Fruit host-dependent fungal communities in the microbiome of wild Queensland fruit fly larvae.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
06 10 2020
Historique:
received: 21 05 2020
accepted: 14 09 2020
entrez: 7 10 2020
pubmed: 8 10 2020
medline: 5 2 2021
Statut: epublish

Résumé

Bactrocera tryoni (Froggatt), the Queensland fruit fly (Qfly), is a highly polyphagous tephritid fly that is widespread in Eastern Australia. Qfly physiology is closely linked with its fungal associates, with particular relationship between Qfly nutrition and yeast or yeast-like fungi. Despite animal-associated fungi typically occurring in multi-species communities, Qfly studies have predominately involved the culture and characterisation of single fungal isolates. Further, only two studies have investigated the fungal communities associated with Qfly, and both have used culture-dependant techniques that overlook non-culturable fungi and hence under-represent, and provide a biased interpretation of, the overall fungal community. In order to explore a potentially hidden fungal diversity and complexity within the Qfly mycobiome, we used culture-independent, high-throughput Illumina sequencing techniques to comprehensively, and holistically characterized the fungal community of Qfly larvae and overcome the culture bias. We collected larvae from a range of fruit hosts along the east coast of Australia, and all had a mycobiome dominated by ascomycetes. The most abundant fungal taxa belonged to the genera Pichia (43%), Candida (20%), Hanseniaspora (10%), Zygosaccharomyces (11%) and Penicillium (7%). We also characterized the fungal communities of fruit hosts, and found a strong degree of overlap between larvae and fruit host communities, suggesting that these communities are intimately inter-connected. Our data suggests that larval fungal communities are acquired from surrounding fruit flesh. It is likely that the physiological benefits of Qfly exposure to fungal communities is primarily due to consumption of these fungi, not through syntrophy/symbiosis between fungi and insect 'host'.

Identifiants

pubmed: 33024226
doi: 10.1038/s41598-020-73649-1
pii: 10.1038/s41598-020-73649-1
pmc: PMC7538879
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

16550

Références

Flint, H. J., Scott, K. P., Louis, P. & Duncan, S. H. The role of the gut microbiota in nutrition and health. Nat. Rev. Gastroenterol. Hepatol. 9, 577. https://doi.org/10.1038/nrgastro.2012.156 (2012).
doi: 10.1038/nrgastro.2012.156 pubmed: 22945443
Nicholson, J. K. et al. Host-gut microbiota metabolic interactions. Science 336, 1262–1267. https://doi.org/10.1126/science.1223813 (2012).
doi: 10.1126/science.1223813
Zhang, Z., Jiao, S., Li, X. & Li, M. Bacterial and fungal gut communities of Agrilus mali at different developmental stages and fed different diets. Sci. Rep. 8, 15634 (2018).
pubmed: 30353073 pmcid: 6199299 doi: 10.1038/s41598-018-34127-x
Engel, P. & Moran, N. A. The gut microbiota of insects–diversity in structure and function. FEMS Microbiol. Rev. 37, 699–735 (2013).
pubmed: 23692388 doi: 10.1111/1574-6976.12025
Paine, T., Raffa, K. & Harrington, T. Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu. Rev. Entomol. 42, 179–206 (1997).
pubmed: 15012312 doi: 10.1146/annurev.ento.42.1.179
Yun, J. H. et al. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl. Environ. Microbiol. 80, 5254–5264 (2014).
pubmed: 24928884 pmcid: 4136111 doi: 10.1128/AEM.01226-14
Fukatsu, T. & Ishikawa, H. A novel eukaryotic extracellular symbiont in an aphid, Astegopteryx styraci (Homoptera, Aphididae, Hormaphidinae). J. Insect Physiol. 38, 765–773 (1992).
doi: 10.1016/0022-1910(92)90029-D
Malacrinò, A., Schena, L., Campolo, O., Laudani, F. & Palmeri, V. Molecular analysis of the fungal microbiome associated with the olive fruit fly Bactrocera oleae. Fungal Ecol. 18, 67–74 (2015).
doi: 10.1016/j.funeco.2015.08.006
Vega, F. E. & Blackwell, M. Insect-Fungal Associations: Ecology and Evolution (Oxford University Press, Oxford, 2005).
Stefanini, I. Yeast-insect associations: it takes guts. Yeast 35, 315–330 (2018).
pubmed: 29363168 pmcid: 29363168 doi: 10.1002/yea.3309
Boyce, A. Bionomics of the walnut husk fly, Rhagoletis completa. Hilgardia 8, 363–579 (1934).
doi: 10.3733/hilg.v08n11p363
Fanson, B. G. & Taylor, P. W. Protein: carbohydrate ratios explain life span patterns found in Queensland fruit fly on diets varying in yeast: sugar ratios. Age 34, 1361–1368 (2012).
pubmed: 21904823 doi: 10.1007/s11357-011-9308-3
Moadeli, T., Mainali, B., Ponton, F. & Taylor, P. Evaluation of yeasts in gel larval diet for Queensland fruit fly, Bactrocera tryoni. J. Appl. Entomol. 142, 679–688 (2018).
doi: 10.1111/jen.12520
Nash, W. J. & Chapman, T. Effect of dietary components on larval life history characteristics in the Medfly (Ceratitis capitata: Diptera, Tephritidae). PLoS ONE 9, e86029 (2014).
pubmed: 24465851 pmcid: 3897573 doi: 10.1371/journal.pone.0086029
Nestel, D. & Nemny-Lavy, E. Nutrient balance in medfly, Ceratitis capitata, larval diets affects the ability of the developing insect to incorporate lipid and protein reserves. Entomol. Exp. Appl. 126, 53–60. https://doi.org/10.1111/j.1570-7458.2007.00639.x (2008).
doi: 10.1111/j.1570-7458.2007.00639.x
Nestel, D., Nemny-Lavy, E. & Chang, C. L. Lipid and protein loads in pupating larvae and emerging adults as affected by the composition of Mediterranean fruit fly (Ceratitis capitata) meridic larval diets. Arch. Insect Biochem. Physiol. 56, 97–109. https://doi.org/10.1002/arch.20000 (2004).
doi: 10.1002/arch.20000 pubmed: 15211548
Mori, B. A. et al. Enhanced yeast feeding following mating facilitates control of the invasive fruit pest Drosophila suzukii. J. Appl. Ecol. 54, 170–177. https://doi.org/10.1111/1365-2664.12688 (2017).
doi: 10.1111/1365-2664.12688
Stamps, J. A., Yang, L. H., Morales, V. M. & Boundy-Mills, K. L. Drosophila regulate yeast density and increase yeast community similarity in a natural substrate. PLoS ONE 7, e42238. https://doi.org/10.1371/journal.pone.0042238 (2012).
doi: 10.1371/journal.pone.0042238 pubmed: 22860093 pmcid: 3409142
Anagnostou, C., Dorsch, M. & Rohlfs, M. Influence of dietary yeasts on Drosophila melanogaster life-history traits. Entomol. Exp. Appl. 136, 1–11. https://doi.org/10.1111/j.1570-7458.2010.00997.x (2010).
doi: 10.1111/j.1570-7458.2010.00997.x
Rohlfs, M. & Kürschner, L. Saprophagous insect larvae, Drosophila melanogaster, profit from increased species richness in beneficial microbes. J. Appl. Entomol. 134, 667–671. https://doi.org/10.1111/j.1439-0418.2009.01458.x (2010).
doi: 10.1111/j.1439-0418.2009.01458.x
Menezes, C. et al. A Brazilian social bee must cultivate fungus to survive. Curr. Biol. 25, 2851–2855. https://doi.org/10.1016/j.cub.2015.09.028 (2015).
doi: 10.1016/j.cub.2015.09.028 pubmed: 26592344
Yun, J. H., Jung, M. J., Kim, P. S. & Bae, J. W. Social status shapes the bacterial and fungal gut communities of the honey bee. Sci. Rep. 8, 2019. https://doi.org/10.1038/s41598-018-19860-7 (2018).
doi: 10.1038/s41598-018-19860-7 pubmed: 29386588 pmcid: 5792453
DeLeon-Rodriguez, C. M. & Casadevall, A. Cryptococcus neoformans: tripping on acid in the phagolysosome. Front. Microbiol. 7, 164. https://doi.org/10.3389/fmicb.2016.00164 (2016).
doi: 10.3389/fmicb.2016.00164 pubmed: 26925039 pmcid: 4756110
Hajek, A. & St. Leger, R. Interactions between fungal pathogens and insect hosts. Annu. Rev. Entomol. 39, 293–322. https://doi.org/10.1146/annurev.en.39.010194.001453 (1994).
doi: 10.1146/annurev.en.39.010194.001453
Lu, H. L., Wang, J. B., Brown, M. A., Euerle, C. & Leger, R. J. S. Identification of Drosophila mutants affecting defense to an entomopathogenic fungus. Sci. Rep. 5, 12350 (2015).
pubmed: 26202798 pmcid: 4511952 doi: 10.1038/srep12350
Almeida, J. E., Batista Filho, A., Oliveira, F. C. & Raga, A. Pathogenicity of the entomopathogenic fungi and nematode on medfly Ceratitis capitata (Wied.)(Diptera: Tephritidae). BioAssay https://doi.org/10.14295/BA.v2 (2007).
doi: 10.14295/BA.v2
Lacey, L. A., Frutos, R., Kaya, H. & Vail, P. Insect pathogens as biological control agents: do they have a future?. Biol. Control 21, 230–248 (2001).
doi: 10.1006/bcon.2001.0938
Ortu, S., Cocco, A. & Dau, R. Evaluation of the entomopathogenic fungus Beauveria bassiana strain ATCC 74040 for the management of Ceratitis capitata. B. Insectol. 62, 245–252 (2009).
Quesada-Moraga, E., Ruiz-García, A. & Santiago-Alvarez, C. Laboratory evaluation of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae against puparia and adults of Ceratitis capitata (Diptera: Tephritidae). J. Econ. Entomol. 99, 1955–1966 (2006).
pubmed: 17195660 doi: 10.1093/jee/99.6.1955
Clarke, A. R., Powell, K. S., Weldon, C. W. & Taylor, P. W. The ecology of Bactrocera tryoni (Diptera: Tephritidae): what do we know to assist pest management?. Ann. Appl. Biol. 158, 26–54 (2011).
doi: 10.1111/j.1744-7348.2010.00448.x
Dominiak, B. C. & Daniels, D. Review of the past and present distribution of Mediterranean fruit fly (Ceratitis capitata Wiedemann) and Queensland fruit fly (Bactrocera tryoni Froggatt) in Australia. Aust. J. Entomol. 51, 104–115 (2012).
doi: 10.1111/j.1440-6055.2011.00842.x
Sutherst, R. W., Collyer, B. S. & Yonow, T. The vulnerability of Australian horticulture to the Queensland fruit fly, Bactrocera (Dacus) tryoni, under climate change. Aust. J. Agric. Res. 51, 467–480 (2000).
doi: 10.1071/AR98203
Dominiak, B., Westcott, A. & Barchia, I. Release of sterile Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae), at Sydney, Australia. Aust. J. Exp. Agric. 43, 519–528 (2003).
doi: 10.1071/EA01146
Deutscher, A. T. et al. Near full-length 16S rRNA gene next-generation sequencing revealed Asaia as a common midgut bacterium of wild and domesticated Queensland fruit fly larvae. Microbiome 6, 85 (2018).
pubmed: 29729663 pmcid: 5935925 doi: 10.1186/s40168-018-0463-y
Drew, R., Courtice, A. & Teakle, D. Bacteria as a natural source of food for adult fruit flies (Diptera: Tephritidae). Oecologia 60, 279–284. https://doi.org/10.1007/BF00376839 (1983).
doi: 10.1007/BF00376839 pubmed: 28310683
Lloyd, A., Drew, R., Teakle, D. & Hayward, A. Bacteria associated with some Dacus species (Diptera: Tephritidae) and their host fruit in Queensland. Aust. J. Biol. Sci. 39, 361–368 (1986).
doi: 10.1071/BI9860361
Morrow, J. L., Frommer, M., Shearman, D. C. & Riegler, M. The microbiome of field-caught and laboratory-adapted Australian tephritid fruit fly species with different host plant use and specialisation. Microb. Ecol. 70, 498–508 (2015).
pubmed: 25666536 doi: 10.1007/s00248-015-0571-1
Murphy, K. M., Teakle, D. S. & MacRae, I. C. Kinetics of colonization of adult Queensland fruit flies (Bactrocera tryoni) by dinitrogen-fixing alimentary tract bacteria. Appl. Environ. Microbiol. 60, 2508–2517 (1994).
pubmed: 16349328 pmcid: 201677 doi: 10.1128/AEM.60.7.2508-2517.1994
Thaochan, N., Drew, R., Hughes, J., Vijaysegaran, S. & Chinajariyawong, A. Alimentary tract bacteria isolated and identified with API-20E and molecular cloning techniques from Australian tropical fruit flies Bactrocera cacuminata and B. tryoni. J. Insect Sci. 10, 131 (2010).
pubmed: 20883132 pmcid: 3016917 doi: 10.1673/031.010.13101
Majumder, R., Sutcliffe, B., Taylor, P. W. & Chapman, T. A. Next-Generation Sequencing reveals relationship between the larval microbiome and food substrate in the polyphagous Queensland fruit fly. Sci. Rep. 9, 1–12 (2019).
doi: 10.1038/s41598-018-37186-2
Shuttleworth, L. A., Khan, M. A. M., Collins, D., Osborne, T. & Reynolds, O. L. Wild bacterial probiotics fed to larvae of mass-reared Queensland fruit fly [Bactrocera tryoni (Froggatt)] do not impact long-term survival, mate selection, or locomotor activity. Insect Sci. 27, 745–755 (2020).
pubmed: 30848568 doi: 10.1111/1744-7917.12670
Shuttleworth, L. A. et al. A walk on the wild side: gut bacteria fed to mass-reared larvae of Queensland fruit fly [Bactrocera tryoni (Froggatt)] influence development. BMC Biotechnol. 19, 1–11 (2019).
doi: 10.1186/s12896-019-0579-6
Woruba, D. N. et al. Diet and irradiation effects on the bacterial community composition and structure in the gut of domesticated teneral and mature Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae). BMC Microbiol. 19, 281 (2019).
pubmed: 31870300 pmcid: 6929413 doi: 10.1186/s12866-019-1649-6
Majumder, R., Sutcliffe, B., Chapman, T. A. & Taylor, P. W. Microbiome of the Queensland fruit fly through metamorphosis. Microorganisms 8, 795 (2020).
pmcid: 7356580 doi: 10.3390/microorganisms8060795 pubmed: 7356580
Deutscher, A. T., Reynolds, O. L. & Chapman, T. A. Yeast: an overlooked component of Bactrocera tryoni (Diptera: Tephritidae) larval gut microbiota. J. Econ. Entomol. 110, 298–300 (2016).
Piper, A. M., Farnier, K., Linder, T., Speight, R. & Cunningham, J. P. Two gut-associated yeasts in a tephritid fruit fly have contrasting effects on adult attraction and larval survival. J. Chem. Ecol. 43, 891–901 (2017).
pubmed: 28836040 doi: 10.1007/s10886-017-0877-1
Toju, H., Tanabe, A. S., Yamamoto, S. & Sato, H. High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS ONE 7, e40863 (2012).
pubmed: 22808280 pmcid: 3395698 doi: 10.1371/journal.pone.0040863
Schmidt, P. A. et al. Illumina metabarcoding of a soil fungal community. Soil Biol. Biochem. 65, 128–132 (2013).
doi: 10.1016/j.soilbio.2013.05.014
Yun, J. H., Jung, M. J., Kim, P. S. & Bae, J. W. Social status shapes the bacterial and fungal gut communities of the honey bee. Sci. Rep. 8, 1–11 (2018).
doi: 10.1038/s41598-017-17765-5
Ravenscraft, A., Berry, M., Hammer, T., Peay, K. & Boggs, C. Structure and function of the bacterial and fungal gut microbiota of Neotropical butterflies. Ecol. Monogr. 89, e01346 (2019).
doi: 10.1002/ecm.1346
Mohammed, W. S., Ziganshina, E. E., Shagimardanova, E. I., Gogoleva, N. E. & Ziganshin, A. M. Comparison of intestinal bacterial and fungal communities across various xylophagous beetle larvae (Coleoptera: Cerambycidae). Sci. Rep. 8, 10073 (2018).
pubmed: 29968731 pmcid: 6030058 doi: 10.1038/s41598-018-27342-z
Sutcliffe, B. et al. Diverse fungal lineages in subtropical ponds are altered by sediment-bound copper. Fungal Ecol. 34, 28–42 (2018).
doi: 10.1016/j.funeco.2018.03.003
Hamby, K. A., Hernández, A., Boundy-Mills, K. & Zalom, F. G. Associations of yeasts with spotted-wing Drosophila (Drosophila suzukii; Diptera: Drosophilidae) in cherries and raspberries. Appl. Environ. Microbiol. 78, 4869–4873 (2012).
pubmed: 22582060 pmcid: 3416361 doi: 10.1128/AEM.00841-12
Kurtzman, C., Fell, J. W. & Boekhout, T. The Yeasts: A Taxonomic Study (Elsevier, Amsterdam, 2011).
Marchesi, J. R. Prokaryotic and eukaryotic diversity of the human gut. Adv. Appl. Microbiol. 72, 43–62 (2010).
pubmed: 20602987 doi: 10.1016/S0065-2164(10)72002-5
Xiang, H. et al. Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm (Helicoverpa armigera). Can. J. Microbiol. 52, 1085–1092 (2006).
pubmed: 17215900 doi: 10.1139/w06-064
Kudo, R., Masuya, H., Endoh, R., Kikuchi, T. & Ikeda, H. Gut bacterial and fungal communities in ground-dwelling beetles are associated with host food habit and habitat. ISME J. 13, 676 (2019).
pubmed: 30333525 doi: 10.1038/s41396-018-0298-3
Broderick, N. A., Raffa, K. F., Goodman, R. M. & Handelsman, J. Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl. Environ. Microbiol. 70, 293–300 (2004).
pubmed: 14711655 pmcid: 321235 doi: 10.1128/AEM.70.1.293-300.2004
Colman, D. R., Toolson, E. C. & Takacs-Vesbach, C. Do diet and taxonomy influence insect gut bacterial communities?. Mol. Ecol. 21, 5124–5137 (2012).
pubmed: 22978555 doi: 10.1111/j.1365-294X.2012.05752.x
Quan, A. S. & Eisen, M. B. The ecology of the Drosophila-yeast mutualism in wineries. PLoS ONE 13, e0196440 (2018).
pubmed: 29768432 pmcid: 5955509 doi: 10.1371/journal.pone.0196440
Starmer, W. T. & Lachance, M. A. Yeast ecology. Yeasts 7, 65–83 (2011).
doi: 10.1016/B978-0-444-52149-1.00006-9
Molnárová, J., Vadkertiová, R. & Stratilová, E. Extracellular enzymatic activities and physiological profiles of yeasts colonizing fruit trees. J. Basic Microbiol. 54, S74–S84 (2014).
pubmed: 23744750 doi: 10.1002/jobm.201300072
White, I. M. & Elson-Harris, M. M. Fruit Flies of Economic Significance: Their Identification and Bionomics (CAB International, Wallingford, 1992).
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294–299 (1994).
pubmed: 7881515
Benson, D. A. et al. GenBank. Nucleic Acids Res. 46, D41–D47 (2018).
pubmed: 29140468 doi: 10.1093/nar/gkx1094
Australia, P. H. The Australian Handbook for the Identification of Fruit Flies. Vol. Version 1.0 (ed. Woods N) 234 (2011).
Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol. Ecol. 2, 113–118 (1993).
pubmed: 8180733 doi: 10.1111/j.1365-294X.1993.tb00005.x
Hoggard, M. et al. Characterizing the human mycobiota: a comparison of small subunit rRNA, ITS1, ITS2, and large subunit rRNA genomic targets. Front. Microbiol. 9, 2208 (2018).
pubmed: 30283425 pmcid: 6157398 doi: 10.3389/fmicb.2018.02208
Fouts, D. E. et al. Next generation sequencing to define prokaryotic and fungal diversity in the bovine rumen. PLoS ONE 7, e48289 (2012).
pubmed: 23144861 pmcid: 3492333 doi: 10.1371/journal.pone.0048289
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335 (2010).
pubmed: 20383131 pmcid: 3156573 doi: 10.1038/nmeth.f.303
Greenfield, P. Greenfield Hybrid Analysis Pipeline (GHAP) v1 (CSIRO, Canberra, 2017).
Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).
pubmed: 20709691 doi: 10.1093/bioinformatics/btq461
Maidak, B. L. et al. The ribosomal database project (RDP). Nucleic Acids Res. 24, 82–85 (1996).
pubmed: 8594608 pmcid: 145599 doi: 10.1093/nar/24.1.82
Deshpande, V. et al. Fungal identification using a Bayesian classifier and the Warcup training set of internal transcribed spacer sequences. Mycologia 108, 1–5 (2016).
pubmed: 26553774 doi: 10.3852/14-293
Nilsson, R. H. et al. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 47, D259–D264 (2019).
pubmed: 30371820 doi: 10.1093/nar/gky1022
Clarke, K. & Ainsworth, M. A method of linking multivariate community structure to environmental variables. Mar. Ecol. Prog. Ser. 92, 205–205 (1993).
doi: 10.3354/meps092205

Auteurs

Rajib Majumder (R)

Applied BioSciences, Macquarie University, North Ryde, NSW, 2109, Australia. rajib.majumder@mq.edu.au.
Biosecurity and Food Safety, NSW Department of Primary Industries, Elizabeth Macarthur Agricultural Institute (EMAI), Menangle, NSW, 2567, Australia. rajib.majumder@mq.edu.au.

Brodie Sutcliffe (B)

Department of Environmental Sciences, Macquarie University, North Ryde, NSW, 2109, Australia.

Phillip W Taylor (PW)

Applied BioSciences, Macquarie University, North Ryde, NSW, 2109, Australia.

Toni A Chapman (TA)

Applied BioSciences, Macquarie University, North Ryde, NSW, 2109, Australia.
Biosecurity and Food Safety, NSW Department of Primary Industries, Elizabeth Macarthur Agricultural Institute (EMAI), Menangle, NSW, 2567, Australia.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH