Simbiyotik Fungusların Cerambycid Türler için Önemi

Abstract

Böcekler, doğada çeşitli mikroorganizmalarla birlikte yaşamakta ve bu mikroorganizmalar böceklere, besinleri zengin hale getirmeleri, sindirimi kolaylaştırmaları, doğal düşmanlardan korumaları, böcekler arası iletişime katkıda bulunmaları, hastalık vektörlerinin etkinliklerini arttırmaları ve üreme sistemlerini düzenlemeleri gibi birçok açıdan yarar sağlamaktadır. Mikroorganizmalarla böceklerin simbiyotik ilişkisi, her iki tarafın birbirine bağımlı yaşadığı obligat mutualizmden, birbirlerinin etkisini azalttıkları veya zarar verdikleri antagonizme kadar geniş bir yelpazede etkileşimler içerisindedir. Bu kapsamda ele alınan uzun antenli böcekler (Coleoptera: Cerambycidae) ise, sindirilmesi zor bileşenler içeren odun dokusunda ömürlerinin büyük bir kısmını geçirebilecek şekilde adapte olmuştur. Bu adaptasyon, ürettiği veya bünyesine aldığı selülotik enzimler ve çeşitli mikroorganizmalarla kurduğu simbiyotik ilişkiler sayesinde meydana gelmektedir. Simbiyotik funguslar, odun dokusundaki karmaşık bileşenleri enzimatik aktivite yoluyla böceklere yararlı hale getirebilmekte ayrıca azot ve vitamin alımı, bitki sekonder metabolitlerinin detoksifikasyonu gibi çeşitli işlevsel rolleri de üstlenebilmektedir. Böceklerin simbiyotik funguslarla olan ilişkileri, onların beslenme ve hayatta kalma stratejilerini anlamak için kritik öneme sahiptir. Günümüzde birçok cerambycid türünün karantina listelerine tabi olduğu düşünüldüğünde, zararlılara karşı etkili mücadele yöntemlerinin geliştirilmesinde bu ilişkilerin anlaşılması ve bu ilişki ağının hedef alınması önemli bir katkı sağlayacaktır. Dolayısıyla, simbiyotik fungusların cerambycid türleri ile ilişkileri üzerine yapılan araştırmaların arttırılması büyük önem taşımaktadır. Bu derlemede, cerambycid türleri ile simbiyotik funguslar arasındaki ilişkileri ve bu ilişkiler sonucunda meydana gelen etkiler ele alınmıştır.

Keywords

• Cerambycidae
• Fungi
• Simbiyotik ilişki
• Uzun antenli böcek

The Importance of Symbiotic Fungi for Cerambycid Species

Abstract

In their natural habitats, insects coexist with various microorganisms that benefit them by enriching their nutrients, facilitating digestion, protecting them from natural enemies, contributing to inter-insect communication, enhancing the effectiveness of pathogen vectors’, and regulating their reproductive systems. The symbiotic relationship between microorganisms and insects encompasses a wide range of interactions, from obligate mutualism, where both parties are dependent on each other, to antagonism, where they reduce each other's effects or cause harm. Longhorn beetles (Coleoptera: Cerambycidae), which are the focus of this discussion, have adapted to spend a significant part of their lives in woody tissues containing hard-to-digest components. This adaptation occurs through the production of cellulolytic enzymes and the establishment of symbiotic relationships with various microorganisms. Symbiotic fungi can enzymatically convert complex components in woody tissues into beneficial forms for the beetles and also play functional roles such as nitrogen and vitamin acquisition and detoxification of plant secondary metabolites. The relationships between insects and symbiotic fungi are critical for understanding their feeding and survival strategies. Considering that many cerambycid species are on quarantine lists today, understanding these relationships and targeting this interaction network is crucial for developing effective pest control methods. Therefore, increasing research on the relationships between symbiotic fungi and cerambycid species is of great importance. This paper reviews the relationships between cerambycid species and symbiotic fungi and the resulting effects of these interactions.

Keywords

• Cerambycidae
• Fungi
• Symbiotic relationship
• Longhorn beetle

References

1. Douglas, A.E. (2015). Multiorganismal insects: diversity and function of resident microorganisms. Annual Review of Entomology, 60, 17–34. https://doi.org/10.1146/annurev-ento-010814-020822
2. Engel, P., Moran, N. A. (2013). The gut microbiota of insects–diversity in structure and function. FEMS Microbiology Reviews, 37(5), 699-735. https://doi.org/10.1111/1574-6976.12025
3. Mason, C.J., Campbell, A.M., Scully, E.D., Hoover, K. (2019). Bacterial and fungal midgut community dynamics and transfer between mother and brood in the Asian longhorned beetle (Anoplophora glabripennis), an invasive xylophage. Microbial Ecology, 77, 230-242. https://doi.org/10.1007/s00248-018-1205-1
4. Kaltenpoth, M., Roeser-Mueller, K., Koehler, S., Peterson, A., Nechitaylo, T.Y., Stubblefield, J.W., Herzner, G., Seger, J., Strohm, E. (2014). Partner choice and fidelity stabilize coevolution in a cretaceous-age defensive symbiosis. Proceedings of the National Academy of Sciences, 111(17), 6359-6364. https://doi.org/10.1073/pnas. 1400457111
5. Moran, N.A., Ochman, H., Hammer, T.J. (2019). Evolutionary and ecological consequences of gut microbial communities. Annu. Rev.Ecol. Evol. Syst. 50, 451–475. https://doi.org/10.1146/annurev-ecolsys-110617-062453
6. Kikuchi, Y. (2009). Endosymbiotic bacteria in insects: their diversity and culturability. Microbes and Environments, 24(3), 195-204. https://doi.org/10.1264/jsme2.ME09140S
7. Broderick, N.A., Raffa, K.F., Handelsman, J. (2006). Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc.Natl. Acad. Sci., 103(41), 15196-15199. https://doi.org/10.1073/pnas.0604865103
8. Douglas, A.E. (1989). Mycetocyte symbiosis in insects. Biol. Rev. 64, 409–34. https://doi.org/10.1111/j.1469-185X.1989.tb00682.x

9. Feldhaar, H., Straka, J., Krischke, M., Berthold, K., Stoll, S., Mueller, M. J., Gross, R. (2007). Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biology, 5, 1-11. https://doi.org/10.1186/1741-7007-5-48
10. Douglas, A.E., Minto, L.B., Wilkinson, T.L. (2001). Quantifying nutrient production by the microbial symbionts in an aphid. Journal of Experimental Biology, 204(2), 349-358 https://doi.org/10.1242/jeb.204.2.349
11. Hosokawa, T., Matsuura, Y., Kikuchi, Y., Fukatsu, T. (2016). Recurrent evolution of gut symbiotic bacteria in pentatomid stinkbugs. Zoological Letters, 2, 1-9. https://doi.org/10.1186/s40851-016-0061-4
12. Breznak, J.A., Brune, A. (1994). Role of microorganisms in the digestion of lignocellulose by termites. Annu Rev Entomol. 39 453-487.
13. Ohkuma, M. (2003). Termite symbiotic systems: efficient bio-recycling of lignocellulose. Applied Microbiology and Biotechnology, 61(1), 1-9. https://doi.org/10.1007/s00253-002-1189-z
14. Hosokawa, T., Hironaka, M., Mukai, H., Inadomi, K., Suzuki, N., Fukatsu, T. (2012). Mothers never miss the moment: a fine-tuned mechanism for vertical symbiont transmission in a subsocial insect. Animal Behaviour, 83(1), 293-300. https://doi.org/10.1016/j.anbehav.2011.11.006.
15. Bistolas, K.S., Sakamoto, R.I., Fernandes, J.A., Goffredi, S. K. (2014). Symbiont polyphyly, co-evolution, and necessity in pentatomid stinkbugs from Costa Rica. Frontiers in Microbiology, 5, 99233. https://doi.org/10.3389/fmicb.2014.00349
16. Arnett, J.R.H., Thomas, M.C., Skelley, P.E., Frank, J.H. (2002) American Beetles. Polyphaga: Scarabaeoidea through Curculionoidea. CRC Press, Boca Raton.
17. Ceriani-Nakamurakare, E.D., Slodowicz, M., Carmarán, C., Gonzalez-Audino, P. (2024). Volatile organic compounds emitted by Megaplatypus mutatus associated fungi: chemical identification and temperature-modulated responses by the ambrosial beetle. Ecological Processes, 13(1), 21. https://doi.org/10.1186/s13717-024-00490-z
18. Mahony, Z.I., Scarlett, K., Carnegie, A.J., Trollip, C., Laurence, M., Guest, D.I. (2024). Fungi associated with the ambrosia beetle Xyleborus perforans (Coleoptera: Curculionidae: Scolytinae) on drought-stressed Pinus in New South Wales, Australia. Australasian Plant Pathology, 53(1), 51-62. https://doi.org/10.1007/s13313-023-00952-6
19. Bracewell, R.R., Six, D.L. (2015). Experimental evidence of bark beetle adaptation to a fungal symbiont. Ecology and Evolution,5(21), 5109-5119. https://doi.org/10.1002/ece3.1772
20. Six, D.L. (2003). Bark beetle-fungus symbioses. Insect symbiosis, 1, 97-114.
21. Hsiau, P.T., Harrington, T.C. (2003). Phylogenetics and adaptations of basidiomycetous fungi fed upon by bark beetles (Coleoptera:Scolytidae). Symbiosis, 34, 111–131.
22. Wertman, D.L. (2024). The evolution of bark beetle–fungus mutualisms: insights from a hardwood system (Doctoral Dissertation). University of British Columbia, Forestry, Canada. p. 220.
23. Schott, J., Rakei, J., Remus-Emsermann, M., Johnston, P., Mbedi, S., Sparmann, S., Hilker, M., Paniagua Voirol, L.R.(2024). Microbial associates of the elm leaf beetle: uncovering the absence of resident bacteria and the influence of fungion insect performance. App. and Env.l Microbio., 90(1), e01057-23. https://doi.org/10.1128/aem.01057-23
24. Kushiyev, R., Tuncer, C., Erper, I., Özer, G. (2021). The utility of Trichoderma spp. isolates to control of Xylosandrus germanus Blandford (Coleoptera: Curculionidae: Scolytinae). Jour. of Pla. Dis. and Pro., 128, 153-160. https://doi.org/10.1007/s41348-020-00375-1
25. Gugliuzzo, A., Aiello, D., Biondi, A., Giurdanella, G., Siscaro, G., Zappalà, L., Vitale, A., Garzia, G.T., Polizzi, G. (2022). Microbial mutualism suppression by Trichoderma and Bacillus species for controlling the invasive ambrosia beetle Xylosandrus compactus. Biological Control, 170, 104929. https://doi.org/10.1016/j.biocontrol.2022.104929
26. Grünwald, S., Pilhofer, M., Höll, W. (2010). Microbial associations in gut systems of wood-and bark-inhabiting longhornedbeetles [Coleoptera: Cerambycidae]. Systematic and Applied Microbiology, 33(1), 25-34. https://doi.org/10.1016/j.syapm.2009.10.002
27. Mohammed, W.S., Ziganshina, E.E., Shagimardanova, E.I., Gogoleva, N.E., Ziganshin, A.M. (2018). Comparison of intestinal bacterial and fungal communities across various xylophagous beetle larvae (Coleoptera: Cerambycidae). ScientificReports, 8(1), 10073. https://doi.org/10.1038/s41598-018-27342-z
28. Wang, Q. (Ed.) (2017). Cerambycidae of the world: biology and pest management. CRC press, Boca Raton.
29. Yanega, D. (1996). Field guide to northeastern longhorned beetles (Coleoptera: Cerambycidae). Illinois Natural HistorySurvey, Illinois.
30. Haack, R.A. (1987). Nutritional ecology of wood-feeding Coleoptera, Lepidoptera, and Hymenoptera. Nutritional Ecology of İnsects, Mites, Spiders, And Related İnvertebrates, 449-486.
31. Haack, R.A., Slansky, F. (1987). Nutritional ecology of wood-feeding Coleoptera, Lepidoptera, and Hymenoptera. In: Nutritional ecology of insects, mites, and spiders (pp. 449–486) Slansky, F., Rodriguez, J.G. (eds.). Wiley, New York.
32. Linnakoski, R., Kasanen, R., Lasarov, I., Marttinen, T., Oghenekaro, A. O., Sun, H., Asiegbu, F.O.,Wingfield, M.J., Hantula,J., Heliövaara, K. (2018). Cadophora margaritata sp. nov. and other fungi associated with the longhorn beetles Anoplophoraglabripennis and Saperda carcharias in Finland. Antonie Van Leeuwenhoek, 111(11), 2195-2211. https://doi.org/10.1007/ s10482-018-1112-y
33. Joseph, R., Keyhani, N.O. (2021). Fungal mutualisms and pathosystems: life and death in the ambrosia beetle mycangia. Applied Microbiology and Biotechnology, 105, 3393-3410. https://doi.org/10.1007/s00253-021-11268-0
34. Martin, M.M. (1992). The evolution of insect-fungus associations: from contact to stable symbiosis. American Zoologist, 32(4),593-605. https://doi.org/10.1093/icb/32.4.593
35. Kukor, J.J., Martin, M.M. (1986). Cellulose digestion in Monochamus marmorator Kby. (Coleoptera: Cerambycidae): roleof acquired fungal enzymes. Journal of Chemical Ecology, 12, 1057-1070. https://doi.org/10.1007/BF01638996
36. Kim, J.M., Choi, M.Y., Kim, J.W., Lee, S.A., Ahn, J.H., Song, J., Kim, S.H., Weon, H.Y. (2017). Effects of diet type, developmental stage, and gut compartment in the gut bacterial communities of two Cerambycidae species (Coleoptera). Journalof Microbiology, 55, 21-30. https://doi.org/10.1007/s12275-017-6561-x
37. Delalibera, Jr,I., Handelsman, J.O., Raffa, K.F. (2005). Contrasts in cellulolytic activities of gut microorganisms between thewood borer, Saperda vestita (Coleoptera: Cerambycidae), and the bark beetles, Ips pini and Dendroctonus frontalis(Coleoptera: Curculionidae). Environmental entomology, 34(3), 541-547. https://doi.org/10.1603/0046-225X-34.3.541
38. Ayayee, P., Rosa, C., Ferry, J.G., Felton, G., Saunders, M., Hoover, K. (2014). Gut microbes contribute to nitrogen provisioning in a wood-feeding cerambycid. Environmental Entomology, 43(4), 903-912. https://doi.org/10.1603/EN14045
39. Abo-Khatwa, N. (1978). Cellulase of fungus-growing termites: a new hypothesis on its origin. Experientia, 34(5), 559-560.https://doi.org/10.1007/BF01936956
40. Martin, M.M., Martin, J.S. (1978). Cellulose digestion in the midgut of the fungus-growing termite Macrotermes natalensis: the role ofacquired digestive enzymes. Science, 199(4336), 1453-1455. DOI: 10.1126/science.199.4336.1453
41. Kukor, J.J., Martin, M.M. (1983). Acquisition of digestive enzymes by siricid woodwasps from their fungal symbiont.Science, 220(4602), 1161-1163. DOI: 10.1126/science.220.4602.1161
42. Martin, M.M. (1987). Invertebrate-microbial ınteractions: ıngested fungal enzymes in arthropod biology. Cornell University Press,Ithaca and London.[43] Kukor, J.J., Martin, M.M. (1986). The trans- formation of Saperda calcarata (Coleoptera: Cerambycidae) into acellulose digester through the inclusion of fungal enzymes in its diet. Oecologia 71:138-141. https://doi.org/10.1007/BF00377333
43. Kukor, J.J., Cowan, D.P., Martin, M.M. (1988). The role of ingested fungal enzymes in cellulose digestion in the larvae of cerambycidbeetles. Physiological Zoology, 61(4), 364-371. ttps://doi.org/10.1086/physzool.61.4.30161254
44. Geib, S.M., Scully, E.D., Jimenez-Gasco, M.D.M., Carlson, J.E., Tien, M., Hoover, K. (2012). Phylogenetic analysis of Fusariumsolani associated with the Asian longhorned beetle, Anoplophora glabripennis. Insects, 3(1), 141-160. https://doi.org/10.3390/insects3010141
45. Geib, S.M., Filley, T.R., Hatcher, P.G., Hoover, K., Carlson, J.E., Jimenez-Gasco, M.D.M., Nakagawa-Izumi, A., Sleighter, R.L., Tien,M. (2008). Lignin degradation in wood-feeding insects. Proceedings of the National Academy of Sciences, 105(35), 12932-12937.https://doi.org/10.1073/pnas.0805257105
46. Scully, E.D., Hoover, K., Carlson, J., Tien, M., Geib, S.M. (2012). Proteomic analysis of Fusarium solani isolated from the Asianlonghorned beetle, Anoplophora glabripennis. PloS one, 7(4), e32990. https://doi.org/10.1371/journal.pone.0032990
47. Calderon, O., Berkov, A. (2012). Midgut and fat body bacteriocytes in neotropical cerambycid beetles (Coleoptera: Cerambycidae).Environmental Entomology, 41(1), 108-117. https://doi.org/10.1603/EN11258
48. Kishigami, M., Matsuoka, F., Maeno, A., Yamagishi, S., Abe, H., Toki, W. (2023). Yeast associated with flower longicorn beetleLeptura ochraceofasciata (Cerambycidae: Lepturinae), with implication for its function in symbiosis. Plos one, 18(3), e0282351. https://doi.org/10.1371/journal.pone.0282351
49. Schomann, H. (1937). Die symbiose der bockkäfer. Zeitschrift für Morphologie und Ökologie der Tiere, 32, 542-612.
50. Heitz, E. (1927). Über intrazelluläre symbiose bei holzfressenden käferlarven I. Zeitschrift für Morphologie und Ökologie der Tiere, 7,279-305.
51. Chararas, C., Pignal, M. C., Vodjdani, G. and Bourgeay-Causse, M. (1983). Glycosidases and B group vitamins produced by six yeaststrains from the digestive tract of Phoracantha semipunctata larvae and their role in the insect development. Mycopathologia, 83, 9-15.https://doi.org/10.1007/BF00437405