genus Lyngbya, Environmental Microbiology, 13:(6) 1601-1610, 2011.
doi: 10.1111/j.1462-2920.2011.02472.x
Andersen RA, Robert A. Algal culturing techniques. Elsevier Academic Press, United States. 2005. ISBN: 9780080456508
Kalčíková G1, Zagorc-Končan J, Zgajnar Gotvajn A. Artemia salina acute immobilization test: a possible tool for aquatic ecotoxicity assessment, Water Science and Technology, 66(4):903- 908.
doi: 10.2166/wst.2012.271
Marston A, Kissling J, Hostettmann K. A rapid TLC bioautographic method for the detection of acetylcholinesterase and butyrylcholinesterase inhibitors in plants, Phytochemical Analysis, 13(1): 51-54, 2002
doi: 10.1002/pca.623
Castellanos F, Amaya-García F, Tello E, Ramos FA, Umaña A, Puyana M, Resende JALC, Castellanos L. Screening of acetylcholinesterase inhibitors in marine organisms from the Caribbean Sea, Natural Product Research, 1-8, 2018.
doi: 10.1080/14786419.2018.1481837
Puyana M, Prato J, Nueto C, Ramos FA, Castellanos L, Pinzón P, Zárate J. Experimental approaches for the evaluation of allelopathic interactions bewteen hermatypic corals and marine benthic cyanobacteria in the Colombian Caribbean, Acta Biológica Colombiana, 24(2): 243-253, 2019.
doi: 10.15446/abc.v24n2.72706
Engene N, Tronholm A, Paul VJ. Uncovering cryptic diversity of Lyngbya: the new tropical marine cyanobacterial genus Dapis (Oscillatoriales), Journal of Phycology, 54: (4) 435-446, 2018.
doi: 10.1111/jpy.12752
Engene N, Paul V, Byrum T, Gerwick W, Thor A, Ellisman M. Five chemically rich species of tropical marine cyanobacteria of the genus Okeania gen. nov. (Oscillatoriales, Cyanoprokaryota), Journal of Phycology, 49: (6) 1095-1106, 2013.
doi: 10.1111/jpy.12115
Bertin MJ, Vulpanovici A, Monroe EA, Korobeynikov A, Sherman DH, Gerwick L, Gerwick WH. The Phormidolide Biosynthetic Gene Cluster: A trans -AT PKS Pathway Encoding a Toxic Macrocyclic Polyketide, ChemBioChem, 17: (2) 164-173, 2016.
doi: 10.1002/cbic.201500467
Foster JS, Green SJ, Ahrendt SR, Golubic S, Reid RP, Hetherington KL, Bebout L. Molecular and morphological characterization of cyanobacterial diversity in the stromatolites of Highborne Cay, Bahamas, The ISME Journal, 3: (5) 573-587, 2009.
doi: 10.1038/ismej.2008.129
Temraleeva AD, Dronova SA, Moskalenko S V., Didovich S V. Modern methods for isolation, purification, and cultivation of soil cyanobacteria, Microbiology, 85: (4) 389-399, 2016.
doi: 10.1134/S0026261716040159
Harrigan GG, Luesch H, Yoshida WY, Moore RE, Nagle DG, Paul VJ, Mooberry SL, Corbett TH, Valeriote FA. Symplostatin 1: A dolastatin 10 analogue from the marine cyanobacterium Symploca hydnoides, Journal of Natural Products, 61: (9) 1075- 1077, 1998.
doi: 10.1021/np980321c
Harrigan GG, Luesch H, Yoshida WY, Moore RE, Nagle DG, Paul VJ. Symplostatin 2: A dolastatin 13 analogue from the marine cyanobacterium Symploca hydnoides, Journal of Natural Products, 62: 655-658, 1999.
doi: 10.1021/np980553b
Society RC. Marin Lit.
Holland A, Kinnear S. Interpreting the possible ecological role(s) of cyanotoxins: compounds for competitive advantage and/or physiological aide, Marine Drugs, 11: (7) 2239-2258, 2013.
doi: 10.3390/md11072239
Alkofahi A, Rupprecht J, Anderson J, McLaughlin J, Mikolajczak K, Scott B. In: Insecticides of Plant Origin. Chapter 42, Search for New Pesticides from Higher Plants. 25-43 ,1989.
doi: 10.1021/bk-1989-0387.ch003
Kalčíková G, Zagorc-Končan J, Žgajnar Gotvajn A. Artemia salina acute immobilization test: a possible tool for aquatic ecotoxicity assessment, Water Science & Technology, 66: (4) 903- 909, 2012.
doi: 10.2166/wst.2012.271
Morohashi M, Tsuchiya K, Mita T, Kawamura M. Identification of (Na,K) ATOase inhibitor in brine shrimp, Artemia salina, as long-chain fatty acids, Journal of Comparative Physiology B, 161: 69-72, 1991.
doi: 10.1007/BF00258748
Prato J. Afloramientos de cianobacterias marinas bentónicas en San Andrés, Providencia y las Islas del Rosario (Caribe colombiano): Caracterización y evaluación de su posible papel ecológico. Universidad Nacional de Colombia. 2013. Theses Dissertation
Nunes B. The use of cholinesterases in ecotoxicology, Reviews of Environmental Contamination Toxicology, 212: 29-59, 2011.
doi: 10.1007/978-1-4419-8453-1_2
Cook W, Beasley V, Lovell R, Dahlem A, Hooser S, Mahmood N, Carmichael W. Consistent inhibition of peripheral cholinesterases by neurotoxins from the freshwater cyanobacterium Anabaena flos-aquae: Studies of ducks, swine, mice and a steer, Environmental Toxicology and Chemistry, 8: (10) 915-922, 1989.
doi: 10.1002/etc.5620081010
Mahmood NA, Carmichael WW. Anatoxin-a(s), an anticholinesterase from the cyanobacterium Anabaena flosaquae NRC-525-17, Toxicon, 25: (11) 1221-1227, 1987.
doi: 10.1016/0041-0101(87)90140-1
Colovic M, Krstic D, Lazarevic-Pasti T, Bondzic A, Vasic V. Acetylcholinesterase Inhibitors: Pharmacology and Toxicology, Current Neuropharmacology, 11: (3) 315-335, 2013.
doi: 10.2174/1570159X11311030006
Ocampo C, Salazar M, Mina N, McAllister J, Brogdon W. Insecticide resistance status of Aedes aegypti in 10 localities in Colombia, Acta Tropica, 118; 37-44, 2011.
doi: 10.1016/j.pestbp.2014.09.014
Maestre R, Gomez D, Ponce G, Flores A. Susceptibility to incecticides and resistance mechanisms in Aedes aegypti from the Colombian Caribbean Region, Pesticide Biochemistry and Physiology, 116:63-73, 2014.
doi: 10.1016/j.pestbp.2014.09.014
Venkateswara Rao J, Kavitha P, Jakka NM, Sridhar V, Usman PK. Toxicity of Organophosphates on Morphology and Locomotor Behavior in Brine Shrimp, Artemia salina, Archives of Environmental Contamination and Toxicology, 53: (2) 227-232, 2007.
doi: 10.1007/s00244-006-0226-9
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