Dynamic Gut Microbiota of Apolygus lucorum Across Different Life Stages Reveals Potential Pathogenic Bacteria for Facilitating the Pest Management.
Apolygus lucorum
Culture-dependent
Culture-independent
Gut bacteria
Life stages
Serratia
Journal
Microbial ecology
ISSN: 1432-184X
Titre abrégé: Microb Ecol
Pays: United States
ID NLM: 7500663
Informations de publication
Date de publication:
04 Dec 2023
04 Dec 2023
Historique:
received:
03
08
2023
accepted:
26
11
2023
medline:
5
12
2023
pubmed:
4
12
2023
entrez:
4
12
2023
Statut:
epublish
Résumé
Insect's gut microbiota has diverse effects on their fitness, and a comprehensive understanding of gut microbiota functions requires analyzing its diversity. Apolygus lucorum is a highly destructive pest that threatens many economically important crops in China. This study investigated the gut microbiota of A. lucorum across its life cycle using both culture-dependent and culture-independent methods. A total of 87 gut bacterial isolates were identified, belonging to 4 phyla, 27 families, and 45 genera, while Miseq sequencing detected 91 amplicon sequence variants (ASVs) assigned to 5 phyla, 28 families, and 39 genera. Proteobacteria and Firmicutes were the predominant phyla, with Staphylococcus and Serratia as the major genera. There were significant differences in the relative abundance of these genera between the nymph and adult stages. Staphylococcus was significantly more abundant in nymphs than it in adults, while Serratia was significantly more abundant in sexually mature adults than in other developmental stages. Notably, Serratia is a common opportunistic pathogen in many insects. Injecting the gut-dominant isolate Serratia marcescens verified its high pathogenicity. Additionally, immune indicators of the bug at different developmental stages supported the hypothesis that Serratia is a pathogen of A. lucorum. This study provides a foundation for understanding the role of gut bacteria in the life history of A. lucorum and developing new pest control strategies based on microbes.
Identifiants
pubmed: 38047964
doi: 10.1007/s00248-023-02324-5
pii: 10.1007/s00248-023-02324-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
9Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Moran NA, Ochman H, Hammer TJ (2019) Evolutionary and ecological consequences of gut microbial communities. Annu Rev Ecol Evol Syst 50:451–475. https://doi.org/10.1146/annurev-ecolsys-110617-062453
doi: 10.1146/annurev-ecolsys-110617-062453
pubmed: 32733173
pmcid: 7392196
Xiong W (2022) Intestinal microbiota in various animals. Integr Zool 17:331–332. https://doi.org/10.1111/1749-4877.12633
doi: 10.1111/1749-4877.12633
pubmed: 35182033
Zhang Y, Zhang S, Xu L (2023) The pivotal roles of gut microbiota in insect plant interactions for sustainable pest management. NPJ Biofilms Microbiomes 9:66. https://doi.org/10.1038/s41522-023-00435-y
doi: 10.1038/s41522-023-00435-y
pubmed: 37735530
pmcid: 10514296
Carissimo G, Pondeville E, McFarlane M, Dietrich I, Mitri C, Bischoff E, Antoniewski C, Bourgouin C, Failloux A-B, Kohl A (2015) Antiviral immunity of Anopheles gambiae is highly compartmentalized, with distinct roles for RNA interference and gut microbiota. Proc Natl Acad Sci 112:E176–E185. https://doi.org/10.1073/pnas.1412984112
doi: 10.1073/pnas.1412984112
pubmed: 25548172
Xu L, Deng J, Zhou F, Cheng C, Zhang L, Zhang J, Lu M (2019) Gut microbiota in an invasive bark beetle infected by a pathogenic fungus accelerates beetle mortality. J Pest Sci 92:343–351. https://doi.org/10.1007/s10340-018-0999-4
doi: 10.1007/s10340-018-0999-4
Devi S, Saini HS, Kaur S (2022) Insecticidal and growth inhibitory activity of gut microbes isolated from adults of Spodoptera litura (Fab.). BMC Microbiol 22:1–14. https://doi.org/10.1186/s12866-022-02476-3
doi: 10.1186/s12866-022-02476-3
Lemoine MM, Engl T, Kaltenpoth M (2020) Microbial symbionts expanding or constraining abiotic niche space in insects. Curr Opin Insect Sci 39:14–20. https://doi.org/10.1016/j.cois.2020.01.003
doi: 10.1016/j.cois.2020.01.003
pubmed: 32086000
Zhu W, Shi X, Qi Y, Wang X, Chang L, Zhao C, Zhu L, Jiang J (2022) Commensal microbiota and host metabolic divergence are associated with the adaptation of Diploderma vela to spatially heterogeneous environments. Integr Zool 17:346–365. https://doi.org/10.1111/1749-4877.12590
doi: 10.1111/1749-4877.12590
pubmed: 34520122
Mistry R, Kounatidis I, Ligoxygakis P (2016) Exploring interactions between pathogens and the Drosophila gut. Dev Comp Immunol 64:3–10. https://doi.org/10.1016/j.dci.2016.01.016
doi: 10.1016/j.dci.2016.01.016
pubmed: 26876781
Lee JH, Lee KA, Lee WJ (2017) Chapter Four - Microbiota, Gut Physiology, and Insect Immunity. Adv Insect Physiol 52:111–138. https://doi.org/10.1016/bs.aiip.2016.11.001
Buchon N, Broderick NA, Lemaitre B (2013) Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat Rev Microbiol 11:615–626. https://doi.org/10.1038/nrmicro3074
doi: 10.1038/nrmicro3074
pubmed: 23893105
Eleftherianos I, Revenis C (2010) Role and importance of phenoloxidase in insect hemostasis. J Innate Immun 3:28–33. https://doi.org/10.1159/000321931
doi: 10.1159/000321931
pubmed: 21051882
Freitak D, Schmidtberg H, Dickel F, Lochnit G, Vogel H, Vilcinskas A (2014) The maternal transfer of bacteria can mediate trans-generational immune priming in insects. Virulence 5:547–554. https://doi.org/10.4161/viru.28367
doi: 10.4161/viru.28367
pubmed: 24603099
pmcid: 4063815
Thakur A, Dhammi P, Saini HS, Kaur S (2015) Pathogenicity of bacteria isolated from gut of Spodoptera litura (Lepidoptera: Noctuidae) and fitness costs of insect associated with consumption of bacteria. J Invertebr Pathol 127:38–46. https://doi.org/10.1016/j.jip.2015.02.007
doi: 10.1016/j.jip.2015.02.007
pubmed: 25725116
Coutinho T, Van der Westhuizen L, Roux J, McFarlane S, Venter S (2015) Significant host jump of Xanthomonas vasicola from sugarcane to a Eucalyptus grandis clone in South Africa. Plant Pathol 64:576–581. https://doi.org/10.1111/ppa.12298
doi: 10.1111/ppa.12298
Amann RI, Ludwig W, Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169. https://doi.org/10.1128/mr.59.1.143-169.1995
doi: 10.1128/mr.59.1.143-169.1995
pubmed: 7535888
pmcid: 239358
Wang S, Wang L, Fan X, Yu C, Feng L, Yi L (2020) An insight into diversity and functionalities of gut microbiota in insects. Curr Microbiol 77:1976–1986. https://doi.org/10.1007/s00284-020-02084-2
doi: 10.1007/s00284-020-02084-2
pubmed: 32535651
Lu Y, Wu K, Wyckhuys KA, Guo Y (2010) Overwintering hosts of Apolygus lucorum (Hemiptera: Miridae) in northern China. Crop Prot 29:1026–1033. https://doi.org/10.1016/j.cropro.2010.03.017
doi: 10.1016/j.cropro.2010.03.017
Yuan W, Li W, Li Y, Wu K (2013) Combination of plant and insect eggs as food sources facilitates ovarian development in an omnivorous bug Apolygus lucorum (Hemiptera: Miridae). J Econ Entomol 106:1200–1208. https://doi.org/10.1603/EC13016
doi: 10.1603/EC13016
pubmed: 23865184
Luo J, Wang A, Cheng Y, Rong H, Guo L, Peng Y, Xu L (2020) Selection and validation of suitable reference genes for RT-qPCR analysis in Apolygus lucorum (Hemiptera: Miridae). J Econ Entomol 113:451–460. https://doi.org/10.1093/jee/toz301
doi: 10.1093/jee/toz301
pubmed: 31773146
Arredondo-Santoyo M, Herrera-Camacho J, Vázquez-Garcidueñas MS, Vázquez-Marrufo G (2020) Corn stover induces extracellular laccase activity in Didymosphaeria sp.(syn.= Paraconiothyrium sp.) and exhibits increased in vitro ruminal digestibility when treated with this fungal species. Folia Microbiol 65:849–861. https://doi.org/10.1007/s12223-020-00795-4
doi: 10.1007/s12223-020-00795-4
Engel P, Moran NA (2013) The gut microbiota of insects–diversity in structure and function. FEMS Microbiol Rev 37:699–735. https://doi.org/10.1111/1574-6976.12025
doi: 10.1111/1574-6976.12025
pubmed: 23692388
Engl T, Kaltenpoth M (2018) Influence of microbial symbionts on insect pheromones. Nat Prod Rep 35:386–397. https://doi.org/10.1039/C7NP00068E
doi: 10.1039/C7NP00068E
pubmed: 29565067
Ong SY, Kho H-P, Riedel SL, Kim S-W, Gan C-Y, Taylor TD, Sudesh K (2018) An integrative study on biologically recovered polyhydroxyalkanoates (PHAs) and simultaneous assessment of gut microbiome in yellow mealworm. J Biotechnol 265:31–39. https://doi.org/10.1016/j.jbiotec.2017.10.017
doi: 10.1016/j.jbiotec.2017.10.017
pubmed: 29101024
Lu Y, Wu K, Cai X, Liu Y (2008) A rearing method for mirids using the green bean, Phaseolus vulgaris in the laboratory. Acta Phytophy Sin 35:215–219. https://doi.org/10.3724/SP.J.1005.2008.01083
doi: 10.1017/S0007485318000883
Obłąk E, Piecuch A, Maciaszczyk-Dziubińska E, Wawrzycka D (2016) Quaternary ammonium salt N-(dodecyloxycarboxymethyl)-N, N, N-trimethyl ammonium chloride induced alterations in Saccharomyces cerevisiae physiology. J Biosci 41:601–614. https://doi.org/10.1007/s12038-016-9644-7
doi: 10.1007/s12038-016-9644-7
pubmed: 27966483
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
doi: 10.1093/molbev/msw054
pubmed: 27004904
pmcid: 8210823
Kim O-S, Cho Y-J, Lee K, Yoon S-H, Kim M, Na H, Park S-C, Jeon YS, Lee J-H, Yi H (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721. https://doi.org/10.1099/ijs.0.038075-0
doi: 10.1099/ijs.0.038075-0
pubmed: 22140171
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series, vol 41. Information Retrieval Ltd., c1979-c2000, London, pp 95–98
Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165. https://doi.org/10.1093/bioinformatics/btr088
Stamatakis A, Ludwig T, Meier H (2004) A fast program for maximum likelihood-based inference of large phylogenetic trees. Proceedings of the 2004 ACM symposium on applied computing, pp 197–201
doi: 10.1145/967900.967940
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754
doi: 10.1093/bioinformatics/17.8.754
pubmed: 11524383
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890. https://doi.org/10.1093/bioinformatics/bty560
doi: 10.1093/bioinformatics/bty560
pubmed: 30423086
pmcid: 6129281
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F (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
doi: 10.1038/s41587-019-0209-9
pubmed: 31341288
pmcid: 7015180
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
doi: 10.1038/nmeth.3869
pubmed: 27214047
pmcid: 4927377
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072. https://doi.org/10.1128/AEM.03006-05
doi: 10.1128/AEM.03006-05
pubmed: 16820507
pmcid: 1489311
Zhao L, Wang W-Q, Xu S-Q, Guan D-L (2022) The comparison of gut bacteria communities and the functions among the sympatric grasshopper species from the Loess Plateau. Front Microbiol 13
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
doi: 10.1128/AEM.01541-09
pubmed: 19801464
pmcid: 2786419
Chapman M, Underwood A (1999) Ecological patterns in multivariate assemblages: information and interpretation of negative values in ANOSIM tests. Mar Ecol Prog Ser 180:257–265. https://doi.org/10.3354/meps180257
doi: 10.3354/meps180257
Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5:169–172. https://doi.org/10.1038/ismej.2010.133
doi: 10.1038/ismej.2010.133
pubmed: 20827291
Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, Lumley T, Maechler M, Magnusson A, Moeller S (2009) gplots: Various R programming tools for plotting data. R package version 2, p 1
Lex A, Gehlenborg N, Strobelt H, Vuillemot R, Pfister H (2014) UpSet: visualization of intersecting sets. IEEE Trans Vis Comput Graph 20:1983–1992. https://doi.org/10.1109/TVCG.2014.2346248
doi: 10.1109/TVCG.2014.2346248
pubmed: 26356912
pmcid: 4720993
Yun J-H, Roh SW, Whon TW, Jung M-J, Kim M-S, Park D-S, Yoon C, Nam Y-D, Kim Y-J, Choi J-H (2014) Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol 80:5254–5264. https://doi.org/10.1128/AEM.01226-14
doi: 10.1128/AEM.01226-14
pubmed: 24928884
pmcid: 4136111
Douglas GM, Beiko RG, Langille MG (2018) Predicting the functional potential of the microbiome from marker genes using PICRUSt. Methods Mol Biol 1849:169–177. https://doi.org/10.1007/978-1-4939-8728-3_11
Adamo SA (2004) Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the cricket Gryllus texensis. J Insect Physiol 50:209–216. https://doi.org/10.1016/j.jinsphys.2003.11.011
doi: 10.1016/j.jinsphys.2003.11.011
pubmed: 15019523
Ramirez JL, Dunlap CA, Muturi EJ, Barletta AB, Rooney AP (2018) Entomopathogenic fungal infection leads to temporospatial modulation of the mosquito immune system. PLoS Negl Trop Dis 12:e0006433. https://doi.org/10.1371/journal.pntd.0006433
doi: 10.1371/journal.pntd.0006433
pubmed: 29684026
pmcid: 5933799
Cao DP, Liu Y, Wei JJ, Li JH, Wang GR (2016) A de novo transcriptomic analysis to reveal functional genes in Apolygus lucorum. Insect Sci 23:2–14. https://doi.org/10.1111/1744-7917.12188
doi: 10.1111/1744-7917.12188
pubmed: 25408247
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009
doi: 10.1016/j.tplants.2004.08.009
pubmed: 15465684
Ni X, Li X, Shen T-L, Qian W-J, Xian M (2021) A sweet H2S/H2O2 dual release system and specific protein S-persulfidation mediated by thioglucose/glucose oxidase. J Am Chem Soc 143:13325–13332. https://doi.org/10.1021/jacs.1c06372
doi: 10.1021/jacs.1c06372
pubmed: 34383487
Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol 44:846–849. https://doi.org/10.1099/00207713-44-4-846
doi: 10.1099/00207713-44-4-846
Ortiz-Cortés LY, Ventura-Canseco LMC, Abud-Archila M, Ruíz-Valdiviezo VM, Velázquez-Ríos IO, Alvarez-Gutiérrez PE (2021) Evaluation of temperature, pH and nutrient conditions in bacterial growth and extracellular hydrolytic activities of two Alicyclobacillus spp. strains. Arch Microbiol 203:4557–4570. https://doi.org/10.1007/s00203-021-02332-4
doi: 10.1007/s00203-021-02332-4
pubmed: 34159433
Pikuta EV, Hoover RB, Tang J (2007) Microbial extremophiles at the limits of life. Crit Rev Microbiol 33:183–209. https://doi.org/10.1080/10408410701451948
doi: 10.1080/10408410701451948
pubmed: 17653987
Liu Y, Xu L, Zhang Z, Huang Z, Fang D, Zheng X, Yang Z, Lu M (2021) Isolation, identification, and analysis of potential functions of culturable bacteria associated with an invasive gall wasp, Leptocybe invasa. Microb Ecol 1–16. https://doi.org/10.1007/s00248-021-01715-w
Chen S, Zhang D, Augustinos A, Doudoumis V, Bel Mokhtar N, Maiga H, Tsiamis G, Bourtzis K (2020) Multiple factors determine the structure of bacterial communities associated with Aedes albopictus under artificial rearing conditions. Front Microbiol 11:605. https://doi.org/10.3389/fmicb.2020.00605
doi: 10.3389/fmicb.2020.00605
pubmed: 32351473
pmcid: 7176356
Maleki-Ravasan N, Ahmadi N, Soroushzadeh Z, Raz AA, Zakeri S, Dinparast Djadid N (2020) New insights into culturable and unculturable bacteria across the life history of medicinal maggots Lucilia sericata (Meigen)(Diptera: Calliphoridae). Front Microbiol 11:505. https://doi.org/10.3389/fmicb.2020.00505
doi: 10.3389/fmicb.2020.00505
pubmed: 32322242
pmcid: 7156559
Veselská T, Švec K, Kostovčík M, Peral-Aranega E, García-Fraile P, Křížková B, Havlíček V, Saati-Santamaría Z, Kolarik M (2022) The core gut microbiome changes throughout life cycle and season of bark beetle Ips typographus. Authorea Preprints. https://doi.org/10.22541/au.167153425.56811139/v1
Xu L, Sun L, Zhang S, Wang S, Lu M (2019) High-resolution profiling of gut bacterial communities in an invasive beetle using PacBio SMRT sequencing system. Insects 10:248. https://doi.org/10.3390/insects10080248
doi: 10.3390/insects10080248
pubmed: 31416137
pmcid: 6722854
Huang K, Wang J, Huang J, Zhang S, Vogler AP, Liu Q, Li Y, Yang M, Li Y, Zhou X (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
doi: 10.3389/fmicb.2021.633075
pubmed: 34239504
pmcid: 8260032
Zhao X, Zhang X, Chen Z, Wang Z, Lu Y, Cheng D (2018) The divergence in bacterial components associated with Bactrocera dorsalis across developmental stages. Front Microbiol 9:114. https://doi.org/10.3389/fmicb.2018.00114
doi: 10.3389/fmicb.2018.00114
pubmed: 29449838
pmcid: 5799270
Cini A, Meriggi N, Bacci G, Cappa F, Vitali F, Cavalieri D, Cervo R (2020) Gut microbial composition in different castes and developmental stages of the invasive hornet Vespa velutina nigrithorax. Sci Total Environ 745:140873. https://doi.org/10.1016/j.scitotenv.2020.140873
doi: 10.1016/j.scitotenv.2020.140873
pubmed: 32758760
Alfano N, Tagliapietra V, Rosso F, Manica M, Arnoldi D, Pindo M, Rizzoli A (2019) Changes in microbiota across developmental stages of Aedes koreicus, an invasive mosquito vector in Europe: indications for microbiota-based control strategies. Front Microbiol 10:2832. https://doi.org/10.3389/fmicb.2019.02832
doi: 10.3389/fmicb.2019.02832
pubmed: 31921019
pmcid: 6914824
Wang M, Xiang X, Wan X (2020) Divergence in gut bacterial community among life stages of the rainbow stag beetle Phalacrognathus muelleri (Coleptera: Lucanidae). Insects 11:719. https://doi.org/10.3390/insects11100719
doi: 10.3390/insects11100719
pubmed: 33096611
pmcid: 7589407
Xue H, Zhu X, Wang L, Zhang K, Li D, Ji J, Niu L, Wu C, Gao X, Luo J (2021) Gut bacterial diversity in different life cycle stages of Adelphocoris suturalis (Hemiptera: Miridae). Front Microbiol 12:670383. https://doi.org/10.3389/fmicb.2021.670383
doi: 10.3389/fmicb.2021.670383
pubmed: 34149656
pmcid: 8208491
De Cock M, Virgilio M, Vandamme P, Bourtzis K, De Meyer M, Willems A (2020) Comparative microbiomics of tephritid frugivorous pests (Diptera: Tephritidae) from the field: A tale of high variability across and within species. Front Microbiol 11:1890. https://doi.org/10.3389/fmicb.2020.01890
doi: 10.3389/fmicb.2020.01890
pubmed: 32849469
pmcid: 7431611
Ugwu JA, Wenzi R, Asiegbu FO (2022) Monocot diet sources drive diversity of gut bacterial communities in Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae. J Appl Entomol 146:942–956. https://doi.org/10.1111/jen.13022
doi: 10.1111/jen.13022
Xue H, Zhu X, Wang L, Zhang K, Li D, Ji J, Niu L, Gao X, Luo J, Cui J (2023) Dynamics and diversity of symbiotic bacteria in Apolygus lucorum at different developmental stages. J Cotton Res 6:1–11. https://doi.org/10.1186/s42397-023-00142-1
doi: 10.1186/s42397-023-00142-1
Arp AP, Quintero G, Sagel A, Batista RG, Phillips PL, Hickner PV (2022) The microbiome of wild and mass-reared new world screwworm, Cochliomyia hominivorax. Sci Rep 12:1042. https://doi.org/10.1038/s41598-022-04828-5
doi: 10.1038/s41598-022-04828-5
pubmed: 35058490
pmcid: 8776964
Dillon RJ, Vennard CT, Charnley AK (2000) Exploitation of gut bacteria in the locust. Nature 403:851–851. https://doi.org/10.1038/35002669
doi: 10.1038/35002669
pubmed: 10706273
Berasategui A, Moller AG, Weiss B, Beck CW, Bauchiero C, Read TD, Gerardo NM, Salem H (2021) Symbiont genomic features and localization in the bean beetle Callosobruchus maculatus. Appl Environ Microbiol 87:e00212–e00221. https://doi.org/10.1128/AEM.00212-21
doi: 10.1128/AEM.00212-21
pubmed: 33863703
pmcid: 8174668
Engl T, Eberl N, Gorse C, Krüger T, Schmidt TH, Plarre R, Adler C, Kaltenpoth M (2018) Ancient symbiosis confers desiccation resistance to stored grain pest beetles. Mol Ecol 27:2095–2108. https://doi.org/10.1111/mec.14418
doi: 10.1111/mec.14418
pubmed: 29117633
Salem H, Kaltenpoth M (2022) Beetle–bacterial symbioses: endless forms most functional. Annu Rev Entomol 67:201–219. https://doi.org/10.1146/annurev-ento-061421-063433
doi: 10.1146/annurev-ento-061421-063433
pubmed: 34606364
Dong Z-X, Li H-Y, Chen Y-F, Wang F, Deng X-Y, Lin L-B, Zhang Q-L, Li J-L, Guo J (2020) Colonization of the gut microbiota of honey bee (Apis mellifera) workers at different developmental stages. Microbiol Res 231:126370. https://doi.org/10.1016/j.micres.2019.126370
doi: 10.1016/j.micres.2019.126370
pubmed: 31739261
Xu W, Wang Y, Wang Y, Zhang Y-n, Wang J (2022) Diversity and dynamics of bacteria at the Chrysomya megacephala pupal stage revealed by third-generation sequencing. Sci Rep 12:2006. https://doi.org/10.1038/s41598-022-06311-7
doi: 10.1038/s41598-022-06311-7
pubmed: 35132164
pmcid: 8821589
Bahia AC, Dong Y, Blumberg BJ, Mlambo G, Tripathi A, BenMarzouk-Hidalgo OJ, Chandra R, Dimopoulos G (2014) Exploring Anopheles gut bacteria for Plasmodium blocking activity. Environ Microbiol 16:2980–2994. https://doi.org/10.1111/1462-2920.12381
doi: 10.1111/1462-2920.12381
pubmed: 24428613
pmcid: 4099322
Tan B, Jackson TA, Hurst MR (2006) Virulence of Serratia strains against Costelytra zealandica. Appl Environ Microbiol 72:6417–6418. https://doi.org/10.1128/AEM.00519-06
doi: 10.1128/AEM.00519-06
pubmed: 16957275
pmcid: 1563684
Luo J, Cheng Y, Guo L, Wang A, Lu M, Xu L (2021) Variation of gut microbiota caused by an imbalance diet is detrimental to bugs’ survival. Sci Total Environ 771:144880. https://doi.org/10.1016/j.scitotenv.2020.144880
doi: 10.1016/j.scitotenv.2020.144880
pubmed: 33736123