Ophiocordyceps : Fungi Entomopatogen Penyebab Zombie Pada Serangga

Ivan Permana Putra(1*)

(1) Division of Mycology, Department of Biology, IPB University
(*) Corresponding Author

Abstract

Ophiocordyceps is special type of entomopathogenic fungi which well known to infect insects and turning them into zombie. A total of 250 species have been described from its genus, and some are known to control their hosts, which are most notably ants. They are ubiquitous within tropical rain forests across the board, with few publication reports from temperate ecosystems. These fungal pathogens possess the capacity to manipulate host behaviour in order to increase their own fitness. These entomopathogenic fungi cause their hosts frezee to die in an exposed area on the abaxial surface of leaves or branches, which then enhancing the fungus spore production and dispersal. Despite the high diversity of fungi and insect with vast tropical forest as well as drugs potency from Ophiocordyceps, publication of Ophiocordyces was rarely reported from Indonesia. This review will explain the evolution of Ophiocordyceps-insect interaction, simbiont distribution, and zombie-insect formation mechanism, in order to induce zombie-insect research in Indonesia. 

Keywords

Fungi, Insect, Ophiocordyceps, Zombie, Indonesia

References

Andersen, S. B., Gerritsma, S., Yusah, K. M., Mayntz, D., Hywel‐Jones, N. L., Billen, J., … Hughes, D. P. 2009. The Life of a Dead Ant: The Expression of an Adaptive Extended Phenotype. The American Naturalist, 174(3), 424–433. Available at: http://dx.doi.org/10.1086/603640

Araújo, J. P. M., & Hughes, D. P. 2016. Diversity of Entomopathogenic Fungi. Advances in Genetics, 1–39. Available at: http://dx.doi.org/10.1016/bs.adgen.2016.01.001.

Araújo, J. P. M., Evans, H. C., Kepler, R., & Hughes, D. P. 2018. Zombie-ant fungi across continents: 15 new species and new combinations within Ophiocordyceps, I. Myrmecophilous hirsutelloid species. Studies in Mycology, 90, 119–160. Available at: http://dx.doi.org/10.1016/j.simyco.2017.12.002.

Araújo, J. P. M., & Hughes, D. P. 2019. Zombie-Ant Fungi Emerged from Non-manipulating, Beetle-Infecting Ancestors. Current Biology, 29(21), 3735–3738. Available at: http://dx.doi.org/10.1016/j.cub.2019.09.004.

Barbosa, B. C., Halfeld, V. R., de Araújo, J. P. M., Maciel, T. T., & Prezoto, F. 2015. Record ofOphiocordyceps unilateralis sensu lato, the zombie-ant fungus, parasitizing Camponotusin an urban fragment of Atlantic Rainforest in southeastern Brazil. Studies on Neotropical Fauna and Environment, 50(1), 21–23. Available at: http://dx.doi.org/10.1080/01650521.2014.991213.

Chicco, G. 2011. Ant Colony System-Based Applications to Electrical Distribution System Optimization. Ant Colony Optimization - Methods and Applications. Available at: http://dx.doi.org/10.5772/13840.

De Bekker, C., Ohm, R. A., Loreto, R. G., Sebastian, A., Albert, I., Merrow, M., Hughes, D. P. 2015. Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. BMC Genomics, 16(1). Available at: http://dx.doi.org/10.1186/s12864-015-1812-x.

De Bekker, C., Ohm, R. A., Evans, H. C., Brachmann, A., & Hughes, D. P. 2017. Ant-infecting Ophiocordyceps genomes reveal a high diversity of potential behavioral manipulation genes and a possible major role for enterotoxins. Scientific Reports, 7(1): 1-13. Available at: http://dx.doi.org/10.1038/s41598-017-12863-w.

Dong, C.-H., & Yao, Y.-J. 2008. In vitro evaluation of antioxidant activities of aqueous extracts from natural and cultured mycelia of Cordyceps sinensis. LWT - Food Science and Technology, 41(4), 669–677. Available at: http://dx.doi.org/10.1016/j.lwt.2007.05.002.

Evans, H. C., Elliot, S. L., & Hughes, D. P. 2011. Hidden Diversity Behind the Zombie-Ant Fungus Ophiocordyceps unilateralis: Four New Species Described from Carpenter Ants in Minas Gerais, Brazil. PLoS ONE, 6(3), 1-9. Available at: http://dx.doi.org/10.1371/journal.pone.0017024.

Ginting, L. A., Oemry, S., Lubis, L. 2015. Uji Patogenitas Jamur Cordyceps militaris L. terhadap Ulat Api (Setothosea asigna E.) (Lepidoptera: Limacodidae) di Rumah Kasa. Jurnal Online Agroekoteknologi, 3(2),785-789.

Halimah, N., Imaningsih, W., & Mariana, M. 2018. Karakterisasi morfologi jamur entomopatogen di Hutan Mandiangin Banjarbaru, Kalimantan Selatan. Jurnal Mikologi Indonesia, 2(1), 39. Available at: http://dx.doi.org/10.46638/jmi.v2i1.39.

Hughes, D. P., Evans, H. C., Hywel-Jones, N., Boomsma, J. J., & Armitage, S. A. O. 2009. Novel fungal disease in complex leaf-cutting ant societies. Ecological Entomology, 34(2), 214–220. Available at: http://dx.doi.org/10.1111/j.1365-2311.2008.01066.x.

Hughes, D. P., Andersen, S. B., Hywel-Jones, N. L., Himaman, W., Billen, J., & Boomsma, J. J. 2011. Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecology, 11(1), 13. Available at: http://dx.doi.org/10.1186/1472-6785-11-13.

Indrayani, I., Soetopo, D., Hartono,J. 2013. Efektivitas Formula Jamur Beauveria Bassiana Dalam Pengendalian Penggerek Buah Kapas (Helicoverpa Armigera). J. Littri, 19(4), 178-185.

Ismanto, A., & Sukartana, P. 2016. Uji efektivitas isolat jamur entomopatogen Metarhizium anisopliae (Metsch.) Sorokin terhadap rayap tanah pada pengujian di laboratorium dan lapangan. Jurnal Penelitian Hasil Hutan, 34(4), 261–268. Available at: http://dx.doi.org/10.20886/jphh.2016.34.4.261-268.

Ji, D.-B., Ye, J., Li, C.-L., Wang, Y.-H., Zhao, J., & Cai, S.-Q. 2009. Antiaging effect of Cordyceps sinensis extract. Phytotherapy Research, 23(1), 116–122. Available at: http://dx.doi.org/10.1002/ptr.2576 .

Joop, G., & Vilcinskas, A. 2016. Coevolution of parasitic fungi and insect hosts. Zoology, 119(4), 350–358. Available at: http://dx.doi.org/10.1016/j.zool.2016.06.005.

Kobayasi Y. 1941. The genus Cordyceps and its allies. Science reports of the Tokyo Bunrika Daigaku 84: 53-260.

Kobmoo, N., Mongkolsamrit, S., Tasanathai, K., Thanakitpipattana, D., & Luangsa-Ard, J. J. 2012. Molecular phylogenies reveal host-specific divergence of Ophiocordyceps unilateralis sensu latofollowing its host ants. Molecular Ecology, 21(12), 3022–3031. Available at: http://dx.doi.org/10.1111/j.1365-294x.2012.05574.x.

Kobmoo, N., Mongkolsamrit, S., Wutikhun, T., Tasanathai, K., Khonsanit, A., Thanakitpipattana, D., & Luangsa-Ard, J. J. 2015. New species of Ophiocordyceps unilateralis, an ubiquitous pathogen of ants from Thailand. Fungal Biology, 119(1), 44–52. Available at: http://dx.doi.org/10.1016/j.funbio.2014.10.008.

Koh, J.-H., Kim, J.-M., Chang, U.-J., & Suh, H.-J. 2003. Hypocholesterolemic Effect of Hot-Water Extract from Mycelia of Cordyceps sinensis. Biological & Pharmaceutical Bulletin, 26(1), 84–87. Available at: http://dx.doi.org/10.1248/bpb.26.84.

Lichtwardt, R. W. (n.d.). 2001. Trichomycetes: Fungi in Relationship with Insects and Other Arthropods. Symbiosis, 575–588. Available at: http://dx.doi.org/10.1007/0-306-48173-1_36.

Li, Y., Wang, X.-L., Jiao, L., Jiang, Y., Li, H., Jiang, S.-P., Yao, Y.-J. 2011. A survey of the geographic distribution of Ophiocordyceps sinensis. The Journal of Microbiology, 49(6), 913–919. Available at: http://dx.doi.org/10.1007/s12275-011-1193-z.

Luangsa-ard, J., Tasanathai, K., Thanakitpipattana, D., Khonsanit, A., & Stadler, M. 2018. Novel and interesting Ophiocordyceps spp. (Ophiocordycipitaceae, Hypocreales) with superficial perithecia from Thailand. Studies in Mycology, 89, 125–142. Available at: http://dx.doi.org/10.1016/j.simyco.2018.02.001.

Mangold, C. A., Ishler, M. J., Loreto, R. G., Hazen, M. L., & Hughes, D. P. 2019. Zombie ant death grip due to hypercontracted mandibular muscles. The Journal of Experimental Biology, 222(14):2-9. Available at: http://dx.doi.org/10.1242/jeb.200683.

Mongkolsamrit, S., Kobmoo, N., Tasanathai, K., Khonsanit, A., Noisripoom, W., Srikitikulchai, P., … Luangsa-ard, J. J. 2012. Life cycle, host range and temporal variation of Ophiocordyceps unilateralis/Hirsutella formicarum on Formicine ants. Journal of Invertebrate Pathology, 111(3), 217–224. Available at: http://dx.doi.org/10.1016/j.jip.2012.08.007.

Mueller, U. G., Schultz, T. R., Currie, C. R., & Malloch, D. 2001. The Origin of the Attine Ant-Fungus Mutualism. The Quarterly Review of Biology, 76(2), 169-197. Available at: http://dx.doi.org/10.1086/393867.

Mueller, U. G., & Gerardo, N. 2002. Fungus-farming insects: Multiple origins and diverse evolutionary histories. Proceedings of the National Academy of Sciences, 99(24), 15247-15249. Available at: http://dx.doi.org/10.1073/pnas.242594799.

Mueller, U.G, Gerardo, N.M, Aanen, D.K, Six D.L, Schultz, T.R. 2005. The evolution of agriculture in insects. Annu Rev Ecol Evol Syst 36: 563-595.

Mueller, U.G., Ortiz, A. & Bacci, M. 2010. Planting of fungus onto hibernating workers of the fungus-growing ant Mycetosoritis clorindae (Attini, Formicidae). Insectes Sociaux, 57(2), pp.209-215. Available at: http://dx.doi.org/10.1007/s00040-010-0072-7.

Pontoppidan, M.-B., Himaman, W., Hywel-Jones, N. L., Boomsma, J. J., & Hughes, D. P. 2009. Graveyards on the Move: The Spatio-Temporal Distribution of Dead Ophiocordyceps-Infected Ants. PLoS ONE, 4(3):1-10. Available at: http://dx.doi.org/10.1371/journal.pone.0004835.

Quandt, C. A., Kepler, R. M., Gams, W., Araújo, J. P. M., Ban, S., Evans, H. C., … Spatafora, J. W. 2014. Phylogenetic-based nomenclatural proposals for Ophiocordycipitaceae (Hypocreales) with new combinations in Tolypocladium. IMA Fungus, 5(1), 121–134. Available at: http://dx.doi.org/10.5598/imafungus.2014.05.01.12.

Rosmiati, A., Hidayat, C., Firmansyah, E., & Setiati, Y. 2018. Potensi Beauveria bassiana sebagai Agens Hayati Spodoptera litura Fabr. pada Tanaman Kedelai. Agrikultura, 29(1), 43. Available at: http://dx.doi.org/10.24198/agrikultura.v29i1.16925.

Sasaki, F., Miyamoto, T., Yamamoto, A., Tamai, Y., & Yajima, T. 2012. Relationship between intraspecific variations and host insects of Ophiocordyceps nutans collected in Japan. Mycoscience, 53(2), 85–91. Available at: http://dx.doi.org/10.1007/s10267-011-0137-0.

Somavilla, A., Barbosa, B. C., Prezoto, F., & Oliveira, M. L. 2019. Infection and behavior manipulation of social wasps (Vespidae: Polistinae) by Ophiocordyceps humbertii in Neotropical forests: new records of wasp-zombification by a fungus. Studies on Neotropical Fauna and Environment, 55(1), 23–28. Available at: http://dx.doi.org/10.1080/01650521.2019.1691908.

Stork, N. E. 2018. How Many Species of Insects and Other Terrestrial Arthropods Are There on Earth? Annual Review of Entomology, 63(1), 31–45. Available at: http://dx.doi.org/10.1146/annurev-ento-020117-043348.

Sung, G.-H., Hywel-Jones, N. L., Sung, J.-M., Luangsa-ard, J. J., Shrestha, B., & Spatafora, J. W. 2007. Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Studies in Mycology, 57, 5–59. Available at: http://dx.doi.org/10.3114/sim.2007.57.01.

Sung, G.-H., Poinar, G. O., & Spatafora, J. W. 2008. The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal–arthropod symbioses. Molecular Phylogenetics and Evolution, 49(2), 495–502. Available at: http://dx.doi.org/10.1016/j.ympev.2008.08.028.

Tasanathai, K., Noisripoom, W., Chaitika, T., Khonsanit, A., Hasin, S., & Luangsa-ard, J. 2019. Phylogenetic and morphological classification of Ophiocordyceps species on termites from Thailand. MycoKeys, 56, 101–129. Available at: http://dx.doi.org/10.3897/mycokeys.56.37636.

Turnip, A., Runtuboi, D. Y. P., & Lantang, D. 2018. Uji Efektivitas Jamur Beauveria bassiana dan Waktu Aplikasi Terhadap Hama Spodoptera litura Pada Tanaman Sawi Hijau (Brassica juncea). JURNAL BIOLOGI PAPUA, 10(1). Available at: http://dx.doi.org/10.31957/jbp.131.

Wu, Y., Ishurd, O., Cuirong, S., & Yuanjiang, P. 2005. Structure Analysis and Antitumor Activity of (1→3)-β-D-Glucans (Cordyglucans) from the Mycelia of Cordyceps sinensis. Planta Medica, 71(4), 381–384. Available at: http://dx.doi.org/10.1055/s-2005-864111.

Wu, Y., Sun, H., Qin, F., Pan, Y., & Sun, C. 2006. Effect of various extracts and a polysaccharide from the edible mycelia of Cordyceps sinensis on cellular and humoral immune response against ovalbumin in mice. Phytotherapy Research, 20(8), 646–652. Available at: http://dx.doi.org/10.1002/ptr.1921

Yao, Y.-J., & Wang, X.-L. 2011. Host insect species of Ophiocordyceps sinensis: a review. ZooKeys, 127, 43–59. Available at: http://dx.doi.org/10.3897/zookeys.127.802.

Zhang, G., Huang, Y., Bian, Y., Wong, J. H., Ng, T. B., & Wang, H. 2006. Hypoglycemic activity of the fungi Cordyceps militaris, Cordyceps sinensis, Tricholoma mongolicum, and Omphalia lapidescens in streptozotocin-induced diabetic rats. Applied Microbiology and Biotechnology, 72(6), 1152–1156. Available at: http://dx.doi.org/10.1007/s00253-006-0411-9.

Zhou, C., Yang, G., Honghui, L., Xiaoling, Y., Shan, L., Yunguo, Z., Jiakuan, C. 2007. Phyolgenetic relationships of host insects of Cordyceps sinensis inferred from mitochondrial Cytochrome b sequences. Progress in Natural Science, 17(7), 789–797. Available at: http://dx.doi.org/10.1080/10002007088537474.

DOI: 10.23917/bioeksperimen.v7i2.11152

Article Metrics

Abstract view(s): 1825 time(s)
PDF (Bahasa Indonesia): 408 time(s)

Refbacks

  • There are currently no refbacks.