Abstract
Recent advances in understanding the symbiotic interactions between bacteria and fruit flies have shown that they are relevant for mass rearing and the sterile insect technique (SIT). SIT involves mass production and release of sterile insects that would copulate with their wild conspecifics and thus decrease the population growth rate. The irradiation process used to sterilize mass-reared flies can modify the diversity and structure of the midgut bacterial communities, which could affect sterile male survival, flight capacity, and sexual competitiveness. Our aim was to compare bacterial communities in the midgut of wild and mass-reared Anastrepha obliqua (Macquart) males irradiated at 0, 60, and 80 Gy. After adult’s emergence, their midguts were dissected, DNA was extracted, and high-throughput sequencing of the V3–V4 region of the 16S rDNA gene was performed. A total of 11 phyla, 17 classes, 47 families, and 52 genera of bacteria were identified. The most representative phylum was Proteobacteria and the predominant family was Enterobacteriaceae. We found that wild males had a different intestinal bacterial community from mass-reared males. In addition, irradiation at 60 and 80 Gy caused changes in the diversity and structure of the midgut microbiota of these sterile males, suggesting that mass rearing and irradiation cause artificial selection of the bacterial communities in the gut of A. obliqua males.
Data Availability
The sequences datasets generated for this study can be found in the GenBank Bioproject PRJNA785925.
Code Availability
Not applicable for that section.
References
Ayushi G, Suresh N (2020) Dynamics of insect–microbiome interaction influence host and microbial symbiont. Front Microbiol. https://doi.org/10.3389/fmicb.2020.01357
Deutscher AT, Chapman TA, Shuttleworth LA, Riegler M, Reynolds OL (2019) Tephritid-microbial interactions to enhance fruit fly performance in sterile insect technique programs. BMC Microbiol 19:287. https://doi.org/10.1186/s12866-019-1650-0
Pereira R, Yuval B, Liedo P, Teal PEA, Shelly T, Mcinnis DO, Haq I, Taylor P, Hendrichs J (2020) Improving post-factory performance of sterile male fruit flies in support of the Sterile Insect Technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique. principles and practice in area-wide integrated pest management, 2nd edn. CRC Press, Boca Raton, pp 631–656
Woruba DN, Morrow JL, Reynolds OL, Chapman TA, Collins DP, Riegle M (2019) 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. https://doi.org/10.1186/s12866-019-1649-6
Cáceres C, Tsiamis G, Yuval B, Jurkevitch E, Bourtzis K (2019) Joint FAO/IAEA coordinated research project on “Use of symbiotic bacteria to reduce mass-rearing costs and increase mating success in selected fruit pests in support of SIT application.” BMC Microbiol 19:284. https://doi.org/10.1186/s12866-019-1644-y
Aluja M, Arredondo J, Díaz-Fleischer F, Birke A, Rull J, Niogret J, Epsky N (2014) Susceptibility of 15 mango (Sapindales: Anacardiaceae) cultivars to the attack by Anastrepha ludens and Anastrepha obliqua (Diptera: Tephritidae) and the role of underdeveloped fruit as pest reservoirs: management implications. J Econ Entomol 107:375–388. https://doi.org/10.1603/ec13045
Orozco-Dávila D, Quintero L, Hernández E, Solís E, Artiaga T, Hernández R, Montoya P (2017) Mass rearing and sterile insect releases for the control of Anastrepha spp. (Diptera: Tephritidae) pests in Mexico. Entomol Exp Appl 164:176–187. https://doi.org/10.1111/eea.12581
Gallardo-Ortiz U, Pérez-Staples D, Liedo P, Toledo J (2018) Sexual competitiveness, field survival, and dispersal of Anastrepha obliqua (Diptera: Tephritidae) fruit flies irradiated at different doses. J Econ Entomol 111:761–769
Sambrook J, Russell DW (2001) Preparation and analysis of eukaryotic genomic DNA. In: Sambrook J (ed) Molecular cloning: laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, NY
Support Illumina. 16S Metagenomic sequencing library preparation part # 15044223 Rev. B [internet]. Available in: https://support.illumina.com/documents/documentation/chemistry_documentation/16s/16s-metagenomic-library-prep-guide-15044223-b.pdf (Accessed 17Jan 2022)
Andrews S (2010) FastQC: A Quality Control Tool for High Throughput Sequence Data [internet]. Available at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (Accessed 29 March 202)
Gallo-Franco JJ, Toro-Perea N (2020) Variations in the bacterial communities in Anastrepha obliqua (Diptera: Tephritidae) according to the insect life stage and host plant. Curr Microbiol 77:1283–1291. https://doi.org/10.1007/s00284-020-01939-y
Marcel M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal. https://doi.org/10.14806/ej.17.1.200
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B, Grisel O, Blondel M, Prettenhofer P, Weiss R, Dubourg V, Vanderplas J, Passos A, Cournapeau D, Brucher M, Perrot M, Duchesnay E (2011) Scikit-learn: machine learning in python. J Mach Learn Res 12:2825–2830
Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Le S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18. https://doi.org/10.18637/jss.v025.i01
Tsirogiannis C, Sandel B (2017) PhyloMeasures: Fast and exact algorithms for computing phylogenetic biodiversity measures. R package version 2.1. https://CRAN.R-project.org/package=PhyloMeasures
Paradis E, Schliep K (2019) Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2020) Vegan: community ecology package. R package version 2.5–7. https://CRAN.R-project.org/package=vegan
Bioinformatics & Evolutionary Genomics [internet]. Available in: http://bioinformatics.psb.ugent.be/webtools/Venn/ Accessed 29 Ma 2021
Msaad-Guerfali M, Djobbi W, Charaabi K, Hamden H, Fadhl S, Marzouki W, Chevrier C (2018) Evaluation of Providencia rettgeri pathogenicity against laboratory Mediterranean fruit fly strain (Ceratitis capitata). PLoS ONE 13:1–18. https://doi.org/10.1371/journal.pone.0196343
Roque-Romero L, Hernández E, Aceituno-Medina M, Ventura C, Toledo J, Malo EA (2020) Attractiveness and sexual competitiveness of Anastrepha obliqua males (Diptera: Tephritidae) fed on a diet enriched with Providencia rettgeri. Front Microbiol 11:1777. https://doi.org/10.3389/fmicb.2020.01777
Scolari F, Sandionigi A, Carlassara M, Bruno A, Casiraghi M, Bonizzoni M (2021) Exploring changes in the microbiota of Aedes albopictus: comparison among breeding site water, larvae, and adults. Front Microbiol 12:624170. https://doi.org/10.3389/fmicb.2021.624170
Benelli G, Romano D (2018) Does indirect mating trophallaxis boost male mating success and female egg load in Mediterranean fruit flies? J Pest Sci 91:181–188. https://doi.org/10.1007/s10340-017-0854-z
Mateos M, Martinez-Montoya H, Lanzavecchia SB, Conte C, Guillén K, Morán-Aceves BM, Toledo J, Liedo P, Asimakis ED, Doudoumis V, Kyritsis GA, Papadopoulos NT, Augustinos AA, Segura DF, Tsiamis G (2020) Wolbachia pipientis associated with tephritid fruit fly pests: from basic research to applications. Front Microbiol 11:1080. https://doi.org/10.3389/fmicb.2020.01080
Lauzon CR, Potter SE (2012) Description of the irradiated and nonirradiated midgut of Ceratitis capitata Wiedemann (Diptera: Tephritidae) and Anastrepha ludens Loew (Diptera: Tephritidae) used for sterile insect technique. J Pest Sci 85:217–226. https://doi.org/10.1007/s10340-011-0410-1
McNulty SN, Mann PR, Robinson JA, Duncavage EJ, Pfeifer JD (2020) Impact of reducing DNA input on next-generation sequencing library complexity and variant detection. JMD 22:720–727
Acknowledgements
We thank Edouard Jurkevitch for reviewing an earlier draft of this manuscript. We also thank Luis Mario Herrera-Mazon, Damara I. Gómez Olea, Oscar Carmona Castro, Azucena Oropeza Cabrera, Gamaliel Mejía González, Luz Verónica García Fajardo, and Javier Francisco Valle Mora for technical assistance. The Moscafrut facility (SENASICA, SADER) for providing the mass-reared insects and the irradiation facilities.
Funding
This research project was partially funded by the Mexican National Fruit Fly Program/SENASICA/SADER, the National Council for Science and Technology (CONACYT) through project 316135 “Biorational alternatives for the management of fruit flies without agrotoxics, and its interaction with glyphosate residues in the region of Soconusco, Chiapas,” and ECOSUR. It was carried out as a partial requirement for LR-R’s doctoral degree. LR-R was granted a scholarship by CONACYT (CVU 711016).
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Experimental design by all authors. Experimental work by LR-R. Molecular and statistical analyses by LR-R and EZ. Preparing first draft LR-R. All authors made contributions in drafting the manuscript, revising it critically for important intellectual content, and approve the submitted version.
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Roque-Romero, L., Guillén-Navarro, K., Zarza, E. et al. Bacterial Diversity Associated with Anastrepha obliqua Males Change Under Mass-Rearing Conditions and with Irradiation. Curr Microbiol 80, 26 (2023). https://doi.org/10.1007/s00284-022-03111-0
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DOI: https://doi.org/10.1007/s00284-022-03111-0