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Although mito-nuclear incompatibility is known to impair mitochondrial function and contribute to hybrid breakdown, its effects on metabolic coordination between cellular organelles remain poorly understood, particularly in insects. Here, we used the black soldier fly (Hermetia illucens L.) as an experimental model and established a mito-nuclear incompatibility system by introducing heterologous mitochondrial genomes into a common nuclear background. Integrating genomic, transcriptomic, metabolomic, and functional analyses, we found that mito-nuclear mismatch disrupted not only mitochondrial oxidative phosphorylation but also peroxisome biogenesis and fatty acid metabolism. We identified the peroxisomal acyl-CoA oxidases ACOX1 and ACOX3 as important components associated with mito-nuclear incompatibility-induced disruption of mitochondria\u2013peroxisome metabolic coordination. Functional knockdown of acyl-CoA oxidase (ACOX) genes recapitulated major metabolic and fitness-related phenotypes associated with mito-nuclear mismatch, including energy deficiency, oxidative stress, delayed larval development, and reduced adult reproductive performance. Moreover, restoration of redox and energetic homeostasis partially rescued ACOX expression, whereas reinstating ACOX expression alleviated lipid metabolic defects in mismatched lines. Together, these findings support a model in which mito-nuclear incompatibility disrupts mitochondrial function and peroxisomal metabolic homeostasis, with reduced ACOX-dependent fatty acid metabolism representing an important component of broader mitochondria\u2013peroxisome metabolic dysregulation. Our findings reveal a previously underappreciated role of mito-nuclear interactions in coordinating mitochondrial\u2013peroxisomal metabolism and provide a mechanistic framework for understanding how genomic compatibility influences metabolic integration across cellular organelles.<\/jats:p>","DOI":"10.1093\/molbev\/msag241","type":"journal-article","created":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T19:24:57Z","timestamp":1789673097000},"source":"Crossref","is-referenced-by-count":0,"title":["Mito-nuclear incompatibility disrupts acyl-CoA oxidase 1\/acyl-CoA oxidase 3\u2013mediated mitochondria\u2013peroxisome metabolic coordination in black soldier flies"],"prefix":"10.1093","volume":"43","author":[{"ORCID":"https:\/\/orcid.org\/0009-0009-1726-5340","authenticated-orcid":false,"given":"Xue","family":"Wang","sequence":"first","affiliation":[{"name":"College of Life Sciences, Nankai University , Tianjin 300071 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-7276-0176","authenticated-orcid":false,"given":"Shuyun","family":"Zhao","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nankai University , Tianjin 300071 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3898-8002","authenticated-orcid":false,"given":"Guoxin","family":"Huang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nankai University , Tianjin 300071 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0001-2158-0396","authenticated-orcid":false,"given":"Runjia","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nankai University , Tianjin 300071 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