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Section: Microbiology
Topic: Agricultural sciences, Ecology, Microbiology

Diversity of bacterial symbionts associated with the tropical plant bug Monalonion velezangeli (Hemiptera: Miridae) revealed by high-throughput 16S-rRNA sequencing

Navarro-Escalante, Lucio1  ; Benavides, Pablo1 ; Acevedo, Flor E.2 
1 Disciplina de Entomología, Centro Nacional de Investigaciones de Café - CENICAFÉ. Manizales, Colombia
2 Department of Entomology, Pennsylvania State University, University Park, PA, United States

10.24072/pcjournal.362 - Peer Community Journal, Volume 4 (2024), article no. e7.

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Insects and microbes have developed complex symbiotic relationships that evolutionarily and ecologically play beneficial roles for both, the symbiont and the host. In most Hemiptera insects, bacterial symbionts offer mainly nutritional, defensive, and reproductive roles in addition to promoting the adaptive radiation of several hemipteran phytophagous lineages. The tropical plant bug Monalonion velezangeli (Hemiptera: Miridae) is a polyphagous herbivore considered an important insect pest for several economically relevant tropical crops, but information about the composition of its bacterial microbiota was missing. In this study, we describe the diversity and structure of the bacterial microbiota in the nymph and adult life stages of M. velezangeli using Illumina high-throughput sequencing of 16S ribosomal RNA gene amplicons (meta-barcoding). We found that both insect life stages share a similar microbiota in terms of bacterial diversity and community structure. The intracellular symbiont Wolbachia dominated the overall microbiome composition (~92%) in these life stages. Members of the core microbiota include Wolbachia, Romboutsia, Ignavibacterium, Clostridium, Allobaculum, Paracoccus, Methylobacterium, Faecalibacterium, Collinsella, Rothia, Sphingomonas and 4 other undetermined bacterial genera. Based on PCR screening and DNA sequencing of the wsp gene, Wolbachia infection was confirmed in almost 80% of samples, and represented by two different isolates or strains within the supergroup B. This data offers opportunities for studying the contribution of symbiotic bacteria in the biological performance of this insect pest, and provides a base to explore other insect control methods.

Published online:
DOI: 10.24072/pcjournal.362
Type: Research article
Keywords: bacterial microbiota, endosymbiont, plant bug, Wolbachia, Monalonion, Coffea
Navarro-Escalante, Lucio 1; Benavides, Pablo 1; Acevedo, Flor E. 2

1 Disciplina de Entomología, Centro Nacional de Investigaciones de Café - CENICAFÉ. Manizales, Colombia
2 Department of Entomology, Pennsylvania State University, University Park, PA, United States
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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     title = {Diversity of bacterial symbionts associated with the tropical plant bug {\protect\emph{Monalonion}} \protect\emph{velezangeli} {(Hemiptera:} {Miridae)} revealed by high-throughput {16S-rRNA} sequencing},
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Navarro-Escalante, Lucio; Benavides, Pablo; Acevedo, Flor E. Diversity of bacterial symbionts associated with the tropical plant bug Monalonion velezangeli (Hemiptera: Miridae) revealed by high-throughput 16S-rRNA sequencing. Peer Community Journal, Volume 4 (2024), article  no. e7. doi : 10.24072/pcjournal.362. https://peercommunityjournal.org/articles/10.24072/pcjournal.362/

Peer reviewed and recommended by PCI : 10.24072/pci.microbiol.100004

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Acevedo, F. E.; Peiffer, M.; Tan, C.-W.; Stanley, B. A.; Stanley, A.; Wang, J.; Jones, A. G.; Hoover, K.; Rosa, C.; Luthe, D.; Felton, G. Fall Armyworm-associated gut bacteria modulate plant defense responses, Molecular Plant-Microbe Interactions, Volume 30 (2017) no. 2, pp. 127-137 (Publisher: Scientific Societies) | DOI

[2] Anderson, M. J. A new method for non‐parametric multivariate analysis of variance, Austral Ecology, Volume 26 (2001) no. 1, pp. 32-46 | DOI

[3] Anderson, M. J.; Walsh, D. C. I. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing?, Ecological Monographs, Volume 83 (2013) no. 4, pp. 557-574 | DOI

[4] Anisimova, M.; Gascuel, O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative, Systematic Biology, Volume 55 (2006) no. 4, pp. 539-552 | DOI

[5] Bi, J.; Wang, Y.-F. The effect of the endosymbiont Wolbachia on the behavior of insect hosts, Insect Science, Volume 27 (2020) no. 5, pp. 846-858 | DOI

[6] Blanton, A. G.; Peterson, B. F. Symbiont-mediated insecticide detoxification as an emerging problem in insect pests, Frontiers in Microbiology, Volume 11 (2020) | DOI

[7] Bolyen, E.; Rideout, J. R.; Dillon, M. R.; Bokulich, N. A.; Abnet, C. C.; Al-Ghalith, G. A.; Alexander, H.; Alm, E. J.; Arumugam, M.; Asnicar, F.; Bai, Y.; Bisanz, J. E.; Bittinger, K.; Brejnrod, A.; Brislawn, C. J.; Brown, C. T.; Callahan, B. J.; Caraballo-Rodríguez, A. M.; Chase, J.; Cope, E. K.; Da Silva, R.; Diener, C.; Dorrestein, P. C.; Douglas, G. M.; Durall, D. M.; Duvallet, C.; Edwardson, C. F.; Ernst, M.; Estaki, M.; Fouquier, J.; Gauglitz, J. M.; Gibbons, S. M.; Gibson, D. L.; Gonzalez, A.; Gorlick, K.; Guo, J.; Hillmann, B.; Holmes, S.; Holste, H.; Huttenhower, C.; Huttley, G. A.; Janssen, S.; Jarmusch, A. K.; Jiang, L.; Kaehler, B. D.; Kang, K. B.; Keefe, C. R.; Keim, P.; Kelley, S. T.; Knights, D.; Koester, I.; Kosciolek, T.; Kreps, J.; Langille, M. G. I.; Lee, J.; Ley, R.; Liu, Y.-X.; Loftfield, E.; Lozupone, C.; Maher, M.; Marotz, C.; Martin, B. D.; McDonald, D.; McIver, L. J.; Melnik, A. V.; Metcalf, J. L.; Morgan, S. C.; Morton, J. T.; Naimey, A. T.; Navas-Molina, J. A.; Nothias, L. F.; Orchanian, S. B.; Pearson, T.; Peoples, S. L.; Petras, D.; Preuss, M. L.; Pruesse, E.; Rasmussen, L. B.; Rivers, A.; Robeson, M. S.; Rosenthal, P.; Segata, N.; Shaffer, M.; Shiffer, A.; Sinha, R.; Song, S. J.; Spear, J. R.; Swafford, A. D.; Thompson, L. R.; Torres, P. J.; Trinh, P.; Tripathi, A.; Turnbaugh, P. J.; Ul-Hasan, S.; van der Hooft, J. J. J.; Vargas, F.; Vázquez-Baeza, Y.; Vogtmann, E.; von Hippel, M.; Walters, W.; Wan, Y.; Wang, M.; Warren, J.; Weber, K. C.; Williamson, C. H. D.; Willis, A. D.; Xu, Z. Z.; Zaneveld, J. R.; Zhang, Y.; Zhu, Q.; Knight, R.; Caporaso, J. G. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2, Nature Biotechnology, Volume 37 (2019) no. 8, pp. 852-857 | DOI

[8] Callahan, B. J.; McMurdie, P. J.; Rosen, M. J.; Han, A. W.; Johnson, A. J. A.; Holmes, S. P. DADA2: High-resolution sample inference from Illumina amplicon data, Nature Methods, Volume 13 (2016) no. 7, pp. 581-583 | DOI

[9] Caporaso, J. G.; Lauber, C. L.; Walters, W. A.; Berg-Lyons, D.; Lozupone, C. A.; Turnbaugh, P. J.; Fierer, N.; Knight, R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample, Proceedings of the National Academy of Sciences of the United States of America, Volume 108 (2011) no. Suppl 1, pp. 4516-4522 | DOI

[10] Casper-Lindley, C.; Kimura, S.; Saxton, D. S.; Essaw, Y.; Simpson, I.; Tan, V.; Sullivan, W. Rapid fluorescence-based screening for Wolbachia endosymbionts in Drosophila germ line and somatic tissues, Applied and Environmental Microbiology, Volume 77 (2011) no. 14, pp. 4788-4794 | DOI

[11] Chandler, J. A.; James, P. M.; Jospin, G.; Lang, J. M. The bacterial communities of Drosophila suzukii collected from undamaged cherries, PeerJ, Volume 2 (2014), p. e474 | DOI

[12] Chong, J.; Liu, P.; Zhou, G.; Xia, J. Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data, Nature Protocols, Volume 15 (2020) no. 3, pp. 799-821 | DOI

[13] Chung, S. H.; Rosa, C.; Scully, E. D.; Peiffer, M.; Tooker, J. F.; Hoover, K.; Luthe, D. S.; Felton, G. W. Herbivore exploits orally secreted bacteria to suppress plant defenses, Proceedings of the National Academy of Sciences, Volume 110 (2013) no. 39, pp. 15728-15733 | DOI

[14] Dereeper, A.; Guignon, V.; Blanc, G.; Audic, S.; Buffet, S.; Chevenet, F.; Dufayard, J.-F.; Guindon, S.; Lefort, V.; Lescot, M.; Claverie, J.-M.; Gascuel, O. Phylogeny.fr: robust phylogenetic analysis for the non-specialist, Nucleic Acids Research, Volume 36 (2008) no. Web Server issue, pp. W465-469 | DOI

[15] Dhariwal, A.; Chong, J.; Habib, S.; King, I. L.; Agellon, L. B.; Xia, J. MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data, Nucleic Acids Research, Volume 45 (2017) no. W1, p. W180-W188 | DOI

[16] Diouf, M.; Miambi, E.; Mora, P.; Frechault, S.; Robert, A.; Rouland-Lefèvre, C.; Hervé, V. Variations in the relative abundance of Wolbachia in the gut of Nasutitermes arborum across life stages and castes, FEMS microbiology letters, Volume 365 (2018) no. 7 | DOI

[17] Dyson, P.; Figueiredo, M.; Andongma, A. A.; Whitten, M. M. A. Symbiont-mediated RNA interference (SMR): using symbiotic bacteria as vectors for delivering RNAi to insects, Methods in Molecular Biology (Clifton, N.J.), Volume 2360 (2022), pp. 295-306 | DOI

[18] Fang, J.-X.; Zhang, S.-F.; Liu, F.; Zhang, X.; Zhang, F.-B.; Guo, X.-B.; Zhang, Z.; Zhang, Q.-H.; Kong, X.-B. Differences in gut bacterial communities of Ips typographus (coleoptera: curculionidae) induced by enantiomer-specific α-pinene, Environmental Entomology, Volume 49 (2020) no. 5, pp. 1198-1205 | DOI

[19] Fu, Z.; Antwi, J. B.; Sword, G. A.; Barman, A. K.; Medina, R. F. Geographic variation of bacterial communities associated with cotton fleahopper, Pseudatomoscelis seriatus, Southwestern Entomologist, Volume 46 (2021) no. 1, pp. 17-32 (Publisher: Society of Southwestern Entomologists) | DOI

[20] Fukui, T.; Kawamoto, M.; Shoji, K.; Kiuchi, T.; Sugano, S.; Shimada, T.; Suzuki, Y.; Katsuma, S. The endosymbiotic bacterium Wolbachia selectively kills male hosts by targeting the masculinizing gene, PLOS Pathogens, Volume 11 (2015) no. 7, p. e1005048 | DOI

[21] Ge, S.-X.; Li, T.-F.; Ren, L.-L.; Zong, S.-X. Host-plant adaptation in xylophagous insect-microbiome systems: Contributionsof longicorns and gut symbionts revealed by parallel metatranscriptome, iScience, Volume 26 (2023) no. 5, p. 106680 | DOI

[22] Gerritsen, J.; Fuentes, S.; Grievink, W.; van Niftrik, L.; Tindall, B. J.; Timmerman, H. M.; Rijkers, G. T.; Smidt, H. Characterization of Romboutsia ilealis gen. nov., sp. nov., isolated from the gastro-intestinal tract of a rat, and proposal for the reclassification of five closely related members of the genus Clostridium into the genera Romboutsia gen. nov., Intestinibacter gen. nov., Terrisporobacter gen. nov. and Asaccharospora gen. nov, International Journal of Systematic and Evolutionary Microbiology, Volume 64 (2014) no. Pt 5, pp. 1600-1616 | DOI

[23] Gerritsen, J.; Hornung, B.; Renckens, B.; van Hijum, S. A. F. T.; Martins Dos Santos, V. A. P.; Rijkers, G. T.; Schaap, P. J.; de Vos, W. M.; Smidt, H. Genomic and functional analysis of Romboutsia ilealis CRIBT reveals adaptation to the small intestine, PeerJ, Volume 5 (2017), p. e3698 | DOI

[24] Gerritsen, J.; Hornung, B.; Ritari, J.; Paulin, L.; Rijkers, G. T.; Schaap, P. J.; Vos, W. M. d.; Smidt, H. A comparative and functional genomics analysis of the genus Romboutsia provides insight into adaptation to an intestinal lifestyle, bioRxiv, 2019 | DOI

[25] Giraldo-Jaramillo, M.; Benavides-Machado, P.; Villegas-Garcia., C. Aspectos morfológicos y biológicos de Monalonion velezangeli Carvalho and Costa Hemiptera : Miridae en café, Cenicafé, Volume 61 (2010) no. 3, pp. 195-205 https://www.cenicafe.org/es/publications/arc061(03)195-2052.pdf

[26] Giraldo-Jaramillo, M.; Machado, P. B. Conozca los hospedantes, sitios de alimentación y oviposición de la chinche de la chamusquina del café, Avances Técnicos Cenicafé (2012), pp. 1-8 (https://publicaciones.cenicafe.org/index.php/avances_tecnicos/article/view/500/553)

[27] Grech-Mora, I.; Fardeau, M.-L.; Patel, B. K. C.; Ollivier, B.; Rimbault, A.; PRENSIER, G.; GARCIA, J.-L.; GARNIER-SILLAM, E. Isolation and characterization of Sporobacter termitidis gen. nov., sp. nov., from the digestive tract of the wood-feeding termite Nasutitermes lujae, International Journal of Systematic and Evolutionary Microbiology, Volume 46 (1996) no. 2, pp. 512-518 | DOI

[28] Guindon, S.; Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood, Systematic Biology, Volume 52 (2003) no. 5, pp. 696-704 | DOI

[29] Hammer, Ø.; Harper, D.; Ryan, P. D. PAST: Paleontological statistics software package for education and data analysis, Palaeontologia Electronica, Volume 4 (2001) no. 1, pp. 1-9

[30] Henry, L. P.; Ayroles, J. F. Meta-analysis suggests the microbiome responds to evolve and resequence experiments in Drosophila melanogaster, BMC microbiology, Volume 21 (2021) no. 1, p. 108 | DOI

[31] Hilgenboecker, K.; Hammerstein, P.; Schlattmann, P.; Telschow, A.; Werren, J. H. How many species are infected with Wolbachia? A statistical analysis of current data, FEMS microbiology letters, Volume 281 (2008) no. 2, pp. 215-220 | DOI

[32] Hiroki, M.; Kato, Y.; Kamito, T.; Miura, K. Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae), Naturwissenschaften, Volume 89 (2002) no. 4, pp. 167-170 | DOI

[33] Hosokawa, T.; Koga, R.; Kikuchi, Y.; Meng, X.-Y.; Fukatsu, T. Wolbachia as a bacteriocyte-associated nutritional mutualist, Proceedings of the National Academy of Sciences, Volume 107 (2010) no. 2, pp. 769-774 | DOI

[34] Hughes, G. L.; Allsopp, P. G.; Brumbley, S. M.; Woolfit, M.; McGraw, E. A.; O'Neill, S. L. Variable infection frequency and high diversity of multiple strains of Wolbachia pipientis in Perkinsiella planthoppers, Applied and Environmental Microbiology, Volume 77 (2011) no. 6, pp. 2165-2168 | DOI

[35] Hurst, G. D. D.; Jiggins, F. M.; Hinrich Graf von der Schulenburg, J.; Bertrand, D.; West, S. A.; Goriacheva, I. I.; Zakharov, I. A.; Werren, J. H.; Stouthamer, R.; Majerus, M. E. N. Male–killingWolbachiain two species of insect, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 266 (1999) no. 1420, pp. 735-740 | DOI

[36] Husseneder, C.; Park, J.-S.; Howells, A.; Tikhe, C. V.; Davis, J. A. Bacteria associated with Piezodorus guildinii (Hemiptera: Pentatomidae), with special reference to those transmitted by feeding, Environmental Entomology, Volume 46 (2017) no. 1, pp. 159-166 | DOI

[37] Jaimes, L. F. T.; Valenzuela, J. R. C.; Londoño, G. A. C.; García, D. A. M.; Zuluaga, M. E. L. Relación entre la presencia y el daño de Monalonion velezangeli Carvalho & Costa y algunos factores climáticos en cultivos de aguacate cv. Hass, Ciencia y Tecnología Agropecuaria, Volume 16 (2015) no. 1, pp. 79-85 | DOI

[38] Janson, E. M.; Stireman, J. O.; Singer, M. S.; Abbot, P. Phytophagous Insect–Microbe Mutualisms And Adaptive Evolutionary Diversification, Evolution, Volume 62 (2008) no. 5, pp. 997-1012 | DOI

[39] Johnson, J. S.; Spakowicz, D. J.; Hong, B.-Y.; Petersen, L. M.; Demkowicz, P.; Chen, L.; Leopold, S. R.; Hanson, B. M.; Agresta, H. O.; Gerstein, M.; Sodergren, E.; Weinstock, G. M. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis, Nature Communications, Volume 10 (2019) no. 1, p. 5029 | DOI

[40] Johnson, T. A.; Sylte, M. J.; Looft, T. In-feed bacitracin methylene disalicylate modulates the turkey microbiota and metabolome in a dose-dependent manner, Scientific Reports, Volume 9 (2019) no. 1, p. 8212 | DOI

[41] Jung, S.; Lee, S. Molecular phylogeny of the plant bugs (Heteroptera: Miridae) and the evolution of feeding habits, Cladistics, Volume 28 (2011) no. 1, pp. 50-79 | DOI

[42] Kaur, R.; Shropshire, J. D.; Cross, K. L.; Leigh, B.; Mansueto, A. J.; Stewart, V.; Bordenstein, S. R.; Bordenstein, S. R. Living in the endosymbiotic world of Wolbachia: A centennial review, Cell Host & Microbe, Volume 29 (2021) no. 6, pp. 879-893 | DOI

[43] Kikuchi, Y.; Hayatsu, M.; Hosokawa, T.; Nagayama, A.; Tago, K.; Fukatsu, T. Symbiont-mediated insecticide resistance, Proceedings of the National Academy of Sciences, Volume 109 (2012) no. 22, pp. 8618-8622 | DOI

[44] Klindworth, A.; Pruesse, E.; Schweer, T.; Peplies, J.; Quast, C.; Horn, M.; Glöckner, F. O. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies, Nucleic Acids Research, Volume 41 (2013) no. 1, p. e1 | DOI

[45] LI, R.; LI, M.; YAN, J.; ZHANG, H. Composition and function of the microbiotas in the different parts of the midgut of Pyrrhocoris sibiricus (Hemiptera: Pyrrhocoridae) revealed using high-throughput sequencing of 16S rRNA, European Journal of Entomology, Volume 117 (2020), pp. 352-371 | DOI

[46] Laidoudi, Y.; Levasseur, A.; Medkour, H.; Maaloum, M.; Ben Khedher, M.; Sambou, M.; Bassene, H.; Davoust, B.; Fenollar, F.; Raoult, D.; Mediannikov, O. An earliest endosymbiont, Wolbachia massiliensis sp. nov., strain PL13 from the bed bug (Cimex hemipterus), type strain of a new supergroup T, International Journal of Molecular Sciences, Volume 21 (2020) no. 21, p. 8064 | DOI

[47] Lariviere, P. J.; Leonard, S. P.; Horak, R. D.; Powell, J. E.; Barrick, J. E. Honey bee functional genomics using symbiont-mediated RNAi, Nature Protocols, Volume 18 (2023) no. 3, pp. 902-928 | DOI

[48] Li, Q.; Fan, J.; Sun, J.; Zhang, Y.; Hou, M.; Chen, J. Anti-plant defense response strategies mediated by the secondary symbiont Hamiltonella defensa in the wheat aphid Sitobion miscanthi, Frontiers in Microbiology, Volume 10 (2019) | DOI

[49] Lu, Y.; Zhou, G.; Ewald, J.; Pang, Z.; Shiri, T.; Xia, J. MicrobiomeAnalyst 2.0: comprehensive statistical, functional and integrative analysis of microbiome data, Nucleic Acids Research, Volume 51 (2023) no. W1, p. W310-W318 | DOI

[50] Luo, J.; Cheng, Y.; Guo, L.; Wang, A.; Lu, M.; Xu, L. Variation of gut microbiota caused by an imbalance diet is detrimental to bugs' survival, Science of The Total Environment, Volume 771 (2021) | DOI

[51] Machtelinckx, T.; Van Leeuwen, T.; Vanholme, B.; Gehesquière, B.; Dermauw, W.; Vandekerkhove, B.; Gheysen, G.; De Clercq, P. Wolbachia induces strong cytoplasmic incompatibility in the predatory bug Macrolophus pygmaeus, Insect Molecular Biology, Volume 18 (2009) no. 3, pp. 373-381 | DOI

[52] Mejía-Alvarado, F. S.; Ghneim-Herrera, T.; Góngora, C. E.; Benavides, P.; Navarro-Escalante, L. Structure and dynamics of the gut bacterial community across the developmental stages of the coffee berry borer, Hypothenemus hampei, Frontiers in Microbiology, Volume 12 (2021) | DOI

[53] Moran, N. A.; Telang, A. Bacteriocyte-associated symbionts of insects, BioScience, Volume 48 (1998) no. 4, pp. 295-304 | DOI

[54] Motta, E. V.; Gage, A.; Smith, T. E.; Blake, K. J.; Kwong, W. K.; Riddington, I. M.; Moran, N. Host-microbiome metabolism of a plant toxin in bees, eLife, Volume 11 (2022), p. e82595 | DOI

[55] Namyatova, A. A.; Cassis, G. Systematic revision and phylogeny of the plant bug tribe Monaloniini (Insecta: Heteroptera: Miridae: Bryocorinae) of the world, Zoological Journal of the Linnean Society, Volume 176 (2016) no. 1, pp. 36-136 | DOI

[56] Narita, S.; Kageyama, D.; Nomura, M.; Fukatsu, T. Unexpected mechanism of symbiont-induced reversal of insect sex: Feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development, Applied and Environmental Microbiology, Volume 73 (2007) no. 13, pp. 4332-4341 | DOI

[57] Navarro-Escalante, L.; Benavides, P.; Acevedo, F. E. Supplementary Data: Diversity of bacterial symbionts associated with the tropical plant bug Monalonion velezangeli (Hemiptera: Miridae) revealed by high-throughput 16S-rRNA sequencing, Zenodo, 2024 | DOI

[58] Nikoh, N.; Hosokawa, T.; Moriyama, M.; Oshima, K.; Hattori, M.; Fukatsu, T. Evolutionary origin of insect-Wolbachia nutritional mutualism, Proceedings of the National Academy of Sciences of the United States of America, Volume 111 (2014) no. 28, pp. 10257-10262 | DOI

[59] Ocampo Flórez, V.; Durán Prieto, J.; Albornoz, M.; Forero, D. New plant associations for Monalonion velezangeli (Hemiptera: Miridae) in green urban areas of Bogotá (Colombia), Acta Biológica Colombiana, Volume 23 (2018) no. 2, pp. 205-208 | DOI

[60] O’Neill, S. L.; Hoffmann, A. A.; Werren, J. H.; (eds) Influential Passengers, Oxford University Press, Oxford, 1997 | DOI

[61] Pavlidis, P.; Noble, W. S. Matrix2png: a utility for visualizing matrix data, Bioinformatics, Volume 19 (2003) no. 2, pp. 295-296 | DOI

[62] Pietri, J. E.; DeBruhl, H.; Sullivan, W. The rich somatic life of Wolbachia, MicrobiologyOpen, Volume 5 (2016) no. 6, pp. 923-936 | DOI

[63] Ramírez-Cortés, H. J.; Gil-Palacio, Z. N.; Benavides-Machado, P. Monalonion velezangeli La chinche de la chamusquina del café, Canicafe, Chinchina, Caldas, Colombia (2008) no. 367, pp. 1-8 (https://www.cenicafe.org/es/publications/avt0367.pdf)

[64] Ramírez-Gil, J. G.; López, J. H.; Henao-Rojas, J. C. Causes of hass avocado fruit rejection in preharvest, harvest, and packinghouse: Economic losses and associated variables, Agronomy, Volume 10 (2020) no. 1, p. 8 | DOI

[65] Ratcliffe, N. A.; Furtado Pacheco, J. P.; Dyson, P.; Castro, H. C.; Gonzalez, M. S.; Azambuja, P.; Mello, C. B. Overview of paratransgenesis as a strategy to control pathogen transmission by insect vectors, Parasites & Vectors, Volume 15 (2022) no. 1, p. 112 | DOI

[66] Ricaboni, D.; Mailhe, M.; Khelaifia, S.; Raoult, D.; Million, M. Romboutsia timonensis, a new species isolated from human gut, New Microbes and New Infections, Volume 12 (2016), pp. 6-7 | DOI

[67] Rodas, C. A.; Serna, R.; Hurley, B. P.; Bolaños, M. D.; Granados, G. M.; Wingfield, M. J. Three new and important insect pests recorded for the first time in Colombian plantations, Southern Forests: a Journal of Forest Science, Volume 76 (2014) no. 4, pp. 245-252 | DOI

[68] Rudman, S. M.; Greenblum, S.; Hughes, R. C.; Rajpurohit, S.; Kiratli, O.; Lowder, D. B.; Lemmon, S. G.; Petrov, D. A.; Chaston, J. M.; Schmidt, P. Microbiome composition shapes rapid genomic adaptation of Drosophila melanogaster, Proceedings of the National Academy of Sciences of the United States of America, Volume 116 (2019) no. 40, pp. 20025-20032 | DOI

[69] Sajnaga, E.; Skowronek, M.; Kalwasińska, A.; Kazimierczak, W.; Lis, M.; Jach, M. E.; Wiater, A. Comparative Nanopore sequencing-based evaluation of the midgut microbiota of the summer chafer (Amphimallon solstitiale l.) associated with possible resistance to entomopathogenic nematodes, International Journal of Environmental Research and Public Health, Volume 19 (2022) no. 6, p. 3480 | DOI

[70] Sato, Y.; Jang, S.; Takeshita, K.; Itoh, H.; Koike, H.; Tago, K.; Hayatsu, M.; Hori, T.; Kikuchi, Y. Insecticide resistance by a host-symbiont reciprocal detoxification, Nature Communications, Volume 12 (2021) no. 1, p. 6432 | DOI

[71] Schausberger, P. Herbivore-Associated Bacteria as Potential Mediators and Modifiers of Induced Plant Defense Against Spider Mites and Thrips, Frontiers in Plant Science, Volume 9 (2018) | DOI

[72] Serbus, L. R.; Casper-Lindley, C.; Landmann, F.; Sullivan, W. The genetics and cell biology of Wolbachia-host interactions, Annual Review of Genetics, Volume 42 (2008), pp. 683-707 | DOI

[73] Shropshire, J. D.; Leigh, B.; Bordenstein, S. R. Symbiont-mediated cytoplasmic incompatibility: What have we learned in 50 years?, eLife, Volume 9 (2020), p. e61989 (Publisher: eLife Sciences Publications, Ltd) | DOI

[74] Shukla, S. P.; Beran, F. Gut microbiota degrades toxic isothiocyanates in a flea beetle pest, Molecular Ecology, Volume 29 (2020) no. 23, pp. 4692-4705 | DOI

[75] Sinkins, S. P. Wolbachia and cytoplasmic incompatibility in mosquitoes, Insect Biochemistry and Molecular Biology (Molecular and population biology of mosquitoes), Volume 34 (2004) no. 7, pp. 723-729 | DOI

[76] Soh, L.-S.; Veera Singham, G. Bacterial symbionts influence host susceptibility to fenitrothion and imidacloprid in the obligate hematophagous bed bug, Cimex hemipterus, Scientific Reports, Volume 12 (2022) no. 1, p. 4919 | DOI

[77] Stouthamer, R.; Breeuwer, J. A.; Hurst, G. D. Wolbachia pipientis: microbial manipulator of arthropod reproduction, Annual Review of Microbiology, Volume 53 (1999), pp. 71-102 | DOI

[78] Sudakaran, S.; Kost, C.; Kaltenpoth, M. Symbiont acquisition and replacement as a source of ecological innovation, Trends in Microbiology, Volume 25 (2017) no. 5, pp. 375-390 | DOI

[79] Sun, D.-L.; Jiang, X.; Wu, Q. L.; Zhou, N.-Y. Intragenomic heterogeneity of 16S rRNA genes causes overestimation of prokaryotic diversity, Applied and Environmental Microbiology, Volume 79 (2013) no. 19, pp. 5962-5969 | DOI

[80] Thompson, J. D.; Higgins, D. G.; Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Research, Volume 22 (1994) no. 22, pp. 4673-4680 | DOI

[81] Van de Peer, Y.; Chapelle, S.; De Wachter, R. A quantitative map of nucleotide substitution rates in bacterial rRNA, Nucleic Acids Research, Volume 24 (1996) no. 17, pp. 3381-3391 | DOI

[82] Vavre, F.; de Jong, J. H.; Stouthamer, R. Cytogenetic mechanism and genetic consequences of thelytoky in the wasp Trichogramma cacoeciae, Heredity, Volume 93 (2004) no. 6, pp. 592-596 | DOI

[83] Volland, J.-M. Shedding light on bacteria associated with an agricultural pest, the tropical plant bug Monalonion velezangeli: a foundational descriptive study, Peer Community in Microbiology (2024), p. 100004 | DOI

[84] Werren, J. H. Biology of Wolbachia, Annual Review of Entomology, Volume 42 (1997), pp. 587-609 | DOI

[85] Werren, J. H.; Baldo, L.; Clark, M. E. Wolbachia: master manipulators of invertebrate biology, Nature Reviews Microbiology, Volume 6 (2008) no. 10, pp. 741-751 | DOI

[86] Wilches, D. M.; Coghlin, P. C.; Floate, K. D. Next generation sequencing, insect microbiomes, and the confounding effect of Wolbachia: a case study using spotted-wing drosophila (Drosophila suzukii) (Diptera: Drosophilidae), Canadian Journal of Zoology, Volume 99 (2021) no. 7, pp. 588-595 (Publisher: NRC Research Press) | DOI

[87] Xue, H.; Zhu, X.; Wang, L.; Zhang, K.; Li, D.; Ji, J.; Niu, L.; Wu, C.; Gao, X.; Luo, J.; Cui, J. Gut bacterial diversity in different life cycle stages of Adelphocoris suturalis (Hemiptera: Miridae), Frontiers in Microbiology, Volume 12 (2021), p. 670383 | DOI

[88] Zhang, D.; Wang, Y.; He, K.; Yang, Q.; Gong, M.; Ji, M.; Chen, L. Wolbachia limits pathogen infections through induction of host innate immune responses, PloS One, Volume 15 (2020) no. 2, p. e0226736 | DOI

[89] Zhang, L.; Yun, Y.; Hu, G.; Peng, Y. Insights into the bacterial symbiont diversity in spiders, Ecology and Evolution, Volume 8 (2018) no. 10, pp. 4899-4906 | DOI

[90] Zhang, S.; Gan, L.; Qin, Q.; Long, X.; Zhang, Y.; Chu, Y.; Tian, Y. Paracoccusacridae sp. nov., isolated from the insect Acrida cinerea living in deserted cropland, International Journal of Systematic and Evolutionary Microbiology, Volume 66 (2016) no. 9, pp. 3492-3497 | DOI

[91] Zhou, J.-C.; Zhao, Q.; Liu, S.-M.; Shang, D.; Zhao, X.; Huo, L.-X.; Dong, H.; Zhang, L.-S. Effects of thelytokous parthenogenesis-inducing Wolbachia on the fitness of Trichogramma dendrolimi Matsumura (Hymenoptera: Trichogrammatidae) in superparasitised and single-parasitised hosts, Frontiers in Ecology and Evolution, Volume 9 (2021) | DOI

[92] Zhou, W.; Rousset, F.; O'Neil, S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences., Proceedings of the Royal Society B: Biological Sciences, Volume 265 (1998) no. 1395, pp. 509-515 | DOI

[93] Zug, R.; Hammerstein, P. Wolbachia and the insect immune system: what reactive oxygen species can tell us about the mechanisms of Wolbachia-host interactions, Frontiers in Microbiology, Volume 6 (2015), p. 1201 | DOI

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