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Impact of Sulfoxaflor Exposure on Bacterial Community and Developmental Performance of the Predatory Ladybeetle Propylea japonica

  • Invertebrate Microbiology
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Abstract

Insects maintain a vast number of symbiotic bacteria, and these symbionts play key roles in the hosts’ life processes. Propylea japonica (Coleoptera: Coccinellidae) is an abundant and widespread ladybeetle in agricultural fields in Asia. Both larvae and adults of P. japonica are likely to be exposed to insecticide residue in the field during their predatory activity. Sulfoxaflor is a highly powerful insecticide that has strong efficacy in controlling sap-sucking pests. To date, there have been several studies on the acute and long-term toxicity of sulfoxaflor to insects, but few studies have reported the impact of sulfoxaflor on the predators’ micro-ecosystems. This study was to determine the impact of sulfoxaflor on the symbiotic bacteria and developmental performance of P. japonica. In the present study, two concentrations (1 mg/L and 5 mg/L) and two exposure periods (1 day and 5 days) were set for P. japonica under sulfoxaflor exposure. The survival rate, developmental duration, pupation rate, emergence rate, and body weight of P. japonica were examined. Moreover, the bacterial community of P. japonica was investigated by high-throughput 16S ribosomal RNA gene sequencing. Our results indicated that bacterial community of P. japonica was mainly composed of Staphylococcus, Pantoea, Acinetobacter, Rhodococcus, and Ralstonia at the genus level. The bacterial community of P. japonica in 1 mg/L and 5 mg/L sulfoxaflor groups was significantly altered on day 1, compared with that in control group. The results also showed that the larval duration was significantly prolonged but the pupal duration was significantly shortened in both sulfoxaflor groups. Meanwhile, the pupation and emergence rate was not significantly changed, but the body weights of adults were significantly decreased in both sulfoxaflor groups. Our study will provide a new perspective for evaluating the safety of pesticides to beneficial arthropods.

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References

  1. Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43. https://doi.org/10.1017/S0021859605005708

    Article  Google Scholar 

  2. Strassemeyer J, Daehmlow D, Dominic AR, Lorenz S, Golla B (2017) SYNOPS-WEB, an online tool for environmental risk assessment to evaluate pesticide strategies on field level. Crop Prot 97:28–44. https://doi.org/10.1016/j.cropro.2016.11.036

    Article  CAS  Google Scholar 

  3. Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62. https://doi.org/10.1146/annurev-ento-010715-023646

    Article  CAS  PubMed  Google Scholar 

  4. Sharma A, Kumar V, Shahzad B, Tanveer M, Sidhu GPS, Handa N, Kohli SK, Yadav P, Bali AS, Parihar RD, Dar OI, Singh K, Jasrotia S, Bakshi P, Ramakrishnan M, Kumar S, Bhardwa R, Thukral AK (2019) Worldwide pesticide usage and its impacts on ecosystem. SN Appl Sci 1:1–16. https://doi.org/10.1007/s42452-019-1485-1

    Article  CAS  Google Scholar 

  5. Köhler HR, Triebskorn R (2013) Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science 341:759–765. https://doi.org/10.1126/science.1237591

    Article  CAS  PubMed  Google Scholar 

  6. Gill HK, Garg H (2014) Pesticide: environmental impacts and management strategies. Pestic: Toxic Asp 8:187–230. https://doi.org/10.5772/57399

    Article  Google Scholar 

  7. Gray ME, Ratcliffe ST, Rice ME (2009) The IPM paradigm: concepts, strategies and tactics. Integr Pest Manage 1:1–13. https://doi.org/10.1017/cbo9780511626463.002

    Article  Google Scholar 

  8. De Castro AA, Corrêa AS, Legaspi JC, Guedes RNC, Serrão JE, Zanuncio JC (2013) Survival and behavior of the insecticide-exposed predators Podisus nigrispinus and Supputius cincticeps (Heteroptera: Pentatomidae). Chemosphere 93:1043–1050. https://doi.org/10.1016/j.chemosphere.2013.05.075

    Article  CAS  PubMed  Google Scholar 

  9. Atta B, Rizwan M, Sabir AM, Gogi MD, Farooq MA, Jamal A (2021) Lethal and sublethal effects of clothianidin, imidacloprid and sulfoxaflor on the wheat aphid, Schizaphis graminum (Hemiptera: Aphididae) and its coccinellid predator, Coccinella septempunctata. Int J Trop Insect Sci 41:345–358. https://doi.org/10.1007/s42690-020-00212-w

    Article  Google Scholar 

  10. Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440

    Article  CAS  PubMed  Google Scholar 

  11. Watson GB, Olson MB, Beavers KW, Loso MR, Sparks TC (2017) Characterization of a nicotinic acetylcholine receptor binding site for sulfoxaflor, a new sulfoximine insecticide for the control of sap-feeding insect pests. Pestic Biochem Physiol 143:90–94. https://doi.org/10.1016/j.pestbp.2017.09.003

    Article  CAS  PubMed  Google Scholar 

  12. Babcock JM, Gerwick CB, Huang JX, Loso MR, Nakamura G, Nolting SP, Rogers RB, Sparks TC, Thomas J, Watson GB, Zhu Y (2011) Biological characterization of sulfoxaflor, a novel insecticide. Pest Manage Sci 67:328–334. https://doi.org/10.1002/ps.2069

    Article  CAS  Google Scholar 

  13. Sparks TC, Watson GB, Loso MR, Geng C, Babcock JM, Thomas JD (2013) Sulfoxaflor and the sulfoximine insecticides: chemistry, mode of action and basis for efficacy on resistant insects. Pestic Biochem Physiol 107:1–7. https://doi.org/10.1016/j.pestbp.2013.05.014

    Article  CAS  PubMed  Google Scholar 

  14. Liao X, Jin R, Zhang X, Ali E, Mao K, Xu P, Li J, Wan H (2019) Characterization of sulfoxaflor resistance in the brown planthopper, Nilaparvata lugens (Stål). Pest Manage Sci 75:1646–1654. https://doi.org/10.1002/ps.5282

    Article  CAS  Google Scholar 

  15. Tran AK, Alves TM, Koch RL (2016) Potential for sulfoxaflor to improve conservation biological control of Aphis glycines (Hemiptera: Aphididae) in soybean. J Econ Entomol 109:2105–2114. https://doi.org/10.1093/jee/tow168

    Article  CAS  PubMed  Google Scholar 

  16. Longhurst C, Babcock JM, Denholm I, Gorman K, Thomas JD, Sparks TC (2013) Cross-resistance relationships of the sulfoximine insecticide sulfoxaflor with neonicotinoids and other insecticides in the whiteflies Bemisia tabaci and Trialeurodes vaporariorum. Pest Manage Sci 69:809–813. https://doi.org/10.1002/ps.3439

    Article  CAS  Google Scholar 

  17. Garzón A, Medina P, Amor F, Viñuela E, Budia F (2015) Toxicity and sublethal effects of six insecticides to last instar larvae and adults of the biocontrol agents Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) and Adalia bipunctata (L.) (Coleoptera: Coccinellidae). Chemosphere 132:87–93. https://doi.org/10.1016/j.chemosphere.2015.03.016

    Article  CAS  PubMed  Google Scholar 

  18. Ricupero M, Desneux N, Zappalà L, Biondi A (2020) Target and non-target impact of systemic insecticides on a polyphagous aphid pest and its parasitoid. Chemosphere 247:125728. https://doi.org/10.1016/j.chemosphere.2019.125728

    Article  CAS  PubMed  Google Scholar 

  19. He F, Sun S, He L, Qin C, Li X, Zhang J, Jiang X (2020) Responses of Harmonia axyridis (Coleoptera: Coccinellidae) to sulfoxaflor exposure. Ecotoxicol Environ Saf 187:109849. https://doi.org/10.1016/j.ecoenv.2019.109849

    Article  CAS  PubMed  Google Scholar 

  20. Zhang S, Luo J, Wang L, Zhang L, Zhu X, Jiang W, Cui J (2019) Bacterial communities in natural versus pesticide-treated Aphis gossypii populations in North China. Microbiologyopen 8:e00652. https://doi.org/10.1002/mbo3.652

    Article  CAS  PubMed  Google Scholar 

  21. Ren Z, Zhang Y, Cai T, Mao K, Xu Y, Li C, He S, Li J, Wan H (2022) Dynamics of microbial communities across the life stages of Nilaparvata lugens (Stål). Microb Ecol 83(4):1049–1058. https://doi.org/10.1007/s00248-021-01820-w

    Article  PubMed  Google Scholar 

  22. Steinigeweg C, Alkassab AT, Erler S, Beims H, Wirtz IP, Richter D, Pistorius J (2022) Impact of a microbial pest control product containing Bacillus thuringiensis on brood development and gut microbiota of Apis mellifera worker honey bees. Microb Ecol. https://doi.org/10.1007/s00248-022-02004-w

  23. Ma M, Tu C, Luo J, Lu M, Zhang S, Xu L (2021) Metabolic and immunological effects of gut microbiota in leaf beetles at the local and systemic levels. Integr Zool 16:313–323. https://doi.org/10.1111/1749-4877.12528

    Article  CAS  PubMed  Google Scholar 

  24. Zhou F, Xu L, Wu X, Zhao X, Liu M, Zhang X (2020) Symbiotic bacterium-derived organic acids protect Delia antiqua larvae from entomopathogenic fungal infection. mSystems 5(6):e00778-20. https://doi.org/10.1128/mSystems.00778-20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Zhang S, Luo J, Jiang W, Wu L, Zhang L, Ji J, Wang L, Ma Y, Cui J (2019) Response of the bacterial community of Propylea japonica (Thunberg) to Cry2Ab protein. Environ Pollut 254:113063. https://doi.org/10.1016/j.envpol.2019.113063

    Article  CAS  PubMed  Google Scholar 

  26. Shang J, Yao YS, Chen LL, Zhu XZ, Niu L, Gao XK, Luo JY, Ji JC, Cui JJ (2021) Sublethal exposure to deltamethrin stimulates reproduction and alters symbiotic bacteria in Aphis gossypii. J Agric Food Chem 69:15097–15107. https://doi.org/10.1021/acs.jafc.1c05070

    Article  CAS  PubMed  Google Scholar 

  27. Shang J, Yao YS, Zhu XZ, Wang L, Li DY, Zhang KX, Gao XK, Wu CC, Niu L, Ji JC, Luo JY, Cui JJ (2021) Evaluation of sublethal and transgenerational effects of sulfoxaflor on Aphis gossypii via life table parameters and 16S rRNA sequencing. Pest Manage Sci 77:3406–3418. https://doi.org/10.1002/ps.6385

    Article  CAS  Google Scholar 

  28. Cheng D, Guo Z, Riegler M, Xi Z, Liang G, Xu Y (2017) Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome 5:1–12. https://doi.org/10.1186/s40168-017-0236-z

    Article  Google Scholar 

  29. Echaubard P, Duron O, Agnew P, Sidobre C, Noël V, Weill M, Michalakis Y (2010) Rapid evolution of Wolbachia density in insecticide resistant Culex pipiens. Heredity 104:15–19. https://doi.org/10.1038/hdy.2009.100

    Article  CAS  PubMed  Google Scholar 

  30. Zhao Y, Yun Y, Peng Y (2020) Bacillus thuringiensis protein Vip3Aa does not harm the predator Propylea japonica: a toxicological, histopathological, biochemical and molecular analysis. Ecotoxicol Environ Saf 192:110292. https://doi.org/10.1016/j.ecoenv.2020.110292

    Article  CAS  PubMed  Google Scholar 

  31. Han P, Niu C, Desneux N (2014) Identification of top-down forces regulating cotton aphid population growth in transgenic Bt cotton in central China. PLoS ONE 9:e102980. https://doi.org/10.1371/journal.pone.0102980

    Article  PubMed  PubMed Central  Google Scholar 

  32. Zhao C, Wu L, Luo J, Niu L, Wang C, Zhu X, Wang L, Zhao P, Zhang S, Cui J (2020) Bt, not a threat to Propylea japonica. Front Physiol 11:1–12. https://doi.org/10.3389/fphys.2020.00758

    Article  Google Scholar 

  33. 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

    Article  CAS  PubMed  Google Scholar 

  34. Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke CH, Liess M, Long E, McField M, Mineau P, Mitchell EAD, Morrissey CA, Noome DA, Pisa L, Settele J, Stark JD, Tapparo A, Van Dyck H, Van Praagh J, Van der Sluijs JP, Whitehorn PR, Wiemers M (2015) Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ Sci Pollut Res 22:5–34. https://doi.org/10.1007/s11356-014-3470-y

    Article  CAS  Google Scholar 

  35. Opolot M, Lee SH, Kwak SY, Sarker A, Cho SC, Kim HJ, Jeong HR, Kim JE (2018) Dissipation patterns of insecticide sulfoxaflor in spinach and Korean cabbage. Korean J Pestic Sci 22:316–326. https://doi.org/10.7585/kjps.2018.22.4.316

    Article  Google Scholar 

  36. Kim SW, Rahman MM, Abd El-Aty AM, Kabir MH, Na TW, Choi JH, Shin HC, Shim JH (2017) Simultaneous detection of sulfoxaflor and its metabolites, X11719474 and X11721061, in lettuce using a modified QuEChERS extraction method and liquid chromatography–tandem mass spectrometry. Biomed Chromatogr 31:e3885. https://doi.org/10.1002/bmc.3885

    Article  CAS  Google Scholar 

  37. Gao X, Hu F, Zhang S, Luo J, Zhu X, Wang L, Zhang K, Li D, Ji J, Niu L, Wu C, Cui J (2021) Glyphosate exposure disturbs the bacterial endosymbiont community and reduces body weight of the predatory ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). Sci Total Environ 790:147847. https://doi.org/10.1016/j.scitotenv.2021.147847

    Article  CAS  PubMed  Google Scholar 

  38. Xu L, Zhao CQ, Zhang YN, Liu Y, Gu ZY (2016) Lethal and sublethal effects of sulfoxaflor on the small brown planthopper Laodelphax striatellus. J Asia-Pac Entomol 19:683–689. https://doi.org/10.1016/j.aspen.2016.06.013

    Article  Google Scholar 

  39. Zhao Y, Zhang S, Luo JY, Wang CY, Lv LM, Cui JJ (2016) Bacterial communities of the cotton aphid Aphis gossypii associated with Bt cotton in Northern China. Sci Rep 6:1–8. https://doi.org/10.1038/srep22958

    Article  CAS  Google Scholar 

  40. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604

    Article  CAS  PubMed  Google Scholar 

  42. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Thukral AK (2017) A review on measurement of alpha diversity in biology. Agric Res J 54:1–10. https://doi.org/10.5958/2395-146X.2017.00001.1

    Article  Google Scholar 

  44. Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8:e76548. https://doi.org/10.1371/journal.pone.0076548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Gontijo PC, Moscardini VF, Michaud JP, Carvalho GA (2014) Non-target effects of chlorantraniliprole and thiamethoxam on Chrysoperla carnea when employed as sunflower seed treatments. J Pest Sci 87:711–719. https://doi.org/10.1007/s10340-014-0611-5

    Article  Google Scholar 

  46. Dai C, Ricupero M, Puglisi R, Lu Y, Desneux N, Biondi A, Zappalà L (2020) Can contamination by major systemic insecticides affect the voracity of the harlequin ladybird? Chemosphere 256:126986. https://doi.org/10.1016/j.chemosphere.2020.126986

    Article  CAS  PubMed  Google Scholar 

  47. Xiao D, Zhao J, Guo X, Chen H, Qu M, Zhai W, Desneux N, Biondi A, Zhang F, Wang S (2016) Sublethal effects of imidacloprid on the predatory seven-spot ladybird beetle Coccinella septempunctata. Ecotoxicology 25:1782–1793. https://doi.org/10.1007/s10646-016-1721-z

    Article  CAS  PubMed  Google Scholar 

  48. Jiang J, Zhang Z, Yu X, Ma D, Yu C, Liu F, Mu W (2018) Influence of lethal and sublethal exposure to clothianidin on the seven-spotted lady beetle, Coccinella septempunctata L. (Coleoptera: Coccinellidae). Ecotoxicol Environ Saf 161:208–213. https://doi.org/10.1016/j.ecoenv.2018.05.076

    Article  CAS  PubMed  Google Scholar 

  49. Simelane DO, Steinkraus DC, Kring TJ (2008) Predation rate and development of Coccinella septempunctata L. influenced by Neozygites fresenii-infected cotton aphid prey. Biol Control 44:128–135. https://doi.org/10.1016/j.biocontrol.2007.10.004

    Article  Google Scholar 

  50. Dai C, Ricupero M, Wang Z, Desneux N, Biondi A, Lu Y (2021) Transgenerational effects of a neonicotinoid and a novel sulfoximine insecticide on the harlequin ladybird. Insects 12:681. https://doi.org/10.3390/insects12080681

    Article  PubMed  PubMed Central  Google Scholar 

  51. Nyman AM, Hintermeister A, Schirmer K, Ashauer R (2013) The insecticide imidacloprid causes mortality of the freshwater amphipod Gammarus pulex by interfering with feeding behavior. PLoS ONE 8:e62472. https://doi.org/10.1371/journal.pone.0062472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Xu N, Tan G, Wang H, Gai X (2016) Effect of biochar additions to soil on nitrogen leaching, microbial biomass and bacterial community structure. Eur J Soil Biol 74:1–8. https://doi.org/10.1016/j.ejsobi.2016.02.004

    Article  CAS  Google Scholar 

  53. Li F, Li M, Mao T, Wang H, Chen J, Lu Z, Qu J, Fang Y, Gu Z, Li B (2020) Effects of phoxim exposure on gut microbial composition in the silkworm Bombyxmori. Ecotoxicol Environ Saf 189:110011. https://doi.org/10.1016/j.ecoenv.2019.110011

    Article  CAS  PubMed  Google Scholar 

  54. Li F, Xu K, Ni M, Wang B, Gu Z, Shen W, Li B (2017) Effect of oxidative phosphorylation signaling pathway on silkworm midgut following exposure to phoxim. Environ Toxicol 32:167–175. https://doi.org/10.1002/tox.22222

    Article  CAS  PubMed  Google Scholar 

  55. Uhl P, Franke LA, Rehberg C, Wollmann C, Stahlschmidt P, Jeker L, Brühl CA (2016) Interspecific sensitivity of bees towards dimethoate and implications for environmental risk assessment. Sci Rep 6:1–7. https://doi.org/10.1038/srep34439

    Article  CAS  Google Scholar 

  56. Vorburger C, Rouchet R (2016) Are aphid parasitoids locally adapted to the prevalence of defensive symbionts in their hosts? BMC Evol Biol 16:1–11. https://doi.org/10.1186/s12862-016-0811-0

    Article  CAS  Google Scholar 

  57. Pan HP, Chu D, Liu BM, Xie W, Wang SL, Wu QJ, Xu BY, Zhang YJ (2013) Relative amount of symbionts in insect hosts changes with host-plant adaptation and insecticide resistance. Environ Entomol 42:74–78. https://doi.org/10.1603/EN12114

    Article  CAS  PubMed  Google Scholar 

  58. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92. https://doi.org/10.1146/annurev.ento.49.061802.123416

    Article  CAS  PubMed  Google Scholar 

  59. Trevelline BK, Fontaine SS, Hartup BK, Kohl KD (2019) Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. Proc R Soc B 286:20182448. https://doi.org/10.1098/rspb.2018.2448

    Article  PubMed  PubMed Central  Google Scholar 

  60. Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci U S A 109:8618–8622. https://doi.org/10.1073/pnas.1200231109

    Article  PubMed  PubMed Central  Google Scholar 

  61. Tang X, Freitak D, Vogel H, Ping L, Shao Y, Cordero EA, Andersen G, Westermann M, Heckel DG, Boland W (2012) Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLoS ONE 7:e36978. https://doi.org/10.1371/journal.pone.0036978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Possemiers S, Bolca S, Verstraete W, Heyerick A (2011) The intestinal microbiome: a separate organ inside the body with the metabolic potential to influence the bioactivity of botanicals. Fitoterapia 82:53–66. https://doi.org/10.1016/j.fitote.2010.07.012

    Article  CAS  PubMed  Google Scholar 

  63. Ruokolainen L, Ikonen S, Makkonen H, Hanski I (2016) Larval growth rate is associated with the composition of the gut microbiota in the Glanville fritillary butterfly. Oecologia 181:895–903. https://doi.org/10.1007/s00442-016-3603-8

    Article  CAS  PubMed  Google Scholar 

  64. Ma M, Chen X, Li S, Luo J, Han R, Xu L (2022) Composition and diversity of gut bacterial community in different life stages of a leaf beetle Gastrolina depressa. Microb Ecol. https://doi.org/10.1007/s00248-022-02054-0

  65. Anjum SI, Shah AH, Aurongzeb M, Kori J, Azim MK, Ansari MJ, Li B (2018) Characterization of gut bacterial flora of Apis mellifera from north-west Pakistan. Saudi J Biol Sci 25:388–392. https://doi.org/10.1016/j.sjbs.2017.05.008

    Article  PubMed  Google Scholar 

  66. Li F, Hu J, Tian J, Xu K, Ni M, Wang B, Shen W, Li B (2016) Effects of phoxim on nutrient metabolism and insulin signaling pathway in silkworm midgut. Chemosphere 146:478–485. https://doi.org/10.1016/j.chemosphere.2015.12.032

    Article  CAS  PubMed  Google Scholar 

  67. Eutick ML, O’Brien RW, Slaytor M (1978) Bacteria from the gut of Australian termites. Appl Environ Microb 35:823–828. https://doi.org/10.1128/aem.35.5.823-828.1978

    Article  CAS  Google Scholar 

  68. Collado MC, Isolauri E, Laitinen K, Salminen S (2008) Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr 88:894–899. https://doi.org/10.1093/ajcn/88.4.894

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the National Natural Science Fund of China (31672317), the Special Foundation for National Science and Technology Basic Research Program of China (2018FY100400), and the Frontier Projects of the Applied Foundation of Wuhan Science and Technology Bureau (2019020701011464).

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J.-J. C., Y. P., and Y. Z. conceived and designed the research. W. L., X.-Q. L., and W.-R. W. conducted the experiments. W. L., S.-C. Z., and Y. Z. analyzed the data and prepared the figures and tables. W. L. and Y. Z. wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Jinjie Cui, Yu Peng or Yao Zhao.

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Li, W., Li, X., Wang, W. et al. Impact of Sulfoxaflor Exposure on Bacterial Community and Developmental Performance of the Predatory Ladybeetle Propylea japonica. Microb Ecol 86, 1226–1239 (2023). https://doi.org/10.1007/s00248-022-02122-5

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