{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,1]],"date-time":"2026-05-01T11:59:43Z","timestamp":1777636783089,"version":"3.51.4"},"reference-count":55,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T00:00:00Z","timestamp":1777420800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>\n                    <jats:italic>Aphidius gifuensis<\/jats:italic>\n                    is an important parasitic wasp used to control\n                    <jats:italic>Myzus persicae<\/jats:italic>\n                    (tobacco aphid), a key pest in tobacco-producing areas. Over the past 10 years, the use of\n                    <jats:italic>A. gifuensis<\/jats:italic>\n                    has been widely promoted, and its natural population has steadily increased, playing a crucial role in aphid control and the prevention of aphid-transmitted viral diseases. However, long-term aphid protection and inbreeding of\n                    <jats:italic>A. gifuensis<\/jats:italic>\n                    populations have led to the degeneration of the species, reduced parasitism efficiency, and increased control costs. In response to these challenges, this study investigated the effects of symbiotic bacteria on the parasitism and reproductive capacity of\n                    <jats:italic>A. gifuensis<\/jats:italic>\n                    . The results show that\n                    <jats:italic>Bacillus subtilis<\/jats:italic>\n                    and\n                    <jats:italic>Exiguobacterium gifuensis<\/jats:italic>\n                    significantly promoted the parasitism rate of\n                    <jats:italic>A. gifuensis<\/jats:italic>\n                    , with the highest increases of 5.33 and 3.67%, respectively, compared to the control. Additionally, the presence of\n                    <jats:italic>Acinetobacter radioresistens<\/jats:italic>\n                    altered the activity of the superoxide dismutase (SOD) enzyme in\n                    <jats:italic>A. gifuensis<\/jats:italic>\n                    . At all tested concentrations, except for 0.97 \u00d7 10\n                    <jats:sup>10<\/jats:sup>\n                    CFU\/mL\n                    <jats:sup>\u20131<\/jats:sup>\n                    , SOD enzyme protein levels were inhibited, with the greatest reduction of 1.81% compared to the control. Furthermore,\n                    <jats:italic>A. radioresistens<\/jats:italic>\n                    significantly reduced the total activity of the SOD enzyme by 1.54%.\n                    <jats:italic>Bacillus subtilis<\/jats:italic>\n                    also significantly suppressed phenoloxidase activity, which was reduced by 44.78% compared to the control. These findings suggest that\n                    <jats:italic>B. subtilis<\/jats:italic>\n                    and\n                    <jats:italic>E. gifuensis<\/jats:italic>\n                    are beneficial for enhancing the parasitism efficacy of\n                    <jats:italic>A. gifuensis<\/jats:italic>\n                    in controlling\n                    <jats:italic>M. persicae<\/jats:italic>\n                    .\n                  <\/jats:p>","DOI":"10.3389\/fmicb.2026.1811839","type":"journal-article","created":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T05:54:51Z","timestamp":1777442091000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Effects of symbiotic bacteria on the parasitism efficacy of Aphidius gifuensis against Myzus persicae"],"prefix":"10.3389","volume":"17","author":[{"given":"Gul Warin","family":"Khan","sequence":"first","affiliation":[{"name":"State Key Laboratory of Agriculture and Forestry Biosecurity\/Biological Control Research Institute, Fujian Agriculture and Forestry University","place":["Fuzhou, China"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gang","family":"Gu","sequence":"additional","affiliation":[{"name":"Fujian Province Corporation of China National Tobacco Corporation","place":["Fuzhou, China"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yufei","family":"Lai","sequence":"additional","affiliation":[{"name":"College of Plant Protection, Shandong Agricultural University","place":["Tai\u2019an, China"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chen","family":"Yang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Agriculture and Forestry Biosecurity\/Biological Control Research Institute, Fujian Agriculture and Forestry University","place":["Fuzhou, China"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ting","family":"Zhou","sequence":"additional","affiliation":[{"name":"Fujian Province Corporation of China National Tobacco Corporation","place":["Fuzhou, China"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rongquan","family":"Lai","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Agriculture and Forestry Biosecurity\/Biological Control Research Institute, Fujian Agriculture and Forestry University","place":["Fuzhou, China"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bang","family":"Zhang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Agriculture and Forestry Biosecurity\/Biological Control Research Institute, Fujian Agriculture and Forestry University","place":["Fuzhou, China"]}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2026,4,29]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"714","DOI":"10.3390\/plants12040714","article-title":"Interaction of plants and endophytic microorganisms: Molecular aspects, biological functions, community composition, and practical applications.","volume":"12","author":"Aleynova","year":"2023","journal-title":"Plants"},{"key":"B2","doi-asserted-by":"publisher","first-page":"476","DOI":"10.1590\/1678-4685-GMB-2016-0057","article-title":"The diversity of citrus endophytic bacteria and their interactions with Xylella fastidiosa and host plants.","volume":"39","author":"Azevedo","year":"2016","journal-title":"Genet. Mol. Biol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"276","DOI":"10.1016\/0003-2697(71)90370-8","article-title":"Superoxide dismutase: improved assays and an assay applicable to acrylamide gels","volume":"44","author":"Beauchamp","year":"1971","journal-title":"Anal. Biochem."},{"key":"B4","doi-asserted-by":"publisher","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"B5","doi-asserted-by":"publisher","first-page":"104098","DOI":"10.1016\/j.dci.2021.104098","article-title":"Immune properties of invertebrate phenoloxidases.","volume":"122","author":"Cerenius","year":"2021","journal-title":"Dev. Comp. Immunol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"392","DOI":"10.3390\/insects16040392","article-title":"From digestion to detoxification: Exploring plant metabolite impacts on insect enzyme systems for enhanced pest control.","volume":"16","author":"Chamani","year":"2025","journal-title":"Insects"},{"key":"B7","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1111\/gcb.16561","article-title":"Challenges in upscaling laboratory studies to ecosystems in soil microbiology research.","volume":"29","author":"Chen","year":"2023","journal-title":"Glob. Chang. Biol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"1972","DOI":"10.3390\/agronomy13081972","article-title":"Bacteria-mediated regulation of Aphidius gifuensis parasitism efficacy in Myzus persicae: Implications for biological control strategies.","volume":"13","author":"Chengpeng","year":"2025","journal-title":"Agronomy"},{"key":"B9","doi-asserted-by":"publisher","first-page":"fiac083","DOI":"10.1093\/femsec\/fiac083","article-title":"The secret life of insect-associated microbes and how they shape insect\u2013plant interactions.","volume":"98","author":"Coolen","year":"2022","journal-title":"FEMS Microbiol. Ecol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1186\/1741-7007-6-27","article-title":"The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone.","volume":"6","author":"Duron","year":"2008","journal-title":"BMC Biol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"46","DOI":"10.3389\/fphys.2013.00046","article-title":"Endophytic bacteria in insects: Guardians of the immune system?","volume":"4","author":"Eleftherianos","year":"2013","journal-title":"Front. Physiol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"1161","DOI":"10.3390\/insects13111161","article-title":"Rickettsia infection benefits its whitefly hosts by manipulating their nutrition and defense.","volume":"13","author":"Fan","year":"2022","journal-title":"Insects"},{"key":"B13","doi-asserted-by":"publisher","first-page":"570","DOI":"10.3390\/pathogens10040570","article-title":"Endophytic fungi: Biological control and induced resistance to phytopathogens and abiotic stresses.","volume":"10","author":"Fontana","year":"2021","journal-title":"Pathogens"},{"key":"B14","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1007\/978-1-0716-3553-7_4","article-title":"Examining Wolbachia-induced parthenogenesis in Hymenoptera.","volume":"2739","author":"Fricke","year":"2023","journal-title":"Methods Mol. Biol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"791","DOI":"10.1098\/rspb.2005.3383","article-title":"Wolbachia infection suppresses both host defence and parasitoid counter-defence.","volume":"273","author":"Fytrou","year":"2006","journal-title":"Proc. Biol. Sci."},{"key":"B16","doi-asserted-by":"publisher","first-page":"100114","DOI":"10.1016\/j.cris.2025.100114","article-title":"Antioxidants, oxidative stress and reactive oxygen species in insects exposed to heat.","volume":"7","author":"Gonz\u00e1lez-Tokman","year":"2025","journal-title":"Curr. Res. Insect Sci."},{"key":"B17","doi-asserted-by":"publisher","first-page":"20180115","DOI":"10.1098\/rstb.2018.0115","article-title":"Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model.","volume":"374","author":"Groothuis","year":"2019","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"B18","doi-asserted-by":"publisher","first-page":"794","DOI":"10.1016\/j.aspen.2017.06.002","article-title":"Nine facultative endosymbionts in aphids: A review.","volume":"20","author":"Guo","year":"2017","journal-title":"J. Asia Pac. Entomol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1007\/s00284-005-0233-5","article-title":"The first finding of a Rickettsia bacterium associated with parthenogenesis induction among insects.","volume":"52","author":"Hagimori","year":"2006","journal-title":"Curr. Microbiol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1016\/j.cbi.2016.04.006","article-title":"Carboxylesterases: General detoxifying enzymes.","volume":"259","author":"Hatfield","year":"2016","journal-title":"Chem. Biol. Interact."},{"key":"B21","doi-asserted-by":"publisher","first-page":"e11699","DOI":"10.1002\/ece3.11699","article-title":"Insect-microbe interactions and their influence on organisms and ecosystems.","volume":"14","author":"Holt","year":"2024","journal-title":"Ecol. Evol."},{"key":"B22","first-page":"123","article-title":"Effects of insecticide stress on antioxidant enzymes in aphids","volume":"52","author":"Hui","year":"2006","journal-title":"J. Insect Physiol"},{"key":"B23","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1016\/j.bioactmat.2025.02.003","article-title":"Enhanced sequential osteosarcoma therapy using a 3D-printed bioceramic scaffold combined with 2D nanosheets via NIR-II photothermal-chemodynamic synergy.","volume":"50","author":"Jian","year":"2025","journal-title":"Bioact. Mater."},{"key":"B24","doi-asserted-by":"publisher","first-page":"105053","DOI":"10.1016\/j.pestbp.2021.105053","article-title":"Effects of insecticide exposure on metabolic enzyme activity and gene expression in Aphidius gifuensis (Hymenoptera: Braconidae).","volume":"181","author":"Jing","year":"2022","journal-title":"Pestic. Biochem. Physiol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.cropro.2017.05.013","article-title":"Myzus persicae and aphid-transmitted viral disease control via variety intercropping in flue-cured tobacco.","volume":"100","author":"Lai","year":"2017","journal-title":"Crop Prot."},{"key":"B26","doi-asserted-by":"publisher","first-page":"311","DOI":"10.3390\/insects16030311","article-title":"How insects balance reproductive output and immune investment.","volume":"16","author":"Leyria","year":"2025","journal-title":"Insects"},{"key":"B27","doi-asserted-by":"publisher","first-page":"1379","DOI":"10.1038\/s41598-024-41269-1","article-title":"Natural selection and genetic diversity maintenance in a parasitic wasp during continuous biological control application.","volume":"15","author":"Li","year":"2024","journal-title":"Nat. Commun."},{"key":"B28","doi-asserted-by":"publisher","first-page":"2419","DOI":"10.3389\/fmicb.2019.02419","article-title":"Anti-plant defense response strategies mediated by the secondary symbiont Hamiltonella defensa in the wheat aphid Sitobion miscanthi.","volume":"10","author":"Li","year":"2019","journal-title":"Front. Microbiol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1186\/s12915-024-01300-3","article-title":"Comparative genomics of the primary endosymbiont Buchnera aphidicola in aphid hosts and their coevolutionary relationships.","volume":"22","author":"Liang","year":"2024","journal-title":"BMC Biol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"e2406788121","DOI":"10.1073\/pnas.2406788121","article-title":"Rickettsia symbionts spread via mixed mode transmission, increasing female fecundity and sex ratio shift by host hormone modulation.","volume":"121","author":"Liu","year":"2024","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B31","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1016\/j.jot.2025.01.006","article-title":"The role of multi-omics in biomarker discovery, diagnosis, prognosis, and therapeutic monitoring of tissue repair and regeneration processes.","volume":"54","author":"Liu","year":"2025","journal-title":"J. Orthop. Translat."},{"key":"B32","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1146\/annurev-ento-121423-012130","article-title":"Biological control of aphids in China: Successes and prospects.","volume":"70","author":"Liu","year":"2024","journal-title":"Annu. Rev. Entomol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"1407","DOI":"10.1126\/science.164.3883.1407","article-title":"Aphid transmission of tobacco mosaic virus.","volume":"164","author":"Lojek","year":"1969","journal-title":"Science"},{"key":"B34","doi-asserted-by":"publisher","first-page":"252","DOI":"10.3389\/fphys.2014.00252","article-title":"Insect prophenoloxidase: The view beyond immunity.","volume":"5","author":"Lu","year":"2014","journal-title":"Front. Physiol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1146\/annurev-ento-020423-092901","article-title":"Insect bacteriocytes: Adaptation, development, and evolution.","volume":"69","author":"Luan","year":"2024","journal-title":"Annu. Rev. Entomol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"20240446","DOI":"10.1098\/rspb.2024.0446","article-title":"Pleiotropy alleviates the fitness costs associated with resource allocation trade-offs in immune signaling networks.","volume":"291","author":"Martin","year":"2024","journal-title":"Proc. Biol. Sci."},{"key":"B37","doi-asserted-by":"publisher","first-page":"20200562","DOI":"10.1098\/rspb.2020.0562","article-title":"Multiple phenotypes conferred by a single insect symbiont are independent.","volume":"287","author":"McLean","year":"2020","journal-title":"Proc. Biol. Sci."},{"key":"B38","doi-asserted-by":"publisher","first-page":"12324","DOI":"10.1074\/jbc.M117.803399","article-title":"The iron-dependent mitochondrial superoxide dismutase SODA promotes Leishmania virulence.","volume":"292","author":"Mittra","year":"2017","journal-title":"J. Biol. Chem."},{"key":"B39","doi-asserted-by":"publisher","first-page":"4065","DOI":"10.1038\/s41598-023-36616-5","article-title":"Symbiont-host interactome mapping reveals effector-targeted modulation of hormone networks and activation of growth promotion.","volume":"14","author":"Osborne","year":"2023","journal-title":"Nat. Commun."},{"key":"B40","doi-asserted-by":"publisher","first-page":"522","DOI":"10.3390\/horticulturae11050522","article-title":"Biocontrol in integrated pest management in fruit and vegetable field production.","volume":"11","author":"Pobo\u017cniak","year":"2025","journal-title":"Horticulturae"},{"key":"B41","doi-asserted-by":"publisher","first-page":"3854","DOI":"10.1021\/cr400677r","article-title":"Superoxide dismutases and superoxide reductases.","volume":"114","author":"Sheng","year":"2014","journal-title":"Chem. Rev."},{"key":"B42","doi-asserted-by":"publisher","first-page":"20212660","DOI":"10.1098\/rspb.2021.2660","article-title":"Impact of heat stress on the fitness outcomes of symbiotic infection in aphids: A meta-analysis.","volume":"289","author":"Tougeron","year":"2022","journal-title":"Proc. Biol. Sci."},{"key":"B43","doi-asserted-by":"publisher","first-page":"e00954","DOI":"10.1002\/mbo3.954","article-title":"The ecological role of bacterial seed endophytes associated with wild cabbage in the United Kingdom.","volume":"9","author":"Tyc","year":"2020","journal-title":"Microbiologyopen"},{"key":"B44","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1016\/0022-1910(62)90074-4","article-title":"A study of housefly esterases by means of a sensitive colorimetric method","volume":"8","author":"van Asperen","year":"1962","journal-title":"J. Insect. Physiol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"787","DOI":"10.1098\/rspb.2007.1588","article-title":"Population dynamics and sex ratio of a parasitoid altered by fungal-infected diet of host butterfly.","volume":"275","author":"van Nouhuys","year":"2008","journal-title":"Proc. Biol. Sci."},{"key":"B46","doi-asserted-by":"publisher","first-page":"1510036","DOI":"10.3389\/fmicb.2025.1510036","article-title":"The role of Bacillus species in the management of plant-parasitic nematodes.","volume":"15","author":"Vasantha-Srinivasan","year":"2025","journal-title":"Front. Microbiol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/j.mib.2004.02.003","article-title":"Proteomic and gene profiling approaches to study host responses to bacterial infection.","volume":"7","author":"Walduck","year":"2004","journal-title":"Curr. Opin. Microbiol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"1915","DOI":"10.1083\/jcb.201803100","article-title":"Superoxide dismutases: Dual roles in controlling ROS damage and regulating ROS signaling.","volume":"217","author":"Wang","year":"2018","journal-title":"J. Cell Biol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"866","DOI":"10.1002\/ps.5793","article-title":"The evolving story of sulfoxaflor resistance in the green peach aphid, Myzus persicae (Sulzer).","volume":"80","author":"Ward","year":"2024","journal-title":"Pest Manag. Sci."},{"key":"B50","doi-asserted-by":"publisher","first-page":"1972","DOI":"10.3390\/agronomy13081972","article-title":"Natural-enemy-based biocontrol of tobacco arthropod pests in China.","volume":"13","author":"Xue","year":"2023","journal-title":"Agronomy"},{"key":"B51","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.pestbp.2015.10.018","article-title":"Gene expression analysis and enzyme assay reveal a potential role of the carboxylesterase gene CpCE-1 from Cydia pomonella in detoxification of insecticides.","volume":"129","author":"Yang","year":"2016","journal-title":"Pestic. Biochem. Physiol."},{"key":"B52","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1201\/9781003169239-2","article-title":"Development and area-wide application of biological control using the parasitoid Aphidius gifuensis against Myzus persicae in China","volume-title":"Area-Wide Integrated Pest Management: Development and Field Application","author":"Yu","year":"2021"},{"key":"B53","doi-asserted-by":"publisher","first-page":"1005","DOI":"10.1002\/ps.5793","article-title":"Wolbachia-infected Trichogramma dendrolimi is outcompeted by its uninfected counterpart in superparasitism but does not have developmental delay.","volume":"79","author":"Zhou","year":"2023","journal-title":"Pest Manag. Sci."},{"key":"B54","doi-asserted-by":"publisher","first-page":"730664","DOI":"10.3389\/fevo.2021.730664","article-title":"Effects of thelytokous parthenogenesis-inducing Wolbachia on the fitness of Trichogramma dendrolimi Matsumura (Hymenoptera: Trichogrammatidae) in superparasitized and single-parasitized hosts.","volume":"9","author":"Zhou","year":"2021","journal-title":"Front. Ecol. Evol."},{"key":"B55","doi-asserted-by":"publisher","first-page":"72","DOI":"10.13496\/j.issn.1007-5119.2015.03.014","article-title":"Effects of conventional insecticides on Aphidius gifuensis Ashmead and its protective enzymes in tobacco fields","volume":"36","author":"Zhu","year":"2015","journal-title":"Chin. Tobacco Sci."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2026.1811839\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T05:54:53Z","timestamp":1777442093000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2026.1811839\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,4,29]]},"references-count":55,"alternative-id":["10.3389\/fmicb.2026.1811839"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2026.1811839","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,4,29]]},"article-number":"1811839"}}