Sponges from Peru and their potential as source of antibacterial compounds

Las esponjas en el Perú y su potencial como fuente de compuestos antibacterianos

Authors

DOI:

https://doi.org/10.25268/bimc.invemar.2022.51.2.1171

Keywords:

antimicrobial activity,, bacteria, biotechnology, marine biodiversity,, Porifera

Abstract

In the last decades, sponges have emerged as the largest source of active compounds of animal origin for pharmaceutical purposes. In Peru information on these animals is incipient and scattered, which limits taking the right measures for their adequate management, exploitation, and conservation. The aim of this study is to provide an update on the scope and perspectives of sponge research in Peru, with
an emphasis on species richness and their antibacterial potential. Likewise, research initiatives carried out in other South American Pacific countries are reviewed. Research efforts in Peru have allowed the description of 46 species; however, the sponge richness is underestimated. On the other hand, in other latitudes, active principles with antimicrobial activity have been isolated from at least 36 species belonging to 11 of the 25 genera recorded in Peru (44 %), suggesting the high potential of Peruvian sponges as a source of antibacterial metabolites. It is
concluded that the implementation of projects that integrate sponge research at different scales is necessary to contribute to the development
of innovation plans and bio-businesses in the fishing, aquaculture, and pharmaceutical industries.

Dimensions

PlumX

Visitas

1270

Downloads

Download data is not yet available.

Author Biographies

Báslavi Marisbel Cóndor Luján, Universidad Científica del Sur

Bióloga con orientación en Hidrobiología y Pesquería, Universidad Nacional Mayor de San Marcos (UNMSM, Peru). Magíster en Zoología, Museu Nacional do Rio de Janeiro de la Universidad Federal do Rio de Janeiro (MNRJ-UFRJ, Brasil). Doctora en Biodiversidad y Biologia Evolutiva (UFRJ, Brasil). Tiene experiencia en el área de Biología Marina, actuando principalmente en taxonomía, sistemática molecular y ecología de esponjas marina del Caribe, Brasil y Perú. Docente investigadora de la carrera de Biología Marina de la Universidad Científica del Sur (UCSUR, Perú).

Juan Carlos Francia Quiroz, Universidad Científica del Sur

Biólogo con Mención en Biología Celular y Genética, Universidad Nacional Mayor de San Marcos (UNMSM, Perú). Magíster en Recursos Acuáticos, mención Acuicultura, UNMSM. Estudios de Segunda Especialidad en Biología Molecular y Genética, Universidad Nacional Federico Villarreal (UNFV, Perú). Estudiante de Doctorado en Ciencias Biológicas, UNMSM. Especialista en Manejo, nutrición, reproducción y genotoxicidad de organismos acuáticos. Docente - investigador de la Carrera de Biología Marina, Universidad Científica del Sur (UCSUR, Perú).

References

Aguilar-Camacho, J.M., J.L. Carballo and J.A. Cruz-Barraza. 2013. Acarnidae Porifera: Demospongiae: Poecilosclerida) from the Mexican Pacific Ocean with the description of six new species. Sci. Mar., 77(4): 677–696. https://doi.org/10.3989/scimar.03800.06A

Aguirre, L.K., Y. Hooker, Ph. Willenz and E. Hajdu. 2011. A new Clathria (Demospongiae, Microcionidae) from Peru occurring on rocky substrates as well as epibiontic on Eucidaris thouarsii sea urchins. Zootaxa, 3085: 41–54. https://doi.org/10.11646/zootaxa.3085.1.3

Anjum K., S.Q. Abbas, S.A.A. Shah, N. Akhter, S. Batool and S.S.U. Hassan. 2016. Marine sponges as a drug treasure. Biomol. Ther. (Seoul), 24(4): 347–362. https://doi.org/10.4062/biomolther.2016.067

Arai, M., M. Sobou, C. Vilchéze, A. Baughn, H. Hashizume, P. Pruksakorn, S. Ishida, M. Matsumoto, W.R. Jacobs Jr. and M. Kobayashi. 2008. Halicyclamine A, a marine spogean alkaloid as a lead for anti–tuberculosis agent. Bioorg. Med. Chem., 16:6732–6736. https://doi.org/10.1016/j.bmc.2008.05.061

Arai, M., S. Ishida, A. Setiawan and M. Kobayashi. 2009. Haliclonacyclamines, tetracyclic alkylpiperidine alkaloids, as anti–dormant mycobacterial substances from marine sponge of Haliclona sp. Chem. Pharm. Bull., 57(10):1136–1138. https://doi.org/10.1248/cpb.57.1136

Arroyo, Y., E. Hajdu, Ph. Willenz and B. Cóndor-Luján. 2020. First record of Ciocalypta Bowerbank, 1862 (Demospongiae, Suberitida, Halichondriidae) in the Eastern Pacific, with description of a new species from Peru. Zootaxa, 4853(3): 429–441. https://doi.org/10.11646/zootaxa.4853.3.6

Azevedo, F., E. Hajdu, Ph. Willenz and M. Klautau. 2009. New records of calcareous sponges (Porifera, Calcarea) from the Chilean coast. Zootaxa, 2072(1): 1–30. https://doi.org/10.11646/zootaxa.2072.1.1

Azevedo, F., B. Cóndor-Luján, Ph. Willenz, E. Hajdu, Y. Hooker and M. Klautau. 2015. Integrative taxonomy of calcareous sponges (subclass Calcinea) from the Peruvian coast: morphology, molecules, and biogeography. Zool. J. Linn. Soc., 173: 787–817. https://doi.org/10.1111/zoj.12213

Berne, S., M. Kalauz, M. Lapat, L. Savin, D. Janussen, D. Kersken, J. Ambrožič, Š. Zemljič, D Jaklič, N. Gunde-Cimerman, M. Lunder, I. Roškar, T. Eleršek, T. Turk and K Sepčić. 2016. Screening of the Antarctic marine sponges (Porifera) as a source of bioactive compounds. Polar Biol., 39:947–959. https://doi.org/10.1007/s00300-015-1835-4

Bertolino, M., G. Costa, G. Bavestrello, M. Pansini and G. Daneri. 2020. New sponge species from Seno Magdalena, Puyuhuapi Fjord and Jacaf Canal(Chile). Eur. J. Taxon., 715: 1–49. https://doi.org/10.5852/ejt.2020.715

Bianco E.M., S.Q. de Oliveira, C. Rigotto, M.L. Tonini, T. da Rosa Guimarães, F. Bittencourt, L.P. Gouvêa, C. Aresi, M.T. de Almeida, M.I. Moritz, C.D. Martins, F. Scherner, J.L. Carraro, P.A. Horta, F.H. Reginatto, M. Steindel, C.M. Simões and E.P. Schenkel. 2013. Anti-infective potential of marine invertebrates and seaweeds from the Brazilian coast. Molecules (Basel, Switzerland), 18(5):5761–5778. https://doi.org/10.3390/molecules18055761

Bispo, A., Ph. Willenz and E. Hajdu. 2022. Diving into the unknown: fourteen new species of haplosclerid sponges (Demospongiae: Haplosclerida) revealed along the Peruvian coast (southeastern Pacific). Zootaxa, 5087(2):201–252. https://doi.org/10.11646/zootaxa.5087.2.1

Boury-Esnault, N. and C. Volkmer-Ribeiro. 1991. The Porifera: description of a new taxon Balliviaspongia wirrmanni n.g., n.sp.: 295–301. In: Dejoux, C. and A. Iltis. (Eds.), Lake Titicaca: a synthesis of limnological knowledge. Monographiae Biologicae, 68. Kluwer Academic: Dordrecht, Boston, London: i-xxiv, 1. 296 p.

Brain, C.K., A.R. Prave, K.H. Hoffmann, A. E. Fallick, A. Botha, D. A. Herd, C. Sturrock, I. Young, D.J. Condon and S.G. Allison. 2012. The first animals: ca. 760-million-year-old sponge-like fossils from Namibia. S. Afr. J. Sci., 108(1/2):1–8. http://dx.doi.org/10.4102/sajs.v108i1/2.658

Brinkmann, C., A. Marker and D. I. Kurtböke. 2017. An overview on marine sponge-symbiotic bacteria as unexhausted sources for natural product discovery. Diversity, 9(4): 40. https://doi.org/10.3390/d9040040

Calabro K., B.E. Chalen, G. Genta-Jouve, K.B. Jaramillo, C. Domínguez, M. de la Cruz, B. Cautain, F. Reyes, O.P. Thomas and J. Rodríguez. 2018. Callyspongidic Acids: amphiphilic diacids from the Tropical Eastern Pacific sponge Callyspongia cf. californica. J. Nat. Prod., 81(10):2301–2305.

Capon, R., M. Miller and F. Rooney. 2001. Mirabilin G: A new alkaloid from a southern Australian marine sponge, Clathria species. J. Nat. Prod., 64 (5):643–644. https://doi.org/10.1021/np000564g

Cárdenas, C.A., E.M. Newcombe, E. Hajdu, M. González-Aravena, S.W. Geange and J.J. Bell. 2016. Sponge richness on algae-dominated rocky reefs in the western Antarctic Peninsula and the Magellan Strait. Polar Res., 35(1):1–6. https://doi.org/10.3402/polar.v35.30532

Carter, G.T. and K.L. Rinehart Jr. 1978. Acarnidines, novel antiviral and antimicrobial compounds from the sponge Acarnus erithacus (de Laubenfels). J.Am. Chem. Soc., 100 (13):4302–4304. https://doi.org/10.1021/ja00481a049

Cavalcanti, F. and M. Klautau. 2011. Solenoid: a new aquiferous system to Porifera. Zoomorphology, 130(4):255–260. https://doi.org/10.1007/s00435-011-0139-7

Cheng, Z.B., H. Xiao., C.Q. Fan, Y.N. Lu, G. Zhang and S. Yin. 2013. Bioactive polyhydroxylated sterols from the marine sponge Haliclona crassiloba. Steroids, 78(14):1353–1358. https://doi.org/10.1016/j.steroids.2013.10.004

Cita, Y.P., F.K. Muzaki, O.K. Radjasa and P. Sudarmono. 2017. Screening of antimicrobial activity of sponges extract from Pasir Putih, East Java (Indonesia). J. Marine Sci. Res. Dev., 7(5):1–5. https://doi.org/10.4172/2155-9910.1000237

Concytec. 2016. Programa Nacional Transversal de Biotecnología 2016–2021. Primera edición. Lima, Perú. 81 p. https://portal.concytec.gob.pe/images/noticias/pronbiotec_final.pdf

Cóndor, B., P. Gallegos y E. Hajdu. 2010. Macrofauna asociada a Hymeniacidon cf. sinapium (Porifera: Demospongiae: Halichondriidae) en bahía de Ancón, Lima, Perú. Segundo Congreso de Ciencias del Mar del Perú, Piura, Perú.

Cóndor-Luján, B., F. Azevedo, E. Hajdu, Y. Hooker, Ph. Willenz and M. Klautau. 2019. Tropical Eastern Pacific Amphoriscidae Dendy, 1892 (Porifera:Calcarea: Calcaronea: Leucosolenida) from the Peruvian coast. Mar. Biodivers., 49(3):1813–1830. https://doi.org/10.1007/s12526-019-00946-y Cóndor-Luján, B., P. Leocorny, A. Padua, F. Azevedo, V. Corrêa Seixas, Y. Hooker, E. Hajdu, Ph. Willenz, T. Pérez and M. Klautau. 2021. Evolutionary history of the calcareous sponge Clathrina aurea: genetic connectivity in the western Atlantic and intriguing occurrence in the Eastern Pacific. Mar.Biol., 168(127):1–23.

https://doi.org/10.1007/s00227-021-03934-8

Davis, R.A., G.C. Mangalindan, Z.P. Bojo, R.R. Antemano, N.O. Rodríguez, G.P. Concepción, S.C. Samson, D. de Guzmán, L.J. Cruz, D. Tasdemir, M.H. Harper, X. Feng, G.T. Carter and C.M. Ireland. 2004. Microcionamides A and B, bioactive peptides from the Philippine sponge Clathria (Thalysias) abietina. J. Org. Chem., 69:4170–4176. https://doi.org/10.1021/jo040129h

Debrenne, F., A.Y. Zhuravlev and P.D. Kruse. 2002. Class Archaecyatha Bornemann, 1884: 1539–1699. In: Hooper, J.N.A. and R.W.M. van Soest. (Eds.) Systema Porifera. A guide to the classification of sponges. Kluwer Academic/Plenum Publishers, New York. 1707 p.

de Goeij, J.M., D. von Oevelen, M.J.A. Vermeij, R. Osinga, J.J. Middelburg, A.F.P.M. de Goeij and W. Admiraal. 2013. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science, 342(6154): 108–110. https://doi.org/10.1126/science.1241981

de Laubenfels, M.W. 1932. The marine and fresh-water sponges of California. Proc. U.S. Natl. Mus., 81 (2927): 1–140. https://doi.org/10.5479/si.00963801.81-2927.1

de Oliveira, J.H.H., M.H.R. Seleghim, C. Timm, A. Grube, M. Köck, G.G.F. Nascimento, A.C.T. Martins, E.G.O. Silva, A.O.De Souza, P.R.R. Minarini, F.C.S. Galetti, C.L. Silva, E. Hajdu and R.G.S. Berlinck. 2006a. Antimicrobial and antimycobacterial activity of cyclostellettamine alkaloids from sponge Pachychalina sp. Mar. Drugs, 4(1): 1–8. https://doi.org/10.3390/md401001

de Oliveira, M.F., J.H.H.L. de Oliveira, F.C.S. Galetti, A.O. de Souza, C. Lopes Silva, E. Hajdu, S. Peixinho and R.G.S. Berlinck. 2006b. Antinycobacterial brominated metabolites from two species of marine sponges. Planta Medica 72(5): 437–441. https://doi.org/10.1055/s-2005-916239

de Silvestri, S. Zea y C. Duque. 1994. Actividad antibacteriana de algunas esponjas del Caribe colombiano. Rev. Col. Cienc. Quím. Farm., 22: 21–26.

Desqueyroux, R. y H. Moyano. 1987. Zoogeografía de demospongias chilenas. Bol. Soc. Biol. Concepc. (Chile), 58: 39–66.

Desqueyroux-Faúndez, R. and R.W.M. van Soest. 1996. A review of Iophonidae, Myxillidae and Tedaniidae occurring in the South East Pacific (Porifera: Poecilosclerida). Rev. Suis. Zool., 103(1): 3–79. https://doi.org/10.5962/bhl.part.79938

Desqueyroux-Faúndez, R. and R.W.M van Soest. 1997. Shallow water Demosponges of the Galápagos Islands. Rev Suisse Zool., 104(2):379–467. https://doi.org/10.5962/bhl.part.80003

Duraikannu, K., D. Edupalli, G. Rameshkumar and S. Ravichandran. 2009. Antimicrobial peptide from marine sponge Clathria indica (Dendy,1889). Am.-Eurasian J. Sci. Res., 4(1):47–53.

Encarnación, D.R., S.G. Franzblau, C.A. Tapia and R. Cedillo-Rivera. 2000. Screening of marine organisms for antimicrobial and antiprotozoal activity. Pharm. Biol., 38(5):379–384. https://doi.org/10.1076/phbi.38.5.379.5964

Escobar, T. 2000. Inventario y estudio taxonómico de las esponjas (Phylum Porifera) de algunas áreas del Pacífico colombiano. Tesis Biol. Mar. Univ. Valle, Cali. 149 p.

Fernández, J.C., M. Gastaldi, G. Zapata-Hernández, L.M. Pardo, F.L. Thompson and E. Hajdu. 2021. New species of Crella (Pytheas) Topsent, 1890 and Crellomima Rezvoi, 1925 (Crellidae, Poecilosclerida, Demospongiae) from Chilean shallow and Argentinean deep waters, with a synthesis on the known phylogenetic relationships of crellid sponges. Zootaxa, 5052(3):353–379. https://doi.org/10.11646/zootaxa.5052.3.3

Fontana, T., B. Cóndor-Luján, F. Azevedo, T. Pérez and M. Klautau. 2018. Diversity and distribution patterns of calcareous sponges (subclass Calcinea) from Martinique. Zootaxa, 4410:331–369. https://doi.org/10.11646/zootaxa.4410.2.5

Frith, D.W. 1976. Animals associated with sponges at North Haying, Hampshire. Zool. J. Linn. Soc., 58:353–362.

García-Suárez, S.D., A. Acosta, E. Londoño-Cruz y J.R. Cantera K. 2012. Organismos sésiles y móviles del litoral rocoso: en el Pacífico colombiano: una guía visual para su identificación. Ser. Doc. Esp., (26). Invemar, Santa Marta. 133 p.

Gazave, E., P. Lapébie, A. Ereskovsky, J. Vacelet, E. Renard, P. Cárdenas and C. Borchiellini. 2012. No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera. In: Maldonado, M., X. Turon, M.A. Becerro and M.J. Uriz (Eds.) Ancient animals, new challenges. Sponge research developments. Hydrobiologia, 687(1): 3–10. https://doi.org/10.1007/s10750-011-0842-x

Granito, R.N., M.R. Custódio and A.C. Rennó. 2016. Natural marine sponges for bone tissue engineering: The state of art and future perspectives. J. Biomed. Mater. Res. Part B Appl. Biomater., 105(6): 1717–1727. https://doi.org/10.1002/jbm.b.33706

Gunasekera, S.P., P.J. McCarthy and M. Kelly-Borges. 1994. Hamacanthins A and B, new antifungal bis indole alkaloids from the deep-water marine sponge, Hamacantha sp. J. Nat. Prod., 57(10): 1437–1441. https://doi.org/10.1021/np50112a014

Gupta, P., U. Sharma, T.C. Schulz, A.B. McLean, A.J. Robins and L.M. West. 2012. Bicyclic C21 terpenoids from the marine sponge Clathria compressa. J. Nat. Prod., 75: 1223–1227. https://doi.org/10.1021/np300265p

Hajdu, E. and R. Desqueyroux-Faúndez. 2008. A reassessment of the phylogeny and biogeography of Rhabderemia Topsent, 1890 (Rhabderemiidae, Poecilosclerida, Demospongiae). Rev. Suis. Zool., 115(2): 377–395.

Hajdu, E., R. Desqueyroux-Faúndez, M.S. Carvalho, G. Lôbo-Hajdu and Ph. Willenz. 2013. Twelve new Demospongiae (Porifera) from Chilean fjords, with remarks upon sponge-derived biogeographic compartments in the SE Pacific. Zootaxa, 3744: 1–64. https://doi.org/10.11646/zootaxa.3744.1.1

Hajdu, E., Y. Hooker and Ph. Willenz. 2015. New Hamacantha from Peru, and resurrection of Zygherpe as subgenus (Demospongiae, Poecilosclerida, Hamacanthidae). Zootaxa, 3926(1): 87‒99. https://doi.org/10.11646/zootaxa.3926.1.3

Han, B.N., L.L. Hong, B.B. Gu, Y.T. Sun, J. Wang, J.T. Liu and H.W. Lin. 2019. Natural products from sponges. In: Li, Z. (Ed.) Symbiotic microbiomes of coral reef sponges and corals. Springer, Dordrecht. 329–463. https://doi.org/10.1007/978-94-024-1612-1_15 Hooper, J., R. van Soest and F. Debrenne. Phylum Porifera Grant, 1836. 2002. 9–13. In: Hooper, J.N.A. and R.W.M. van Soest. (Eds.) Systema Porifera. A guide to the classification of sponges. Kluwer Academic/Plenum Publishers, New York. 1707 p.

Hutagalung, R.A., V.M. Karjadidjaja, V. D. Prasasty and N. Mulyono. 2014. Extraction and characterization of bioactive compounds from cultured and natural sponge, Haliclona molitba and Stylotella aurantium Origin of Indonesia. Int. J. Biosci. Biochem. Bioinform., 4(1): 14–18.

Hyatt, A. 1877. Revision of the North American Poriferae; with remarks upon foreign species. Part II. Mem. Boston Soc. Nat. Hist., 2: 481–554, pls XV–XVII. Ibrahim, H.A., H.O. Ahmed, F.A.A. El Razek and E. Elmasry. 2018. Proteolysis and heat sensitive antibacterial agents from several levantine sponge species. Int. J. Adv. Res., 6(2): 14–27. http://dx.doi.org/10.21474/IJAR01/6403

Ibrahim, H.A.H., D.E. Elabiary and M.M. Hamed. 2020. Antimicrobial activity of some Egyptian marine invertebrates, Red Sea. Egypt. J. Aquat. Biol. Fish., 24(4): 321–340. http://doi.org/10.21608/ejabf.2020.98494

Jaramillo, K.B., B. Cóndor-Luján, B. Longakit. J. Rodriguez, O.P. Thomas, G. McCormack and E. Hajdu. 2021. New records of Demospongiae (Porifera) from Reserva Marina El Pelado (Santa Elena, Ecuador), with description of Tedania (Tedania) ecuadoriensis sp. nov. Zookeys, 1011:101–120. https://doi.org/10.3897/zookeys.1011.54485

Karimpoor, M., E. Kamrani, M. Yousefzadi and M. Nazemi. 2018. Antibacterial and antioxidant potential of Haliclona caerulea extracts from Tidal Island Larak, Persian Gulf. JMBS, 9(3): 347–353.

Kaplan, A.R., C.L. Schrank and W.M. Wuest. 2021. An efficient synthesis of 3-alkylpyridine alkaloids enables their biological evaluation. Chem. Med. Chem., 16: 2487–2490. https://doi.org/10.1002/cmdc.202100134

Kersken, D., D. Janussen and P. Martínez. 2018. Deep-sea glass sponges (Hexactinellida) from polymetallic nodule fields in the Clarion-Clipperton Fracture Zone (CCFZ), northeastern Pacific: Part I – Amphidiscophora. Mar. Biodivers., 48(1):545–573. https://doi.org/10.1007/s12526-017-0727-y

Klautau, M. 2016. Capitulo 7 Porifera. En: Fransozo, A. y M.L. Negreiros-Fransozo (Eds). Zoologia dos Invertebrados. Editora Guanabara Koogan, Rio de Janeiro. Kobayashi, J., C. Zeng, M. Ishibashi, H. Shigemori, T. Sasakib and Y. Mikami. 1992. Niphatesines E-H, new pyridine alkaloids from the Okinawan marine sponge Niphates sp. J. Chem. Soc., 1: 1291–1294.

Koltun, V.M. 1970. Sponge fauna of the northwestern Pacific from the shallows to the hadal depths: 165–221. In: Bogorov, V.G. (Ed.) Fauna of the KurileKamchatka Trench and its environment. Inst. Oceanol. Acad. Sci. U.S.S.R., 86 (Akademiya Nauk SSSR. Trudy Instituta Okeanologii in P.P. Shishov and Izdatelstvo Nauka, Moskwa). 372 p, pls 1–8.

Konuklugil, B. and B. Gozcelioglu. 2015. Antimicrobial activity of marine samples collected from the different coasts of Turkey. Turk. J. Pharm. Sci., 12(3): 116–125.

Kulchin, Y., A.V. Bezverbny, O.A. Bukin, S.S. Voznesensky, A.N. Galkina, A. L. Drozdov and I.G. Nagorny. 2009. Optical and nonlinear optical properties of sea glass sponge spicules: 315–340. In: Müller, W.E.G. and M.A. Grachev (Eds.) Biosilica in evolution, morphogenesis, and nanobiotechnology. Prog. Mol. Subcell Biol., 47. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-88552-8_14

Kunzmann, K. 1996. Associated fauna of selected sponges (Hexactinellida and Demospongiae) from the Weddell Sea, Antarctica. Berich. Polarfors., 210: 1–93. Latifah, L.A., A. Tahir and N.H. Soekamto. 2021. Antibacterial assay of crude extracts from marine sponge Haliclona fascigera in Badi Island of Spermonde Archipelago against shrimp pathogenic bacteria. IOP Conf. Ser.: Earth Environ. Sci., 763:012029. https://doi.org/10.1088/1755-1315/763/1/012029

Lee, Y., K.H. Jang, J. Jeon, W.Y. Yang, C.J. Sim, K.B. Oh and J. Shin. 2012. Cyclic Bis–1,3 dialkylpyridinoums from the sponge Haliclona sp. Mar. Drugs, 10:2116–2137. https://doi.org/10.3390/md10092126

León, J., J. Aponte, S. Montero, N. Galindo, M. Huamán y U. Tarazona. 2015. Aislamiento de actinomicetos asociados a esponjas marinas y evaluación del potencial antimicrobiano frente a patógenos multi-drogo-resistentes (MDR). XXIV Reun. Cient. Inst. Invest. Cienc. Biol. Antonio Raymundi, Lima.

Lévi, C. 1964. Spongiaires des zones bathyale, abyssale et hadale. Galathea Rep. Sci. Res. Danish Deep-Sea Exp. Round World, 1950-52. 7: 63-112, pls II-XI. 93 p.

Lino, M., J. León y M. Huáman. 2016. Evaluación de la capacidad antagonista de un antimicrobiano producido por Streptomyces sp. CEPA 13A-2 frente a microorganismos resistentes a β-lactámico de origen hospitalario. Rev. Peru Investig. Matern. Perinat., 5(1): 28‒34. https://doi.org/10.33421/inmp.201652

Lippert, H., R. Brinkmeyer, T. Mulhaupt and K. Iken. 2003. Antimicrobial activity in sub-Arctic marine invertebrates. Polar Biol., 26: 591‒600. https://doi.org/10.1007/s00300-003-0525-9

Lizarazo, N., S. Zea, L. Chasqui y N. Rincón-Díaz. 2020a. Diversidad de esponjas (Porifera) en los riscales y morros del Pacífico norte chocoano: 82‒91. En: Chasqui, L. (Ed.). Biodiversidad de los arrecifes rocosos (riscales y morros) del Pacífico norte chocoano. Ser. Publ. Gen. Invemar. 318 p. https://n2t.net/ark:/81239/m9x11f

Lizarazo, N., S. Zea, L. Chasqui y N. Rincón-Díaz. 2020b. Biodiversidad de esponjas en arrecifes rocosos del Chocó norte, Pacífico colombiano. Bol. Invest. Mar. Cost., 49(2): 79‒130.

López, Y., V. Cepas and S.M. Soto. 2018. The marine ecosystem as a source of antibiotics. In: Rampelotttao, P. and A. Trincone (Eds.) Grand challenges in marine biotechnology. Springer, Cham. https://doi.org/10.1007/978-3-319-69075-9_1

Maarisit, W., D.B.Abdjul, H. Yamazaki, H. Kato, H. Rotinsulu, D. S. Wewengkang, D. A. Sumilat, M. M. Kapojos, K. Ukai and M. Namikoshi. 2017. Antimycobacterial alkaloids, cyclic 3-alkyl pyridinium dimers, from the Indonesian marine sponge Haliclona sp. Bioorg. Med. Chem. Lett., 27:3503–3506. https://doi.org/10.1016/j.bmcl.2017.05.067

Mahaut, M.L., O. Basuyaux, E. Baudinière, C. Chataignier, J. Pain and C. Caplat. 2013. The porifera Hymeniacidon perlevis (Montagu, 1818) as a bioindicator for water quality monitoring. Environ. Sci. Pollut. Res. Int., 20(5): 2984‒2992. https://doi.org/10.1007/s11356-012-1211-7

Maldonado, M., R. Aguilar, R.J. Bannister, J.J. Bell, K.W. Conway, P.K. Dayton, C. Diaz, J. Gutt, M. Kelly, E.L.R. Kenchington, S. Leys, S.A. Pomponi, H.T. Rapp, K. Rützler, O.S. Tendal, J. Vacelet and C.M. Young. 2016. Sponge grounds as keys marine habitats: a synthetic review of types, structure, functional roles, and conservation concerns: 1‒39. In: Rossi, S., L. Bramanti, A. Gori and C. Orejas Saco del Valle (Eds.) Marine animal forests: The ecology of benthic biodiversity hotspots. Springer, Switzerland. https://doi.org/10.1007/978-3-319-17001-5_24-1

Manuel, M., R. Borojevic, N. Boury-Esnault and J. Vacelet. 2002. Class Calcarea Bowerbank, 1864: 1103‒1110. In: Hooper, J.N.A. and R.W.M. van Soest. (Eds.) Systema Porifera. A guide to the classification of sponges. Kluwer Academic/Plenum Publishers, New York. 1707 p.

Marinho, P.R., G.R.S. Muricy, M.F.L. Silva, M.G. de Marval and M.S. Laport. 2010. Antibiotic resistant bacteria inhibited by extracts and fractions from Brazilian marine sponges. Rev. Bras. Farmacogn., 20(2): 267–275. https://doi.org/10.1590/S0102-695X2010000200022

McCauley E.P., I.C. Piña, A.D. Thompson, K. Bashir, M. Weinberg, S. L. Kurz and P. Crews. 2020. Highlights of marine natural products having parallel scaffolds found from marine-derived bacteria, sponges, and tunicates. J. Antibiot., 73:504–525. https://doi.org/10.1038/s41429-020-0330-5

McClintock, J.B. and J.J. Gauthier. 1992. Antimicrobial activities of Antarctic sponges. Antarct. Sci., 4(2): 179–183. https://doi.org/10.1017/S0954102092000270

Narváez, K. 1999. Identificación y aspectos ecológicos de las esponjas del arrecife coralino de Playa Blanca, isla Gorgona (Pacífico colombiano). Tesis Biol. Mar., Univ. Valle, Cali. 57 p.

Nazemi, M., M.A. Salimi, P.A. Salimi, A. Motallebi, S.T. Jahromi and O. Ahmadzadeh. 2014. Antifungal and antibacterial activity of Haliclona sp. from the Persian Gulf, Iran. J. Mycol. Med., 24: 220– 224. https://doi.org/10.1016/j.mycmed.2014.03.005

Nuzzo, G., M.L. Ciavatta, G. Villani, E. Manzo, A. Zanfardino, M. Varcamonti and M. Gavagnin. 2012. Fulvynes, antimicrobial polyoxygenated acetylenes from the Mediterranean sponge Haliclona fulva. Tetrahedron, 68(2):754–760. https://doi.org/10.1016/j.tet.2011.10.068

O’Hara, T.D., A. Williams, S.T. Ahyong, P. Alderslade, T. Alvestad, D. Bray, I. Burghardt, N. Budaeva, F. Criscione, A.L. Crowther, M. Ekins, M. Eléaume, C.A. Farrelly1, J.K. Finn, M.N. Georgieva, A. Graham, M. Gomon, K. Gowlett-Holmes, L.M. Gunton, A. Hallan, A.M. Hosie, P. Hutchings, H. Kise, F. Köhler, J.A. Konsgrud, E. Kupriyanova, C.C. Lu, M. Mackenzie, C. Mah, H. MacIntosh, K.L. Merrin, A. Miskelly, M.L. Mitchell, K. Moore, A. Murray, P.M. O’Loughlin, H. Paxton, J.J. Pogonoski, D. Staples, J.E. Watson, R.S. Wilson, J. Zhang and N.J. Bax. 2020. The lower bathyal and abyssal seafloor fauna of eastern Australia. Mar. Biodivers. Rec., 13: 11. https://doi.org/10.1186/s41200-020-00194-1

Orhan, I.E., B. Ozcelik, B. Konuklugil, A. Putz, U.G. Kaban and P. Proksch. 2012. Bioactivity screening of the selected Turkish marine sponges and three compounds from Agelas oroides. Rec. Nat. Prod., 6(4): 356–367.

Pearse, A.S. 1932. Inhabitants of certain sponges at Dry Tortugas. Carnegie Instit. Wash., 435:117–124.

Pech-Puch, D., M. Pérez-Povedano, P. Gómez, M. Martínez-Guitián, C. Lasarte-Monterrubio, J.C. Vásquez-Ucha, M.L. Novoa-Olmedo, S. Guillén-Hernández, H. Villegas-Hernández, G. Bou, J. Rodríguez, A. Beceiro and C. Jiménez. 2020. Marine organisms from the Yucatan Peninsula (Mexico) as a potential natural source of antibacterial compounds. Mar. Drugs, 18(7):369. https://doi.org/10.3390/md18070369

Pérez, T., M.-C. Díaz, C. Ruiz, B. Cóndor-Luján, M. Klautau, E. Hajdu, G. Lobo-Hajdu, S. Zea, S.A. Pomponi, R.W. Thacker, S. Carteron, G. Tollu, A. Pouget-Cuvelier, P. Thélamon, J.-P. Marechal, O.P. Thomas, A.V. Ereskovsky, J. Vacelet and N. Boury-Esnault. 2017. How a collaborative integrated taxonomic effort has trained new spongiologists and improved knowledge of Martinique Island (French Antilles, eastern Caribbean Sea) marine biodiversity. PLoS One, 12(3): e0173859. https://doi.org/10.1371/journal.pone.0173859

Pierdacaris S., T. Vlachogianni and A. Valavanidis. 2013. Bioactive natural substances from marine sponges: new developments and prospects for future pharmaceuticals. Nat. Prod. Chem. Res., 1(3): 1000114:1–8. https://doi.org/10.4172/2329-6836.1000114

Quévrain, E., M. Roué, I. Domart-Coulon and M. Bourguet- Kondracki. 2014. Assessing the potential bacterial origin of the chemical diversity in calcareous sponges. J. Mar. Sci. Technol., 22(1):36–49. https://doi.org/10.6119/JMST-013-0718-2

Ravichandran, S., S. Wahidullahb, L. D’Souza and R.M. Anbuchezhian. 2011. Antimicrobial activity of marine sponge Clathria indica (Dendy, 1889). Russ. J. Bioorganic Chem., 37(4): 428–435. https://doi.org/10.1134/s106816201104011x

Recinos, R., U. Pinheiro, Ph. Willenz and E. Hajdu. 2020. Three new Raspailiidae Hentschel, 1923 (Axinellida, Demospongiae) from Peru. Zootaxa, 4778(3): 521–545. https://doi.org/10.11646/zootaxa.4778.3.5

Reiswig, H.M. 2002. Class Hexactinellida Schmidt, 1870: 1201–1202. In: Hooper, J.N.A. and R.W.N. van Soest. (Eds.) Systema Porifera. A guide to the classification of sponges. Kluwer Academic/Plenum Publishers, New York. 1707 p.

Ridley, S.O. 1881. XI. Spongida. Horny and siliceous sponges of Magellan Straits, S.W. Chili, and Atlantic off SW Brazil. In: Günther, A. (Ed.) Account of the Zoological Collections made during the Survey of H.M.S. ‘Alert’ in the Straits of Magellan and on the Coast of Patagonia. Proc. Zool. Soc. Lond., 107-141, pls. X-XI. https://doi.org/10.1111/j.1096-3642.1881.tb01270.x

Ridley, S.O. and A. Dendy. 1887. Report on the Monaxonida collected by H.M.S. “Challenger” during the years 1873–76. Report on the Scientific Results of the Voyage of H.M.S. Challenger during the years 1873–76. Zoology. 20 (part 59): i-lxviii, 1-275, pl. 1-51, 1 map. https://doi.org/10.5962/bhl.title.6513

Rossi, A.L., M. Farina, R. Borojevic and M. Klautau. 2006. Occurrence of five-rayed spicules in a calcareous sponge: Sycon pentactinalis sp. nov. (Porifera:Calcarea). Cah. Biol. Mar., 47(3):261–270.

Sahidin, I., C.W. Sabandar, R. Wahyuni, R. Hamsidi, M.H. Malaka, B. Sadarun and L.O. Aslan. 2018. A nor steroids from the marine sponge, Clathria species. MJAS, 22(3):375–382. https://doi.org/10.17576/mjas-2018-2203-02

Sánchez-Lozano, I., C.J. Hernández-Guerrero, M. Muñoz-Ochoa and C. Hellio. 2019. Biomimetic approaches for the development of new antifouling solutions: Study of incorporation of macroalgae and sponge extracts for the development of new environmentally friendly coatings. Int. J. Mol. Sci., 20(19): 4863. https://doi.org/10.3390/ijms20194863

San Martín, A., J. Rovirosa, I. Vaca, K. Vergara, L. Acevedo, F. Orallo and C.M. Chamy. 2011. New butyrolactone from a marine-derived fungus Aspergillus sp. J. Chil. Chem. Soc., 56(1): 625–627. https://doi.org/10.4067/S0717-97072011000100023

Santhanam, R., S. Ramesh and A. Sunilson. 2019. Biology and ecology of pharmaceutical marine sponges. CRC Press. 342 p.

Saravanakumar, K., B. Ramkumar and V. Muthuraj. 2016. In vitro antimicrobial potential efficiency of Clathria frondifera marine sponge. Int. J. Res. Pharm. Chem., 6(3):458–464. https://doi.org/10.5958/0974-360X.2020.00664.2

Selvin, J. and A.P. Lipton. 2004. Biopotentials of secondary metabolites isolated from marine sponges. Hydrobiologia, 513: 231–238. https://doi.org/10.1023/B:hydr.0000018183.92410.21

Shushizadeh, M.R., S. Behroozi, A A. Behfar and M. Nazemi. 2018. Antibacterial activity and GC-Mass analysis of organic extract from Persian Gulf Haliclona sp. Pharmacophore, 9(2): 19–24. https://pharmacophorejournal.com/3ASNkVr

Sim-Smith, C., C. Hickman Jr. and M. Kelly. 2021. New shallow-water sponges (Porifera) from the Galápagos Islands. Zootaxa, 5012(1): 1–71. https://doi.org/10.11646/zootaxa.5012.1.1

Solé-Cava, A.M., M. Klautau, N. Boury-Esnault, R. Borojevic and J.P. Thorpe. 1991. Genetic evidence for cryptic speciation in allopatric populations of two cosmopolitan species of the calcareous sponge genus Clathrina. Mar. Biol., 111(3):381–386. https://doi.org/10.1007/BF01319410

Sun, S., C.B. Canning, K. Bhargava, X. Sun, W. Zhu, N. Zhou, Y. Zhang and K. Zhou. 2015. Polybrominated diphenyl ethers with potent and broad spectrum antimicrobial activity from the marine sponge Dysidea. Bioorg. Med. Chem. Lett., 25(10):2181–2183. https://doi.org/10.1016/j.bmcl.2015.03.057

Tadesse, M, B. Gulliksen, M.B. Strøm, O.B. Styrvold and T. Haug. 2008. Screening for antibacterial and antifungal activities in marine benthic invertebrates from northern Norway. J. Invertebr. Pathol., 99(3): 286–293. https://doi.org/10.1016/j.jip.2008.06.009

Thiele, J. 1905. Die Kiesel- und Hornschwämme der Sammlung Plate. Zool. Jahrb. Suppl.6 (Fauna Chiliensis III): 407–496, 427–433.

Vacelet, J. and N. Boury-Esnault. 1995. Carnivorous sponges. Nature, 373:333–335.

van Soest, R.W.M., J.N.A. Hooper and F. Hiemstra. 1991. Taxonomy, phylogeny and biogeography of the marine sponge genus Acarnus (Porifera: Poecilosclerida). Beaufortia, 42(3): 49–88.

van Soest, R.W.M., N. Boury-Esnault, J. Vacelet, M. Dohrmann, D. Erpenbeck, N.J. de Voogd, N. Santodomingo, B. anhoorne, M. Kelly and J.N.A. Hooper. 2012. Global diversity of sponge (Porifera). PLoS One, 7(4): e35105. https://doi.org/10.1371/journal.pone.0035105

van Soest, R.W.M., N. Boury-Esnault, J.N.A. Hooper, K. Rützler, N.J. de Voogd, B. Álvarez, E. Hajdu, A.B. Pisera, R. Manconi, C. Schönberg, M. Klautau, M. Kelly, J. Vacelet, M. Dohrmann, M.C. Díaz, P. Cárdenas, J.L. Carballo, P. Ríos, R. Downey and C.C. Morrow. 2020. World Porifera database. Accessed at http://www.marinespecies.org/porifera on 2020-11-22.

Viegelmann, C., J. Parker, T. Ooi, C. Clements, G. Abbott, L. Young, J. Kennedy, A.D.W. Dobson, A.D.W. and R. Edrada-Ebel. 2014. Isolation and identification of antitrypanosomal and antimycobacterial active steroids from the sponge Haliclona simulans. Mar. Drugs, 12:2937–2952. https://doi.org/10.3390/md12052937

von Lendenfeld, R. 1910. The Sponges. 2. The Erylidae. In: Reports on the Scientific Results of the Expedition to the Eastern Tropical Pacific, in charge of Alexander Agassiz, by the U.S. Fish Commission Steamer ‘Albatross’, from October, 1904, to March, 1905, Lieut. Commander L.M. Garrett, U.S.N., Commanding, and of other Expeditions of the Albatross, 1888-1904. (21). Mem. Mus. Comp. Zoology Harv. Coll., 41(2):261–324, pls 1–8.

von Lendenfeld, R. 1915. The Sponges. 3. Hexactinellida. In: Reports on the Scientific Results of the Expedition to the Eastern Tropical Pacific, in charge of Alexander Agassiz, by the U.S. Fish Commission Steamer ‘Albatross’, from October, 1904, to March, 1905, Lieut. Commander L.M. Garrett, U.S.N., Commanding, and of other expeditions of the ‘Albatross’, 1891-1899. (29). Mem. Mus. Comp. Zoology Harv. Coll., 42(2). pls.1–109, 396 p. http://www.marinespecies.org/aphia.php?p=sourcedetails&id=7835

Vos, L., K. Rützler, N. Boury-Esnault, C. Donadey and J. Vacelet. 1991. Atlas of sponge morphology. Atlas de morphologie des éponges. Washington. Smithsonian Institution Press. 117 p.

Warsidah, Masrianih, M.S.J. Sofiana, I. Safitri, A. Sapar, A.B. Aritonang, Y. Saputri and D. Fadly. 2020. Protein isolation from sponge Niphates sp. as an antibacterial and antioxidant. Sys. Rev. Pharm. 11(9): 518–521

Wei, X., N. Henriksen, J. Skalicky, M. Harper, T. Cheatham, C. Ireland and R. Wagoner. 2011. Araiosamines A–D: Tris-bromoindole cyclic guanidine alkaloids from the marine sponge Clathria (Thalysias) araiosa. J. Org. Chem., 76(14):5515–5523. https://doi.org/10.1021/jo200327d

WHO. 2014 . Antimicrobial resistance: global report on surveillance. Technical report, World Health Organization. 232 p. https://apps.who.int/iris/handle/10665/112642

WHO. 2015 . Global Action Plan on Antimicrobial Resistance. Technical report, World Health Organization, 45 p. https://www.who.int/publications/i/item/9789241509763

Wilson, H.V. 1904. Reports on an exploration off the west coast of Mexico, Central and South America, and off the Galapagos Islands, in charge of Alexander Agassiz, by the US Fish Commission steamer” Albatross” during 1891, Lieut. Commander Z.L. Tanner, U.S.S., Commanding. XXVI. The Sponges. Mem. Mus. Comp. Zoology Harv. Coll., 30:1–164

Woo, J.K.., C.K. Kim, C. H. Ahn, D.C. Oh, K.B. Oh and J. Shin. 2015. Additional sesterterpenes and a nortriterpene saponin from the sponge Clathria gombawuiensis. J. Nat. Prod., 78(2):218–224. https://doi.org/10.1021/np500753q

Zuleta, I., M. Vitelli, R. Baggio, M. Garland, A. Seldes and J. Palermo. 2002. Novel pteridine alkaloids from the sponge Clathria sp. Tetrahedron, 58:4481–4486. https://doi.org/10.1016/S0040-4020(02)00392-7

Published

2022-10-28

How to Cite

1.
Cóndor Luján BM, Francia Quiroz JC. Sponges from Peru and their potential as source of antibacterial compounds: Las esponjas en el Perú y su potencial como fuente de compuestos antibacterianos. Bol. Investig. Mar. Costeras [Internet]. 2022 Oct. 28 [cited 2024 Nov. 22];51(2):107-28. Available from: http://boletin.invemar.org.co/ojs/index.php/boletin/article/view/1171
سرور مجازی ایران Decentralized Exchange

Issue

Section

Review Articles
فروشگاه اینترنتی