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Disentangling the gut bacterial communities of the agave weevil, Scyphophorus acupunctatus (Coleoptera: Curculionidae)

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Abstract

The agave weevil, Scyphophorus acupunctatus, is a pest of agave. Its larvae cause damage to agaves by boring holes in the plant. Boring requires that the insect consume the constituents of its host plant, which contains sugars and many recalcitrant polymers. It has been hypothesized for many years that the gut bacterial communities of S. acupunctatus play a role in its ability to metabolize agave components. However, studies exploring this insect's gut bacterial communities have yet to be performed. In this work, we used a 16S rRNA gene-based metabarcoding approach to characterize the gut bacterial communities of field-collected agave weevils from different localities in Mexico. We found that external factors, including host plants, have important effects on the structure of the gut bacterial communities of S. acupunctatus. Despite this variability, we found a discrete core bacterial community mainly composed of the genera Prevotella, Pectinatus, Liquorilactobacillus, Secundilactobacillus, Paucilactobacillus, and Pseudomonas. These genera may be necessary for S. acupunctatus as metabolic helpers and/or gatekeepers. Additional studies are needed to fully assess the functionality of the gut bacterial community of this species in terms of its metabolic contribution, which may help to decipher their potential ecological implications. The information we provided here is the first step for guiding further questions.

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References

  • Adams AS, Adams SM, Currie CR, Gillette NE, Raffa KF (2010) Geographic variation in bacterial communities associated with the red turpentine beetle (Coleoptera: Curculionidae). Environ Entomol 39(2):406–414

    Article  PubMed  Google Scholar 

  • Almeida LGD, Moraes LABD, Trigo JR, Omoto C, Consoli FL (2017) The gut microbiota of insecticide-resistant insects houses insecticide-degrading bacteria: A potential source for biotechnological exploitation. PLoS ONE 12(3):e0174754. https://doi.org/10.1371/journal.pone.0174754

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Angzzas SMK, Ashuvila MA, Dayang NFAZ (2016) Potential lignin degraders isolated from the gut of Rhynchophorus ferrugineus. In: International Conference on Mechanics, Materials and Structural Engineering (ICMMSE 2016). Atlantis Press, pp 124–130. https://doi.org/10.2991/icmmse-16.2016.22

  • Aquino-Bolaños T, Sánchez-García JA, Ortíz-Hernández YD, Hernández-Cruz J, Cortés-Martínez CI (2020) Carrier and vector of Pectobacterium carotovorum subsp. carotovorum and its handling through a base of entomopathogenic fungi in Agave sp. Fla Entomol 103(2):243–246

    Article  Google Scholar 

  • Axelsson L, Ahrné S (2000) Lactic acid bacteria. Applied microbial systematics. Springer Netherlands, Dordrecht, pp 367–388

    Chapter  Google Scholar 

  • Bez C, Esposito A, Thuy HD et al (2021) The rice foot rot pathogen dickeya zeae alters the in-field plant microbiome. Environ Microbiol 23(12):7671–7687

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brindle PA, Baker FC, Tsai LW, Reuter CC, Schooley DA (1987) Sources of propionate for the biogenesis of ethyl-branched insect juvenile hormones: role of isoleucine and valine. Proc Natl Acad Sci U S A 84(22):7906–7910. https://doi.org/10.1073/pnas.84.22.7906

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cao Y, Dong Q, Wang D, Zhang P, Liu Y, Niu C (2022) MicrobiomeMarker: an R/Bioconductor package for microbiome marker identification and visualization. Bioinformatics 38(16):4027–4029. https://doi.org/10.1093/bioinformatics/btac438

    Article  CAS  PubMed  Google Scholar 

  • 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(7):581–583

  • Callahan BJ, McMurdie PJ, Holmes SP (2017) Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 11(12):2639–2643

  • Ceja-Navarro JA, Vega FE, Karaoz U, Hao Z et al (2015) Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat Commun 6:7618. https://doi.org/10.1038/ncomms8618

    Article  CAS  PubMed  Google Scholar 

  • Chakraborty A, Ashraf MZ, Modlinger R, Synek J, Schlyter F, Roy A (2020) Unravelling the gut bacteriome of Ips (Coleoptera: Curculionidae: Scolytinae): identifying core bacterial assemblage and their ecological relevance. Sci Rep 10:18572

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chakraborty A, Purohit A, Khara A, Modlinger R, Roy A (2023) Life-stage and geographic location determine the microbial assemblage in Eurasian spruce bark beetle, Ips typographus L. (Coleoptera: Curculionidae). Front For Glob Change 6(1176160):10–3389

    Google Scholar 

  • Chelack BJ, Ingledew WM (1987) Anaerobic Gram-negative bacteria in brewing - a review. J Am Soc Brew Chem 45(4):123–127

    CAS  Google Scholar 

  • Clemens K (2015) Geocoding with openstreetmap data. GEOProcessing 10

  • Corbin K, Byrt C, Bauer S, DeBolt S, Chambers D et al (2015) Prospecting for energy-rich renewable raw materials: agave leaf case study. PLoS ONE 8(10):e0135382. https://doi.org/10.1371/journal.pone.0135382

    Article  CAS  Google Scholar 

  • Cruz Faustino JJ, Figueroa Castro P, Alcántara Jimenéz JA, López Martínez V, Silva García F (2019) Vegetal synergists for trapping the adult of Scyphophorus acupunctatus Gyllenhal, in pheromone baited traps, in Agave angustifolia Haw., in Morelos, Mexico. Acta Zool Mex 35. https://doi.org/10.21829/azm.2019.3502187

  • Cruz-Jardón LF, Figueroa-Castro P, López-Martínez V, Pérez-Figueroa M (2018) Semiochemicals-baited traps for detecting and estimating the population density of Scyphophorus acupunctatus Gyllenhal (Coleoptera: Dryopthoridae), in agaves, in Tlaquiltenango, Morelos. Acta Zool Mex 34. https://doi.org/10.21829/azm.2018.3412163

  • Cuervo-Parra JA, Pérez-España VH, Pérez PAL, Morales-Ovando MA, Arce-Cervantes O, Aparicio-Burgos JE, Romero-Cortes T (2019) Scyphophorus acupunctatus (Coleoptera: Dryophthoridae): a weevil threatening the production of agave in Mexico. Fla Entomol 102:1–9

    Article  Google Scholar 

  • Da Silva Brito SS, Villa M, Benhadi-Marín J, da Silva F, Pereira JA (2021) The temporal and spatial variation of arthropod associations inhabiting non-crop vegetation in a Sisal crop, Agave sisalana in the Caatinga biome. Appl Sci 11(14):6498. https://doi.org/10.3390/app11146498

    Article  CAS  Google Scholar 

  • Daisley BA, Pitek AP, Chmiel, et al (2020) Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees. Commun Biol 3(1):534. https://doi.org/10.1038/s42003-020-01259-8

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Desgarennes D, Garrido E, Torres-Gomez MJ et al (2014) Diazotrophic potential among bacterial communities associated with wild and cultivated Agave species. FEMS Microbiol Ecol 90(3):844–857. https://doi.org/10.1111/1574-6941.12438

    Article  CAS  PubMed  Google Scholar 

  • Desnoues N, Lin M, Guo X, Ma L, Carreño-Lopez R, Elmerich C (2003) Nitrogen fixation genetics and regulation in a Pseudomonas stutzeri strain associated with rice. Microbiology 149(8):2251–2262

    Article  CAS  PubMed  Google Scholar 

  • Dodd D, Moon YH, Swaminathan K, Mackie RI, Cann IK (2010) Transcriptomic analyses of xylan degradation by Prevotella bryantii and insights into energy acquisition by xylanolytic bacteroidetes. J Biol Chem 285(39):30261–30273. https://doi.org/10.1074/jbc.M110.141788

    Article  PubMed Central  PubMed  Google Scholar 

  • Dumond L, Lam LPY et al (2021) Termite gut microbiota contribution to wheat straw delignification in anaerobic bioreactors. ACS Sustain Chem Eng 9(5):2191–2202. https://doi.org/10.1021/acssuschemeng.0c07817

    Article  CAS  Google Scholar 

  • Dunnington D, Thorne B (2020) ggspatial: Spatial Data Framework for ggplot2. R package version 1.1.4

  • Farine JP, Habbachi W, Cortot J, Roche S, Ferveur JF (2017) Maternally-transmitted microbiota affects odor emission and preference in Drosophila larvae. Sci Rep 7(1):6062. https://doi.org/10.1038/s41598-017-04922-z

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Figueroa-Castro P, González-Hernández H, Carrillo-Sánchez JL, Solís-Aguilar JF, Real-Laborde JId, Rojas JC (2016) Effect of the height and distribution pattern of pheromone-baited traps on the capture of Scyphophorus acupunctatus (Coleoptera: Dryophthoridae) on blue agave (Asparagales: Asparagaceae). Fla Entomol 2(99):297–299. https://doi.org/10.1653/024.099.0222

    Article  Google Scholar 

  • Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6(2):121–131. https://doi.org/10.1038/nrmicro1817

    Article  CAS  PubMed  Google Scholar 

  • Fox AR, Soto G, Valverde C et al (2016) Major cereal crops benefit from biological nitrogen fixation when inoculated with the nitrogen-fixing bacterium Pseudomonas protegens Pf-5 X940. Environ Microbiol 18(10):3522–3534

    Article  CAS  PubMed  Google Scholar 

  • George AS et al (2018) Interactions of Salmonella enterica serovar Typhimurium and Pectobacterium carotovorum within a tomato soft rot. Appl Environ Microbiol 84(5):e01913-e1917

    Article  PubMed Central  PubMed  Google Scholar 

  • Gálvez EJ, Iljazovic A, Amend L, Lesker TR, Renault T, Thiemann S, Strowig T (2020) Distinct polysaccharide utilization determines interspecies competition between intestinal Prevotella spp. Cell Host & Microbe 28(6):838–852

  • González-Hernández H, Solís-Aguilar JF, Pacheco Sánchez C, Flores-Mendoza FJ, Rubio-Cortés R, Rojas-León JC (2007) Insectos barrenadores del agave tequilero. In: González-Hernandéz H, del Real Laborde JI, Solís-Aguilar JF (eds), Manejo de Plagas del Agave Tequilero. Colegio de Postgraduados and Tequila Sauza, S.A. de C.V., Zapopan, Jalisco, México, pp 39–67

  • Grgas D, Rukavina M, Bešlo D, Štefanac T, Crnek V, Šikić T, ... Landeka Dragičević T (2023) The bacterial degradation of lignin—a review. Water 15(7):1272

  • He B, Chen X, Yang H, Cernava T (2021) Microbiome structure of the aphid Myzus persicae (Sulzer) is shaped by different solanaceae plant diets. Front Microbiol 12:667257. https://doi.org/10.3389/fmicb.2021.667257

    Article  PubMed Central  PubMed  Google Scholar 

  • Huang K, Wang J, Huang J et al (2021) Host phylogeny and diet Shape gut microbial communities within bamboo-feeding insects. Front Microbiol 12:633075. https://doi.org/10.3389/fmicb.2021.633075

    Article  PubMed Central  PubMed  Google Scholar 

  • Ibarra-Juárez LA et al (2020) Evidence for succession and putative metabolic roles of fungi and bacteria in the farming mutualism of the ambrosia beetle Xyleborus affinis. Msystems 5(5):e00541-e620. https://doi.org/10.1128/mSystems.00541-20

    Article  PubMed Central  PubMed  Google Scholar 

  • Iorizzo M, Letizia F, Ganassi S et al (2022) Functional properties and antimicrobial activity from lactic acid bacteria as resources to improve the health and welfare of honey bees. Insects 13(3):308. https://doi.org/10.3390/insects13030308

    Article  PubMed Central  PubMed  Google Scholar 

  • Jones AG, Mason CJ, Felton GW, Hoover K (2019) Host plant and population source drive diversity of microbial gut communities in two polyphagous insects. Sci Rep 9:2792

    Article  PubMed Central  PubMed  Google Scholar 

  • Juvonen R, Suihko M (2006) Megasphaera paucivorans Sp. Nov, Megasphaera sueciensis sp. nov. and Pectinatus haikarae sp. nov., isolated from brewery samples, and emended description of the genus Pectinatus. Int J Syst Evol Microbiol 4(56):695–702. https://doi.org/10.1099/ijs.0.63699-0

    Article  CAS  Google Scholar 

  • Kabel MA, Yeoman CJ, Han Y et al (2011) Biochemical characterization and relative expression levels of multiple carbohydrate esterases of the xylanolytic rumen bacterium Prevotella ruminicola 23 grown on an ester-enriched substrate. Appl Environ Microbiol 77(16):5671–5681. https://doi.org/10.1128/AEM.05321-11

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kahle DJ, Wickham H (2013) ggmap: spatial visualization with ggplot2. R J 5(1):144

    Article  Google Scholar 

  • Kampers LF, Koehorst JJ, van Heck RJ, Suarez-Diez M, Stams AJ, Schaap PJ (2021) A metabolic and physiological design study of Pseudomonas putida KT2440 capable of anaerobic respiration. BMC Microbiol 21:1–15. https://doi.org/10.1186/s12866-020-02058-1

    Article  CAS  Google Scholar 

  • Kim JN, Méndez-García C, Geier RR et al (2017) Metabolic networks for nitrogen utilization in Prevotella ruminicola 23. Sci Rep 7:7851. https://doi.org/10.1038/s41598-017-08463-3

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41(1), e1-e1

  • Lahti L, Shetty S (2012) microbiome R package (2012–2019)

  • Lee SY, Mabee MS, Jangaard NO (1978) Pectinatus, a new genus of the family Bacteroidaceae. Int J Syst Bacteriol 4(28):582–594. https://doi.org/10.1099/00207713-28-4-582

    Article  Google Scholar 

  • Li J, Wang S, Zhao J, Dong Z, Shao T (2022) Gut microbiota of Ostrinia nubilalis larvae degrade maize cellulose. Front Microbiol 13:816954. https://doi.org/10.3389/fmicb.2022.816954

    Article  PubMed Central  PubMed  Google Scholar 

  • López-Bautista V, Mora-Aguilera G, Gutiérrez-Espinosa MA et al (2020) Morphological and molecular characterization of Fusarium spp. associated to the regional occurrence of wilt and dry bud rot in Agave tequilana. Rev Mex Fitopat 38:79–106. https://doi.org/10.18781/r.mex.fit.1911-4

    Article  Google Scholar 

  • Miyazaki K, Martin JC, Marinsek-Logar R, Flint HJ (1997) Degradation and utilization of xylans by the rumen anaerobe Prevotella bryantii (formerly P. ruminicola subsp. brevis) B14. Anaerobe 3(6):373–381. https://doi.org/10.1006/anae.1997.0125

    Article  CAS  PubMed  Google Scholar 

  • McMurdie, P. J., & Holmes, S. (2013). phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PloS one 8(4):e61217

  • Munive F, Páez M, Romero-Granja C, Espín N, Casa-Villegas M (2014) Fermentation of Agave americana L. sap produced in Cayambe-Ecuador. Rev Bionatura 8:15

    Google Scholar 

  • Ortiz-Basurto R, Pourcelly G, Doco T, Williams P, Dornier M, Belleville M (2008) Analysis of the main components of the aguamiel produced by the maguey-pulquero (Agave mapisaga) throughout the harvest period. J Agric Food Chem 10(56):3682–3687. https://doi.org/10.1021/jf072767h

  • Osei R, Yang C, Cui L, Ma T, Li Z, Boamah S (2022) Isolation, identification, and pathogenicity of Lelliottia amnigena causing soft rot of potato tuber in China. Microb Pathog 164:105441. https://doi.org/10.1016/j.micpath.2022.105441

    Article  CAS  PubMed  Google Scholar 

  • Palemón-Alberto F, Ortega-Acosta SA, Domínguez-Monge S, Castañeda-Vildozola A, Reyes-García G, Cruz-Lagunas B, Flores-Simon OU (2021) First report of bud soft rot on Agave angustifolia caused by Pantoea dispersa in México. Plant Dis 105(10):3286. https://doi.org/10.1094/PDIS-02-21-0316-PDN

  • Palemón-Alberto F, Ortega-Acosta SA, Castañeda-Vildozola A, Reyes-García G et al (2022) Damage by Scyphophorus acupunctatus Gyllenhal in Species of Agave. Southwest Entomol 47(2):437–442. https://doi.org/10.3958/059.047.0219

  • Paradh AD (2015) Gram-negative spoilage bacteria in brewing. In: Brewing microbiology. Woodhead Publishing, pp 175–194

  • Poveda J (2021) Insect frass in the development of sustainable agriculture. A Review. Agron Sustain Dev 41:5. https://doi.org/10.1007/s13593-020-00656-x

    Article  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41(Database issue):D590–6. https://doi.org/10.1093/nar/gks1219

  • R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/ Accessed 23 Mar 2023

  • Rendón-Salcido LA, Colunga-GarcíaMarín P, Barahona-Pérez LF et al (2009) Sugars and alcoholic byproducts from henequen (Agave fourcroydes) as influenced by plant age and climate. Rev Fitotec 32:39–44

    Google Scholar 

  • Reyes-Zambrano SJ, Lecona-Guzmán CA, Gutiérrez-Miceli, et al (2020) Scanning electron microscopy and enzymatic analysis in Agave americana during Fusarium oxysporum infection. Rev Mex Fitopatol 38(3):408–419. https://doi.org/10.18781/r.mex.fit.2005-3

    Article  Google Scholar 

  • Robacker DC, Lauzon CR (2002) Purine metabolizing capability of Enterobacter agglomerans affects volatiles production and attractiveness to Mexican fruit fly. J Chem Ecol 28:1549–1563. https://doi.org/10.1023/a:1019920328062

    Article  CAS  PubMed  Google Scholar 

  • Rozadilla G, Cabrera N, Virla E, Greco N, McCarthy C (2020) Gut Microbiota of Spodoptera frugiperda (J.E. Smith) larvae as revealed by metatranscriptomic analysis. J Appl Entomol 5(144):351–363. https://doi.org/10.1111/jen.12742

    Article  CAS  Google Scholar 

  • Rubio-Cortés R (2007) Enfermedades del cultivo de agave. In: Rulfo-Vilchis O, Pérez-Domínguez JF, del Real Laborde JI, Byerly-Murphy KF (eds), Conocimiento y prácticas agronómicas para la producción de Agave tequilana Weber en la zona de denominación de origen del tequila. Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias. Centro de Investigación Regional del Pacífico Centro. Libro técnico Núm. 4. México, pp. 169–195

  • Saïd I, Renou M, Morin JP, Ferreira JM, Rochat D (2005) Interactions between acetoin, a plant volatile, and pheromone in Rhynchophorus palmarum: Behavioral and olfactory neuron responses. J Chem Ecol 31:1789–1805. https://doi.org/10.1007/s10886-005-5927-4

    Article  CAS  PubMed  Google Scholar 

  • Sanow S, Kuang W, Schaaf G et al (2023) Molecular mechanisms of Pseudomonas assisted plant nitrogen uptake-opportunities for modern agriculture. Mol Plant Microbe Interact. https://doi.org/10.1094/MPMI-10-22-0223-CR

  • Sawada H, Fujikawa T, Tsuji M, Satou M (2021) Pseudomonas allii sp. nov., a pathogen causing soft rot of onion in Japan. Int J Syst Evol Microbiol 71:004582. https://doi.org/10.1099/ijsem.0.004582

    Article  CAS  Google Scholar 

  • Shukla SP, Sanders JG, Byrne MJ, Pierce NE (2016) Gut microbiota of dung beetles correspond to dietary specializations of adults and larvae. Mol Ecol 25(24):6092–6106

    Article  CAS  PubMed  Google Scholar 

  • Solís-Aguilar JF, González-Hernández H, Leyva-Vázquez JL, Equihua-Martínez A, Flores Mendoza FJ, Martínez-Garza A (2001) Scyphophorus acupunctatus Gyllenhal, plaga del agave tequilero en Jalisco, México. Agrociencia 35(6):663–670

  • Suárez-Moo P, Cruz-Rosales M, Ibarra-Laclette E et al (2020) Diversity and composition of the gut microbiota in the developmental stages of the dung beetle Copris incertus Say (Coleoptera, Scarabaeidae). Front Microbiol 11:1698. https://doi.org/10.3389/fmicb.2020.01698

    Article  PubMed Central  PubMed  Google Scholar 

  • Ueki A, Akasaka H, Satoh A, Suzuki D, Ueki K (2007) Prevotella paludivivens sp. nov., a novel strictly anaerobic, gram-negative, hemicellulose-decomposing bacterium isolated from plant residue and rice roots in irrigated rice-field soil. Int J Syst Evol Microbiol 57:1803–1809. https://doi.org/10.1099/ijs.0.64914-0

    Article  PubMed  Google Scholar 

  • Valdés-Rodríguez S, Ramírez-Choza JL, Reyes-López J, Blanco-Labra A (2004) Respuestas del insecto Max (Scyphophorus acupunctatus Gyllenhal [Coleoptera: Curculionidae] hacia algunos compuestos atrayentes del henequén. Acta Zool Mex 20(3):157–166

    Article  Google Scholar 

  • Vásquez A, Forsgren E, Fries I et al (2012) Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS ONE 7(3):e33188. https://doi.org/10.1371/journal.pone.0033188

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vega-Petlacalco M, Arzuffi R, Valdez J et al (2018) Food quality influences ovarian development Inscyphophorus acupunctatus (Coleoptera: Dryophthoridae). Fla Entomol 3(101):447–452. https://doi.org/10.1653/024.101.0301

    Article  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang L, Liu T, Wu Y et al (2018) Bacterial microbiota assemblage in Aedes albopictus mosquitoes and its impacts on larval development. Mol Ecol 14(27):2972–2985. https://doi.org/10.1111/mec.14732

  • Wang K, Gao P, Geng L, Liu C, Zhang J, Shu C (2022) Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line. Microbiome 10:1–16

    Article  Google Scholar 

  • Waring GL, Smith RL (1986) Natural history and ecology of Scyphophorus acupunctatus (Coleoptera: Curculionidae) and its associated microbes in cultivated and native agaves. Ann Entomol Soc Am 79(2):334–340. https://doi.org/10.1093/aesa/79.2.334

    Article  Google Scholar 

  • Wickham H (2011) ggplot2. Wiley interdisciplinary reviews: computational statistics. 3(2):180–185

  • Xie S, Lan Y, Sun C, & Shao, Y. (2019). Insect microbial symbionts as a novel source for biotechnology. World J Microbiol Biotechnol 35:1–7

  • Xu S et al (2021) ggtreeExtra: compact visualization of richly annotated phylogenetic data. Mol Biol Evol 38(9):4039–4042

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu S, Zhan L, Tang W et al (2023) MicrobiotaProcess: a comprehensive R package for deep mining microbiome. The Innovation 4(2). https://doi.org/10.18129/B9.bioc.MicrobiotaProcess

  • Yu G (2020) Using ggtree to visualize data on tree-like structures. Curr Protocol Bioinforma 69:e96

    Article  Google Scholar 

  • Yun J et al (2014) Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol 80(17):5254–5264

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhao X, Tian Y, Yue L et al (2022) Identification and characterization of pathogenicity of Lelliottia nimipressuralis causing soft rot of Codonopsis pilosula (dangshen) roots in China. Plant Pathol 71(8):1801–1811. https://doi.org/10.1111/ppa.13606

    Article  CAS  Google Scholar 

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Acknowledgements

Salazar-Rivera G.I. thanks Mexico’s Consejo Nacional de Humanidades, Ciencias y Tecnología (CONAHCYT) for postdoctoral fellowship 239732 and the Centro de Investigación y Asistencia Tecnológica del Estado de Jalisco (CIATEJ). The anonymous reviewers deserve gratitude for their constructive feedback, which significantly enhanced this article. This research was supported by CONAHCYT-FORDECYT 292474 and 296369.

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JNEV, EIL, JAZB.

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Conceived and designed the analysis: GSR, JNEV, APS, JAZB.

Collected the data: GSR, MOM, JNEV.

Contributed data or analysis tools: GSR, MOM, JNEV, JAZB.

Performed the analysis: GSR, AGMAC, APS, JAZB.

Review and edit the manuscript: AGMAC, EIL, IMHV.

Wrote the paper: GSR, APS, IMHV, JNEV, JAZB.

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Correspondence to Jhony Navat Enríquez-Vara or Jesús Alejandro Zamora-Briseño.

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Salazar-Rivera, G.I., Pereira-Santana, A., Hernández-Velázquez, I.M. et al. Disentangling the gut bacterial communities of the agave weevil, Scyphophorus acupunctatus (Coleoptera: Curculionidae). Symbiosis 92, 381–392 (2024). https://doi.org/10.1007/s13199-024-00978-4

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