The Mycobiome of The Gut of Willow Wood Borer, Xiphydria Prolongata (Hymenoptera: Xiphydriidae): A Rich Source of Rare Yeasts

Year 2024, Volume: 29 Issue: 1, 45 - 52, 30.04.2024

Özgül Doğan , Ertan Mahir Korkmaz , Mahir Budak

https://doi.org/10.53433/yyufbed.1373533

Abstract

A high-throughput amplicon sequencing as a culture-independent approach was used to identify the gut mycobiome of the willow wood borer Xiphydria prolongata. The findings of this study are significant in terms of the insect-fungal interactions and indicate the unexpected richness of the mycobiome and the presence of many rare yeast species in the wood borer gut. A total of 40 fungal genera were found, and among them, only one endophytic fungus, Daldinia (Hypoxylaceae), has been previously reported in Xiphydria. Zygosaccharomyces siamensis is the most prevalent ascomycete species, while Rhodosporidiobolus colostri is the most abundant basidiomycetous yeast in X. prolongata. Some of the species identified here were known as very rare fungi such as Skoua fertilis, Chaetomium nepalense, R. colostri, and Vustinia terrae. This study is also the first report on S. fertilis and V. terrae in the insect gut flora. These funguses most likely aid in the digestion of lignocellulose in the gut of wood borer. Therefore, further research is required to know the source of acquisition and functional role of these yeast and their industrial potential.

Keywords

Endosymbiosis, Insect-fungal interactions, ITS1, Metabarcoding, Willow wood borer, Yeasts

Project Number

F-614

Odun Arısı Xiphydria Prolongata'nın (Hymenoptera: Xiphydriidae) Bağırsak Mikobiyomu: Nadir Mayalar İçin Zengin Bir Kaynak

Abstract

Söğüt odun arısı Xiphydria prolongata'nın bağırsak mikobiyomunu tanımlamak için kültürden bağımsız bir yaklaşım olarak yüksek verimli amplikon dizileme kullanılmıştır. Bu çalışmanın bulguları böcek-fungal etkileşimleri açısından önem taşımakta ve mikobiyomun beklenmedik zenginliğini ve ağaç kurdu bağırsağında birçok nadir maya türünün varlığını göstermektedir. Toplam 40 mantar cinsi bulunmuştur ve bunlar arasında sadece biri endofitik mantar olan Daldinia (Hypoxylaceae) daha önce Xiphydria'da rapor edilmiştir. Zygosaccharomyces siamensis en yaygın askomiset türü iken, Rhodosporidiobolus colostri X. prolongata'da en bol bulunan bazidiomiset mayadır. Tanımlanan türlerden Skoua fertilis, Chaetomium nepalense, R. colostri ve Vustinia terrae çok nadir bulunan mantarlar olarak bilinmektedir. Bu çalışma aynı zamanda S. fertilis ve V. terrae'nın böcek bağırsak florasındaki ilk raporudur. Bu funguslar büyük olasılıkla odun kurdunun bağırsağındaki lignoselülozun sindirimine yardımcı olmaktadır. Bu nedenle, bu mayaların elde edilme kaynağı ve işlevsel rolü ile endüstriyel potansiyellerinin bilinmesi için daha fazla araştırma yapılması gerekmektedir.

Keywords

Böcek-mantar etkileşimleri, Endosimbiyoz, ITS1, Mayalar, Metabarkodlama, Odun arıları

Ethical Statement

The author declares no conflicts of interest.

Supporting Institution

Sivas Cumhuriyet University BAP (CÜBAP)

Project Number

F-614

Thanks

The members of Evolutionary Bioinformatics Research Groups (EBRG) from Sivas Cumhuriyet University are thanked for their contributions in laboratory work.

References

• Amir, A., McDonald, D., Navas-Molina, J. A., Kopylova, E., Morton, J. T., Zech Xu, Z., …, & Knight, R. (2017). Deblur rapidly resolves single-nucleotide community sequence patterns. MSystems, 2(2), e00191-16. doi:10.1128/mSystems.00191-16
• Bai, L., He, L., Yu, P., Luo, J., Yang, M., Xiangren, A., & Xiaoxing, W. (2020). Molecular characterization of mycobiota and Aspergillus species from Eupolyphaga sinensis Walker based on high-throughput sequencing of ITS1 and CaM. Journal of Food Quality, 2020, Article ID 1752415. doi:10.1155/2020/1752415
• Brentassi, M. E., Medina, R., de la Fuente, D., Franco, M. EE., Toledo, A. V., Saparrat, M. CN., & Balatti, P. A. (2020). Endomycobiome associated with females of the planthopper Delphacodes kuscheli (Hemiptera: Delphacidae): A metabarcoding approach. Heliyon, 6(8), e04634. doi:10.1016/j.heliyon.2020.e04634
• Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581-583. doi:10.1038/nmeth.3869
• Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., & Madden, T. L. (2009). BLAST+: architecture and applications. BMC Bioinformatics, 10(1), 421. doi:10.1186/1471-2105-10-421
• Chikano, M., & Takahashi, J. (2020). Complete mitochondrial DNA sequence of the yeast Zygosaccharomyces siamensis (Saccharomycetes: Saccharomycetales) from fermented honey of the Apis cerana japonica in Japan. Mitochondrial DNA Part B, 5(3), 2645-2647. doi:10.1080/23802359.2020.1785961
• Douglas, A. E. (2015). Multiorganismal insects: diversity and function of resident microorganisms. Annual Review of Entomology, 60, 17-34. doi:10.1146/annurev-ento-010814-020822
• Fujii, K., Ikeda, K., & Yoshida, S. (2012). Isolation and characterization of aerobic microorganisms with cellulolytic activity in the gut of endogeic earthworms. International Microbiology: The Official Journal of the Spanish Society for Microbiology, 15(3), 121-130. doi:10.2436/20.1501.01.165
• Ilmi, M., Badrani, A., & Fauziyah, A. (2023). Increasing lipid production from Zygosaccharomyces siamensis AP1 in molasses substrate using sequencing batch method. Preparative Biochemistry & Biotechnology, 53(3), 288-296. doi:10.1080/10826068.2022.2081859
• Johansson, N., & Larsson, A. (2020). Xiphydria betulae (Enslin, 1911) new to Sweden and new records of Xiphydria picta Konow, 1897 (Hymenoptera: Xiphydriidae) with additional notes on two rare ichneumonid parasitoids associated with xiphydriid wood wasps. Entomologisk Tidskrift, 140(3-4), 145-155.
• Kachalkin, A. V., Turchetti, B., Inácio, J., Carvalho, C., Mašínová, T., Pontes, A., …, & Yurkov, A. M. (2019). Rare and undersampled dimorphic basidiomycetes. Mycological Progress, 18(7), 945-971. doi:10.1007/s11557-019-01491-5
• Kim, J. A., Jeon, J., Park, S.-Y., Jeon, M. J., Yeo, J.-H., Lee, Y.-H., & Kim, S. (2020). Draft genome sequence of Daldinia childiae JS-1345, an endophytic fungus isolated from stem tissue of Korean fir. Microbiology Resource Announcements, 9(14). doi:10.1128/MRA.01284-19
• Kim, J., Ko, H., Hur, J.-S., An, S., Lee, J. W., Deyrup, S. T., Noh, M., & Shim, S. H. (2022). Discovery of pan-peroxisome proliferator-activated receptor modulators from an endolichenic fungus, Daldinia childiae. Journal of Natural Products, 85(12), 2804-2816. doi:10.1021/acs.jnatprod.2c00791
• Kõljalg, U., Nilsson, H. R., Schigel, D., Tedersoo, L., Larsson, K.-H., May, T. W., …, & Abarenkov, K. (2020). The taxon hypothesis paradigm-on the unambiguous detection and communication of taxa. Microorganisms, 8(12), 1910. doi:10.3390/microorganisms8121910
• Lewis, Z., & Lizé, A. (2015). Insect behaviour and the microbiome. Current Opinion in Insect Science, 9, 86-90. doi:10.1016/j.cois.2015.03.003
• Lin, W., Wang, P., Hsieh, S., Tsai, C., & Hsiao, S. (2018). Yeasts associated with Euploea butterflies. Mycosphere, 9(1), 149-154. doi:10.5943/mycosphere/9/1/4
• Malacrinò, A., Schena, L., Campolo, O., Laudani, F., & Palmeri, V. (2015). Molecular analysis of the fungal microbiome associated with the olive fruit fly Bactrocera oleae. Fungal Ecology, 18, 67-74. doi:10.1016/j.funeco.2015.08.006
• Margesin, R., Ludwikowski, T. M., Kutzner, A., & Wagner, A. O. (2022). Low-temperature biodegradation of lignin-derived aromatic model monomers by the cold-adapted yeast Rhodosporidiobolus colostri isolated from Alpine forest soil. Microorganisms, 10(3), 515. doi:10.3390/microorganisms10030515
• Masiulionis, V. E., & Pagnocca, F. C. (2017). Rhodosporidiobolus geoffroeae sp. nov., a basidiomycetous yeast isolated from the waste deposit of the attine ant Acromyrmex lundii. International Journal of Systematic and Evolutionary Microbiology, 67(4), 1028-1032. doi:10.1099/ijsem.0.001738
• Miller, S. A., Dykes, D. D., & Polesky, H. F. (1988). A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Research, 16(3), 1215-1215. doi:10.1093/nar/16.3.1215
• Pažoutová, S., Šrůtka, P., Holuša, J., Chudíčková, M., & Kolařík, M. (2010). Diversity of xylariaceous symbionts in Xiphydria woodwasps: role of vector and a host tree. Fungal Ecology, 3(4), 392-401. doi:10.1016/j.funeco.2010.07.002
• Pažoutová, S., Follert, S., Bitzer, J., Keck, M., Surup, F., Šrůtka, P., Holuša, J., & Stadler, M. (2013). A new endophytic insect-associated Daldinia species, recognised from a comparison of secondary metabolite profiles and molecular phylogeny. Fungal Diversity, 60(1), 107-123. doi:10.1007/s13225-013-0238-5
• R Core Team. (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing: Vienna, Austria. https://www.R-project.org/
• Saksinchai, S., Suzuki, M., Chantawannakul, P., Ohkuma, M., & Lumyong, S. (2012). A novel ascosporogenous yeast species, Zygosaccharomyces siamensis, and the sugar tolerant yeasts associated with raw honey collected in Thailand. Fungal Diversity, 52(1), 123-139. doi:10.1007/s13225-011-0115-z
• Samal, D., Sethy, J., & Sahu, H. (2014). Isolate of fungi associated with dead honey bee. Journal of Wildlife Research, 2(4), 31-38.
• Smith, D. R. (1976). The xiphydriid woodwasps of North America (Hymenoptera : Xiphydriidae). American Entomological Society, 102(2), 101-131.
• Smith, D. R. (1983). Xiphydria prolongata (Geoffroy) (Hymenoptera: Xiphydriidae) adventive in North America. Proceedings- Entomological Society of Washington, 85, 860-861.
• Smith, D. R. (2008). Xiphydriidae of the Philippines, Insular Malaysia, Indonesia, Papua New Guinea, New Caledonia, and Fiji (Hymenoptera). Beiträge Zur Entomologie=Contributions to Entomology, 58(1), 15-95. doi:10.21248/contrib.entomol.58.1.15-95
• Šrůtka, P., Pažoutová, S., & Kolařík, M. (2007). Daldinia decipiens and Entonaema cinnabarina as fungal symbionts of Xiphydria wood wasps. Mycological Research, 111(2), 224-231. doi:10.1016/j.mycres.2006.10.006
• Taeger, A., Liston, A. D., Prous, M., Groll, E. K., Gehroldt, T., & Blank, S. M. (2018). ECatSym – Electronic World Catalog of Symphyta (Insecta, Hymenoptera). Program version 5.0 (19 Dec 2018), data version 40 (23 Sep 2018). Senckenberg Deutsches Entomologisches Institut (SDEI), Müncheberg. https://sdei.de/ecatsym/ Access Date: 15 Feb 2020.
• Theelen, B., Cafarchia, C., Gaitanis, G., Bassukas, I. D., Boekhout, T., & Dawson, T. L. (2018). Malassezia ecology, pathophysiology, and treatment. Medical Mycology, 56(suppl_1), S10-S25. doi:10.1093/mmy/myx134
• Vega, F. E., & Biedermann, P. H. W. (2020). On interactions, associations, mycetangia, mutualists and symbiotes in insect-fungus symbioses. Fungal Ecology, 44, 100909. doi:10.1016/j.funeco.2019.100909
• Višňovská, D., Pyszko, P., Šigut, M., Kostovčík, M., Kolařík, M., Kotásková, N., & Drozd, P. (2020). Caterpillar gut and host plant phylloplane mycobiomes differ: a new perspective on fungal involvement in insect guts. FEMS Microbiology Ecology, 96(9), fiaa116. doi:10.1093/femsec/fiaa116
• Wynns, A. A. (2015). Convergent evolution of highly reduced fruiting bodies in Pezizomycotina suggests key adaptations to the bee habitat. BMC Evolutionary Biology, 15(1), 145. doi:10.1186/s12862-015-0401-6
• Zhang, N., Suh, S.-O., & Blackwell, M. (2003). Microorganisms in the gut of beetles: evidence from molecular cloning. Journal of Invertebrate Pathology, 84(3), 226-233. doi:10.1016/j.jip.2003.10.002
• Zhang, J., Gao, D., Li, Q., Zhao, Y., Li, L., Lin, H., Bi, Q., & Zhao, Y. (2020). Biodegradation of polyethylene microplastic particles by the fungus Aspergillus flavus from the guts of wax moth Galleria mellonella. Science of The Total Environment, 704, 135931. doi:10.1016/j.scitotenv.2019.135931