Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

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Yeasts of Pichia (Pichiaceae) dominate the mycobiome of Hermetia illucens (Diptera: Stratiomyidae) larvae during urban composting
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Vallejo-Arróliga, M., & Rojas-Jimenez, K. (2024). Yeasts of Pichia (Pichiaceae) dominate the mycobiome of Hermetia illucens (Diptera: Stratiomyidae) larvae during urban composting. Revista De Biología Tropical, 72(1), e57898. https://doi.org/10.15517/rev.biol.trop.v71i1.57898

Abstract

Introduction: Hermetia illucens is a fly found worldwide in tropical and temperate regions that feeds on decaying organic matter in its larval stage, which makes them useful to accelerate composing processes. Bacterial component on the larval guts that helps to degrade organic matter is well studied, however fungal communities information is more scarse, specially in tropical regions. Objective: To determine fungal communities in the gut of H. illucens larvae naturally occurring during urban composting processes in a tropical region. Methods: ITS sequencing was employed to characterize fungal communities present in H. illucens larval gut. Results: The analysis of amplicon sequence variants (ASVs) unveiled a notable dominance of Saccharomycetales, being yeasts of the genus Pichia the most abundant. Other relatively abundant yeasts were Candida and Galactomyces and the genus Archaeospora from Archaeosporales. The last two groups not being reported in H. illucens before. Conclusions: Yeasts of the genus Pichia are the most abundant group, this result is in concordance with previous studies which suggest a stable insect-yeast relation. The description of previously unreported fungal groups highlights the importance of continuing to explore the mycobiome dynamics of this larva. This study offers insight into the mycobiome of naturally occurring H. illucens larvae in a tropical region.

https://doi.org/10.15517/rev.biol.trop..v71i1.57898
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References

Abdel-Banat, B. M. A., Hoshida, H., Ano, A., Nonklang, S., & Akada, R. (2010). High-temperature fermentation: How can processes for ethanol production at high temperatures become superior to the traditional process using mesophilic yeast? Applied Microbiology and Biotechnology, 85(4), 861–867.

Aime, M. C., & Brearley, F. Q. (2012). Tropical fungal diversity: Closing the gap between species estimates and species discovery. Biodiversity and Conservation, 21(9), 2177–2180.

Bajaj, B. K., Raina, S., & Singh, S. (2013). Killer toxin from a novel killer yeast Pichia kudriavzevii RY55 with idiosyncratic antibacterial activity. Journal of Basic Microbiology, 53(8), 645–656.

Biedermann, P. H. W., & Vega, F. E. (2020). Ecology and Evolution of Insect–Fungus Mutualisms. Annual Review of Entomology, 65(1), 431–455.

Boccazzi, I. V., Ottoboni, M., Martin, E., Comandatore, F., Vallone, L., Spranghers, T., Eeckhout, M., Mereghetti, V., Pinotti, L., & Epis, S. (2017). A survey of the mycobiota associated with larvae of the black soldier fly (Hermetia illucens) reared for feed production. PLOS ONE, 12(8), e0182533.

Boekhout, T., Amend, A. S., El Baidouri, F., Gabaldón, T., Geml, J., Mittelbach, M., Robert, V., Tan, C. S., Turchetti, B., Vu, D., Wang, Q. M., & Yurkov, A. (2021). Trends in yeast diversity discovery. Fungal Diversity, 114(1), 491–537.

Brown, J. H. (2014). Why are there so many species in the tropics? Journal of Biogeography, 41(1), 8–22.

Bruno, D., Bonelli, M., De Filippis, F., Di Lelio, I., Tettamanti, G., Casartelli, M., Ercolini, D., & Caccia, S. (2019). The intestinal microbiota of Hermetia illucens larvae is affected by diet and shows a diverse composition in the different midgut regions. Applied and Environmental Microbiology, 85(2), e01864-18.

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.

Chaijak, P., Lertworapreecha, M., & Sukkasem, C. (2018). Phenol removal from palm oil mill effluent using Galactomyces reessii termite-associated yeast. Polish Journal of Environmental Studies, 27(1), 39.

Chamnipa, N., Thanonkeo, S., Klanrit, P., & Thanonkeo, P. (2018). The potential of the newly isolated thermotolerant yeast Pichia kudriavzevii RZ8-1 for high-temperature ethanol production. Brazilian Journal of Microbiology, 49(2), 378–391.

Chandler, J. A., Eisen, J. A., & Kopp, A. (2012). Yeast Communities of Diverse Drosophila Species: Comparison of Two Symbiont Groups in the Same Hosts. Applied and Environmental Microbiology, 78(20), 7327.

Chelliah, R., Ramakrishnan, S. R., Prabhu, P. R., & Antony, U. (2016). Evaluation of antimicrobial activity and probiotic properties of wild-strain Pichia kudriavzevii isolated from frozen idli batter. Yeast, 33(8), 385–401.

Cifuentes, Y., Vilcinskas, A., Kämpfer, P., & Glaeser, S. P. (2022). Isolation of Hermetia illucens larvae core gut microbiota by two different cultivation strategies. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 115(6), 821–837.

Contreras, M., Grande-Tovar, C. D., Vallejo, W., & Chaves-López, C. (2019). Bio-Removal of Methylene Blue from Aqueous Solution by Galactomyces geotrichum KL20A. Water, 11(2), 282.

Cruz-Ramírez, M. G., Rivera-Ríos, J. M., Téllez-Jurado, A., Maqueda-Gálvez, A. P., Mercado-Flores, Y., & Arana-Cuenca, A. (2012). Screening for thermotolerant ligninolytic fungi with laccase, lipase, and protease activity isolated in Mexico. Journal of Environmental Management, 95(SUPPL.), S256–S259.

Czekała, W., Janczak, D., Cieślik, M., Mazurkiewicz, J., & Pulka, J. (2020). Food Waste Management Using Hermetia Illucens Insect. Journal of Ecological Engineering, 21(4), 214–216.

da Silva, G. D. P., & Hesselberg, T. (2020). A Review of the Use of Black Soldier Fly Larvae, Hermetia illucens (Diptera: Stratiomyidae), to Compost Organic Waste in Tropical Regions. Neotropical Entomology, 49(2), 151–162.

De Smet, J., Wynants, E., Cos, P., & Van Campenhout, L. (2018). Microbial Community Dynamics during Rearing of Black Soldier Fly Larvae (Hermetia illucens) and Impact on Exploitation Potential. Applied and Environmental Microbiology, 84(9).

Dehghani, R., Asadi, M. A., Charkhloo, E., Mostafaie, G., Saffari, M., Mousavi, G. A., Pourbabaei, M., Dehghani, R., Asadi, M. A., Charkhloo, E., Mostafaie, G., Saffari, M., Mousavi, G. A., & Pourbabaei, M. (2012). Identification of Fungal Communities in Producing Compost by Windrow Method. Journal of Environmental Protection, 3(1), 61–67.

Deshpande, V., Wang, Q., Greenfield, P., Charleston, M., Porras-Alfaro, A., Kuske, C. R., Cole, J. R., Midgley, D. J., & Tran-Dinh, N. (2016). Fungal identification using a Bayesian classifier and the Warcup training set of internal transcribed spacer sequences. Mycologia, 108(1), 1–5.

Di Piazza, S., Houbraken, J., Meijer, M., Cecchi, G., Kraak, B., Rosa, E., & Zotti, M. (2020). Thermotolerant and Thermophilic Mycobiota in Different Steps of Compost Maturation. Microorganisms, 8(6), 880.

Diener, S., Zurbrügg, C., & Tockner, K. (2009). Conversion of organic material by black soldier fly larvae: establishing optimal feeding rates. Waste Management & Research, 27(6), 603–610.

El Hayany, B., El Fels, L., Kouisni, L., Yasri, A., & Hafidi, M. (2022). An insight into role of microorganisms in composting and its applications in agriculture. Microbial Biotechnology for Sustainable Agriculture, 1, 1185–203.

Fletcher, E., Feizi, A., Kim, S. S., Siewers, V., & Nielsen, J. (2015). RNA-seq analysis of Pichia anomala reveals important mechanisms required for survival at low pH. Microbial Cell Factories, 14(1), 1–11.

França, R. C., Conceição, F. R., Mendonça, M., Haubert, L., Sabadin, G., de Oliveira, P. D., Amaral, M. G., Silva, W. P. da, & Moreira, Â. N. (2015). Pichia pastoris X-33 has probiotic properties with remarkable antibacterial activity against Salmonella Typhimurium. Applied Microbiology and Biotechnology, 99(19), 7953–7961.

Furtado, J., Siles, X., & Campos, H. (2009). Carotenoid concentrations in vegetables and fruits common to the Costa Rican diet. International Journal of Food Sciences and Nutrition, 55(2), 101–113.

Gabriel, R., Mueller, R., Floerl, L., Hopson, C., Harth, S., Schuerg, T., Fleissner, A., & Singer, S. W. (2021). CAZymes from the thermophilic fungus Thermoascus aurantiacus are induced by C5 and C6 sugars. Biotechnology for Biofuels, 14(1), 169.

Gil-Rodríguez, A. M., & Garcia-Gutierrez, E. (2021). Antimicrobial mechanisms and applications of yeasts. Advances in Applied Microbiology, 114, 37–72.

Golubev, W. I. (2006). Antagonistic Interactions Among Yeasts. In G. Péter, C. Rosa (Eds.), Biodiversity and Ecophysiology of Yeasts (197–219). Springer.

Guilhot, R., Xué, A., Lagmairi, A., Olazcuaga, L., & Fellous, S. (2023). Microbiota acquisition and transmission in Drosophila flies. ISCIENCE, 26, 107656.

Guo, G., Tian, F., Zhao, Y., Tang, M., Liu, W., Liu, C., Xue, S., Kong, W., Sun, Y., & Wang, S. (2019). Aerobic decolorization and detoxification of Acid Scarlet GR by a newly isolated salt-tolerant yeast strain Galactomyces geotrichum GG. International Biodeterioration & Biodegradation, 145, 104818.

Gusmão, D. S., Santos, A. V., Marini, D. C., Bacci, M., Berbert-Molina, M. A., & Lemos, F. J. A. (2010). Culture-dependent and culture-independent characterization of microorganisms associated with Aedes aegypti (Diptera: Culicidae) (L.) and dynamics of bacterial colonization in the midgut. Acta Tropica, 115(3), 275–281.

Hamby, K. A., Hernández, A., Boundy-Mills, K., & Zalom, F. G. (2012). Associations of yeasts with spotted-wing Drosophila (Drosophila suzukii; Diptera: Drosophilidae) in cherries and raspberries. Applied and Environmental Microbiology, 78(14), 4869–4873.

Hemidat, S., Jaar, M., Nassour, A., & Nelles, M. (2018). Monitoring of Composting Process Parameters: A Case Study in Jordan. Waste and Biomass Valorization, 9(12), 2257–2274.

IJdema, F., De Smet, J., Crauwels, S., Lievens, B., & Van Campenhout, L. (2022). Meta-analysis of larvae of the black soldier fly (Hermetia illucens) microbiota based on 16S rRNA gene amplicon sequencing. FEMS Microbiology Ecology, 98(9).

Jiang, C. L., Jin, W. Z., Tao, X. H., Zhang, Q., Zhu, J., Feng, S. Y., Xu, X. H., Li, H. Y., Wang, Z. H., & Zhang, Z. J. (2019). Black soldier fly larvae (Hermetia illucens) strengthen the metabolic function of food waste biodegradation by gut microbiome. Microbial Biotechnology, 12(3), 528–543.

Joosten, L., Lecocq, A., Jensen, A. B., Haenen, O., Schmitt, E., & Eilenberg, J. (2020). Review of insect pathogen risks for the black soldier fly (Hermetia illucens) and guidelines for reliable production. Entomologia Experimentalis et Applicata, 168(6–7), 432–447.

Kannan, M., Vitenberg, T., Ben-Mordechai, L., Khatib, S., & Opatovsky, I. (2023). Effect of yeast supplementation on growth parameters and metabolomics of black soldier fly larvae, Hermetia illucens (L.) (Diptera: Stratiomyidae). Journal of Insects as Food and Feed, 19(1), 1–12.

Kaya, C., Generalovic, T. N., Ståhls, G., Hauser, M., Samayoa, A. C., Nunes-Silva, C. G., Roxburgh, H., Wohlfahrt, J., Ewusie, E. A., Kenis, M., Hanboonsong, Y., Orozco, J., Carrejo, N., Nakamura, S., Gasco, L., Rojo, S., Tanga, C. M., Meier, R., Rhode, C., … Sandrock, C. (2021). Global population genetic structure and demographic trajectories of the black soldier fly, Hermetia illucens. BMC Biology 2021, 19(1), 1–22.

Kieliszek, M., Kot, A. M., Bzducha-Wróbel, A., BŁażejak, S., Gientka, I., & Kurcz, A. (2017). Biotechnological use of Candida yeasts in the food industry: A review. Fungal Biology Reviews, 31(4), 185–198.

Kim, J. G., Choi, Y. C., Choi, J. Y., Kim, W.T., Jeong, G. S., Park, K. H., & Hwang, S. J. (2008). Ecology of the Black Soldier Fly, Hermetia illucens (Diptera: Stratmyidae) in Korea. Korean Journal of Applied Entomology, 47(4), 337–343.

Klüber, P., Müller, S., Schmidt, J., Zorn, H., & Rühl, M. (2022a). Isolation of Bacterial and Fungal Microbiota Associated with Hermetia illucens Larvae Reveals Novel Insights into Entomopathogenicity. Microorganisms, 10(2), 319.

Klüber, P., Tegtmeier, D., Hurka, S., Pfeiffer, J., Vilcinskas, A., Rühl, M., & Zorn, H. (2022b). Diet Fermentation Leads to Microbial Adaptation in Black Soldier Fly (Hermetia illucens; Linnaeus, 1758) Larvae Reared on Palm Oil Side Streams. Sustainability, 14(9), 5626.

Kumar, S., Dheeran, P., Singh, S. P., Mishra, I. M., & Adhikari, D. K. (2015). Bioprocessing of bagasse hydrolysate for ethanol and xylitol production using thermotolerant yeast. Bioprocess and Biosystems Engineering, 38(1), 39–47.

Madden, A. A., Epps, M. J., Fukami, T., Irwin, R. E., Sheppard, J., Sorger, D. M., & Dunn, R. R. (2018). The ecology of insect–yeast relationships and its relevance to human industry. Proceedings of the Royal Society B: Biological Sciences, 285(1875).

Malassigné, S., Minard, G., Vallon, L., Martin, E., Moro, C. V., & Luis, P. (2021). Diversity and functions of yeast communities associated with insects. Microorganisms, 9(8), 1552.

Mehetre, G. T., Dastager, S. G., & Dharne, M. S. (2019). Biodegradation of mixed polycyclic aromatic hydrocarbons by pure and mixed cultures of biosurfactant producing thermophilic and thermo-tolerant bacteria. Science of The Total Environment, 679, 52–60.

Mendes, T. D., Rodrigues, A., Dayo-Owoyemi, I., Marson, F. A. L., & Pagnocca, F. C. (2012). Generation of Nutrients and Detoxification: Possible Roles of Yeasts in Leaf-Cutting Ant Nests. Insects, 3(1), 228–245.

Meshrif, W. S., Rohlfs, M., & Roeder, T. (2016). The Effect of Nutritive Yeasts on the Fitness of the Fruit Fly Drosophila melanogaster (Diptera: Drosophilidae). African Entomology, 24(1), 90–99.

Morales-Rodríguez, C., Sferrazza, I., Aleandri, M. P., Dalla Valle, M., Speranza, S., Contarini, M., & Vannini, A. (2021). The fungal community associated with the ambrosia beetle Xylosandrus compactus invading the mediterranean maquis in central Italy reveals high biodiversity and suggests environmental acquisitions. Fungal Biology, 125(1), 12–24.

Nakasaki, K., Araya, S., & Mimoto, H. (2013). Inoculation of RB1 degrades the organic acids present in raw compost material and accelerates composting. Bioresource Technology, 144, 521–528.

Nozhevnikova, A. N., Mironov, V. V., Botchkova, E. A., Litti, Y. V., & Russkova, Y. I. (2019). Composition of a Microbial Community at Different Stages of Composting and the Prospects for Compost Production from Municipal Organic Waste (Review). Applied Biochemistry and Microbiology, 55(3), 199–208.

Oksanen, J., Simpson, G. L., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O´Hara, R. B., Solymos, P., Stevens, M. H. H., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., de Caceres, M., Durand, S.,…Weedon, J. (2022). vegan: Community Ecology Package (Version 2.6-4, “R Package”). https://CRAN.R-project.org/package=vegan

Østergaard, L. H., & Olsen, H. S. (2011). Industrial Applications of Fungal Enzymes. Industrial Applications, 269–290.

Park, H. J., Bae, J. H., Ko, H. J., Lee, S. H., Sung, B. H., Han, J. I., & Sohn, J. H. (2018). Low-pH production of d-lactic acid using newly isolated acid tolerant yeast Pichia kudriavzevii NG7. Biotechnology and Bioengineering, 115(9), 2232–2242.

Pongcharoen, P., Chawneua, J., & Tawong, W. (2018). High temperature alcoholic fermentation by new thermotolerant yeast strains Pichia kudriavzevii isolated from sugarcane field soil. Agriculture and Natural Resources, 52(6), 511–518.

Queiroz, S. D., Jofre, F. M., Bianchini, I. D., Boaes, T. D., Bordini, F. W., Chandel, A. K., & Felipe, M. D. (2023). Current advances in Candida tropicalis: Yeast overview and biotechnological applications. Biotechnology and Applied Biochemistry, 70(6), 2069–2087.

Querejeta, M., Hervé, V., Perdereau, E., Marchal, L., Herniou, E. A., Boyer, S., & Giron, D. (2023). Changes in Bacterial Community Structure Across the Different Life Stages of Black Soldier Fly (Hermetia illucens). Microbial Ecology, 86(2), 1254–1267.

R Core Team. (2023). R: A Language and Environment for Statistical Computing (Software). R Foundation for Statistical Computing. https://www.R-project.org/

Rassati, D., Marini, L., & Malacrinò, A. (2019). Acquisition of fungi from the environment modifies ambrosia beetle mycobiome during invasion. PeerJ, (11), e8103.

Sacchi, L., Genchi, M., Clementi, E., Bigliardi, E., Avanzati, A. M., Pajoro, M., Negri, I., Marzorati, M., Gonella, E., Alma, A., Daffonchio, D., & Bandi, C. (2008). Multiple symbiosis in the leafhopper Scaphoideus titanus (Hemiptera: Cicadellidae): Details of transovarial transmission of Cardinium sp. and yeast-like endosymbionts. Tissue and Cell, 40(4), 231–242.

Santos, A., San Mauro, M., Bravo, E., & Marquina, D. (2009). PMKT2, a new killer toxin from Pichia membranifaciens, and its promising biotechnological properties for control of the spoilage yeast Brettanomyces bruxellensis. Microbiology, 155(2), 624–634.

Shokry, N., Eldakak, M. M., Hegazi, E., Aziz, A., & Alseqely, M. (2023). Assessing Fungal and Bacterial Microbiome Diversity in The Black Soldier Fly (Hermetia illucens L.) Gut and Its Different Feeding Media. Advances in Biotechnology & Microbiology, 17(2), 555958.

Shrivastava, A., Pal, M., & Sharma, R. K. (2023). Pichia as yeast cell factory for production of industrially important bio-products: Current trends, challenges, and future prospects. Journal of Bioresources and Bioproducts, 8(2), 108–124.

Stefanini, I. (2018). Yeast-insect associations: It takes guts. Yeast, 35(4), 315–330.

Steyn, A., Roets, F., & Botha, A. (2016). Yeasts Associated with Culex pipiens and Culex theileri Mosquito Larvae and the Effect of Selected Yeast Strains on the Ontogeny of Culex pipiens. Microbial Ecology, 71(3), 747–760.

Tanga, C. M., Waweru, J. W., Tola, Y. H., Onyoni, A. A., Khamis, F. M., Ekesi, S., & Paredes, J. C. (2021). Organic Waste Substrates Induce Important Shifts in Gut Microbiota of Black Soldier Fly (Hermetia illucens L.): Coexistence of Conserved, Variable, and Potential Pathogenic Microbes. Frontiers in Microbiology, 12, 635881.

Tegtmeier, D., Hurka, S., Klüber, P., Brinkrolf, K., Heise, P., & Vilcinskas, A. (2021). Cottonseed Press Cake as a Potential Diet for Industrially Farmed Black Soldier Fly Larvae Triggers Adaptations of Their Bacterial and Fungal Gut Microbiota. Frontiers in Microbiology, 12, 634503.

Tettamanti, G., Campenhout, L. Van, & Casartelli, M. (2022). A hungry need for knowledge on the black soldier fly digestive system. Journal of Insects as Food and Feed, 8(3), 217–222.

Vitenberg, T., & Opatovsky, I. (2022). Assessing Fungal Diversity and Abundance in the Black Soldier Fly and its Environment. Journal of Insect Science, 22(6), 3–4.

Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16), 5261–5267.

Willis, A., Rodrigues, B. F., & Harris, P. J. C. (2013). The Ecology of Arbuscular Mycorrhizal Fungi. Critical Reviews in Plant Sciences, 32(1), 1–20.

Wynants, E., Frooninckx, L., Crauwels, S., Verreth, C., De Smet, J., Sandrock, C., Wohlfahrt, J., Van Schelt, J., Depraetere, S., Lievens, B., Van Miert, S., Claes, J., & Van Campenhout, L. (2019). Assessing the Microbiota of Black Soldier Fly Larvae (Hermetia illucens) Reared on Organic Waste Streams on Four Different Locations at Laboratory and Large Scale. Microbial Ecology, 77(4), 913–930.

Zhang, L., Shen, Y., Hui, F., & Niu, Q. (2015). Degradation of residual lincomycin in fermentation dregs by yeast strain S9 identified as Galactomyces geotrichum. Annals of Microbiology, 65, 1333-1340.

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