Academic Journal
Phenotypic divergence is driven by mobile genetic elements in a heritable insect symbiont.
| Τίτλος: | Phenotypic divergence is driven by mobile genetic elements in a heritable insect symbiont. |
|---|---|
| Συγγραφείς: | Panossian B; School of Biological and Behavioural Sciences, Queen Mary University of London, London E1 4NS, United Kingdom., Kolp MR; Department of Microbiology, University of Tennessee, Knoxville, TN 37996., Wu T; School of Biological and Behavioural Sciences, Queen Mary University of London, London E1 4NS, United Kingdom., Tallapragada K; Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599., Patel V; Department of Entomology, University of Georgia, Athens, GA 30602., Goldstein EB; Department of Microbiology, University of Tennessee, Knoxville, TN 37996., Oliver KM; Department of Entomology, University of Georgia, Athens, GA 30602., Henry LM; School of Biological and Behavioural Sciences, Queen Mary University of London, London E1 4NS, United Kingdom., Parker BJ; Department of Microbiology, University of Tennessee, Knoxville, TN 37996.; Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599. |
| Πηγή: | Proceedings of the National Academy of Sciences of the United States of America [Proc Natl Acad Sci U S A] 2026 Sep 29; Vol. 123 (39), pp. e2607226123. Date of Electronic Publication: 2026 Sep 21. |
| Τύπος έκδοσης: | Journal Article |
| Γλώσσα: | English |
| Στοιχεία περιοδικού: | Publisher: National Academy of Sciences Country of Publication: United States NLM ID: 7505876 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1091-6490 (Electronic) Linking ISSN: 00278424 NLM ISO Abbreviation: Proc Natl Acad Sci U S A Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: Washington, DC : National Academy of Sciences |
| Ιατρικοί όροι (MeSH): | Symbiosis*/genetics , Aphids*/microbiology , Aphids*/genetics , Interspersed Repetitive Sequences*/genetics , Enterobacteriaceae*/genetics, Plasmids/genetics ; Animals ; Phenotype ; Phylogeny ; Gene Transfer, Horizontal |
| Περίληψη: | Heritable microbes profoundly influence insect biology, yet the traits they confer often evolve rapidly and differ among closely related symbiont strains. Despite their importance, we lack a clear understanding of how novel traits arise in symbionts and how this diversity influences host ecology in nature. The aphid facultative symbiont Regiella insecticola is ideally suited to address this question due to strong lineage-specific variation in host benefits. By generating 20 high-quality genomes, we found that Regiella's evolution is driven largely by gene gains mediated by mobile genetic elements (MGEs). A plasmid (pRILSR1) encoding a type IV secretion system and a highly expressed predicted effector has spread horizontally between distantly related Regiella clades associated with pea aphids. Notably, only pRILSR1-bearing strains confer protection against the fungal pathogen Pandora neoaphidis. Moreover, loss of the plasmid by a protective strain in culture resulted in the loss of protection, indicating that pRILSR1 is required for the defensive phenotype. In a multiyear field study, pRILSR1 frequency varied systematically among host plant-associated pea aphid populations and predicted differences in symbiont-mediated fungal resistance. Together, our results show that gain and loss of a single MGE contributes to divergence in a key adaptive trait, providing a mechanism by which symbiont evolution generates phenotypic differences among host populations. |
| Competing Interests: | Competing interests statement:The authors declare no competing interest. |
| References: | Bioinformatics. 2018 Jan 15;34(2):292-293. (PMID: 29028899) Proc Biol Sci. 2022 Oct 26;289(1985):20221269. (PMID: 36285493) Mol Biol Evol. 2024 Apr 2;41(4):. (PMID: 38577785) Bioinformatics. 2015 Jan 15;31(2):166-9. (PMID: 25260700) Bioinformatics. 2015 Oct 15;31(20):3350-2. (PMID: 26099265) Curr Biol. 2013 Sep 9;23(17):1713-7. (PMID: 23993843) Curr Biol. 2024 Dec 16;34(24):5659-5670.e7. (PMID: 39549700) Annu Rev Entomol. 1998;43:17-37. (PMID: 15012383) Nature. 2018 May;557(7704):252-255. (PMID: 29720654) Evolution. 2023 Jun 29;77(7):1704-1711. (PMID: 37094805) Mol Biol Evol. 2026 May 01;43(5):. (PMID: 41873149) Trends Ecol Evol. 2012 Apr;27(4):226-32. (PMID: 22104387) Mol Ecol. 2023 Feb;32(4):936-950. (PMID: 36458425) ISME J. 2021 Sep;15(9):2537-2546. (PMID: 33712703) Bioinformatics. 2008 Aug 15;24(16):1757-64. (PMID: 18567917) Nature. 2017 Mar 9;543(7644):243-247. (PMID: 28241146) Ecol Lett. 2015 Jun;18(6):516-25. (PMID: 25868533) Science. 2004 Mar 26;303(5666):1989. (PMID: 15044797) Proc Biol Sci. 2020 Jun 24;287(1929):20200562. (PMID: 32546097) Mol Ecol. 2002 Oct;11(10):2123-35. (PMID: 12296954) Nat Rev Microbiol. 2003 Nov;1(2):137-49. (PMID: 15035043) Mol Ecol. 2017 Aug;26(15):4072-4084. (PMID: 28464440) Curr Biol. 2020 May 18;30(10):1949-1957.e6. (PMID: 32243856) Mol Ecol Resour. 2008 Nov;8(6):1189-201. (PMID: 21586006) Curr Biol. 2019 Jun 3;29(11):R521-R537. (PMID: 31163166) Bioinformatics. 2015 Nov 15;31(22):3691-3. (PMID: 26198102) Biol Lett. 2017 May;13(5):. (PMID: 28566541) Bioinformatics. 2010 Mar 1;26(5):589-95. (PMID: 20080505) Appl Environ Microbiol. 2013 Apr;79(7):2455-8. (PMID: 23354709) Genome Biol Evol. 2019 Dec 1;11(12):3510-3522. (PMID: 31725149) Environ Microbiol. 2023 Dec;25(12):3333-3348. (PMID: 37864320) Bioinformatics. 2014 May 1;30(9):1312-3. (PMID: 24451623) Curr Protoc Bioinformatics. 2020 Jun;70(1):e102. (PMID: 32559359) J Evol Biol. 2015 Oct;28(10):1753-60. (PMID: 26206380) Proc Natl Acad Sci U S A. 2023 May 2;120(18):e2217278120. (PMID: 37094148) Genome Biol Evol. 2018 Mar 1;10(3):786-802. (PMID: 29452355) Bioinformatics. 2018 Sep 1;34(17):i884-i890. (PMID: 30423086) Mol Microbiol. 2021 Mar;115(3):436-452. (PMID: 33326642) Mol Biol Evol. 2021 Sep 27;38(10):4647-4654. (PMID: 34320186) Nat Rev Genet. 2022 Jan;23(1):23-39. (PMID: 34389828) Evolution. 2017 May;71(5):1222-1231. (PMID: 28252804) Oecologia. 2007 Aug;153(2):323-9. (PMID: 17415589) Genome Biol Evol. 2019 Jan 1;11(1):253-262. (PMID: 30576446) Appl Environ Microbiol. 2003 Feb;69(2):820-6. (PMID: 12571000) Nat Methods. 2021 Apr;18(4):366-368. (PMID: 33828273) IEEE/ACM Trans Comput Biol Bioinform. 2022 Nov-Dec;19(6):3564-3577. (PMID: 34469305) Nucleic Acids Res. 2021 Jul 2;49(W1):W293-W296. (PMID: 33885785) Biom J. 2008 Jun;50(3):346-63. (PMID: 18481363) Biol Lett. 2010 Feb 23;6(1):109-11. (PMID: 19776066) Genome Res. 2009 Sep;19(9):1639-45. (PMID: 19541911) Bioinformatics. 2010 Jan 1;26(1):139-40. (PMID: 19910308) Proc Natl Acad Sci U S A. 2015 Aug 18;112(33):10169-76. (PMID: 25713367) BMC Genomics. 2020 Mar 14;21(1):230. (PMID: 32171249) Nat Microbiol. 2021 Dec;6(12):1575-1582. (PMID: 34819638) Bioinformatics. 2016 Oct 1;32(19):3047-8. (PMID: 27312411) Nucleic Acids Res. 2016 Jul 8;44(W1):W16-21. (PMID: 27141966) Bioinformatics. 2019 Oct 15;35(20):4162-4164. (PMID: 30865266) Mol Ecol. 2008 Feb;17(3):916-29. (PMID: 18179430) Annu Rev Entomol. 2010;55:247-66. (PMID: 19728837) Environ Microbiol. 2010 Aug;12(8):2060-9. (PMID: 21966902) PLoS Comput Biol. 2011 Oct;7(10):e1002195. (PMID: 22039361) Evolution. 2014 Aug;68(8):2421-9. (PMID: 24689981) Mol Ecol. 2013 Apr;22(7):2045-59. (PMID: 23379399) Microbiol Resour Announc. 2020 Oct 1;9(40):. (PMID: 33004445) Proc Biol Sci. 2013 Jan 22;280(1751):20122103. (PMID: 23193123) Appl Environ Microbiol. 2024 Jun 18;90(6):e0229323. (PMID: 38786361) Mol Biol Evol. 2018 Feb 1;35(2):518-522. (PMID: 29077904) Mol Biol Evol. 2015 Jan;32(1):268-74. (PMID: 25371430) Ecol Lett. 2025 Feb;28(2):e70082. (PMID: 39964074) Genome Res. 2012 Jan;22(1):106-14. (PMID: 21948522) Genome Res. 2015 Jul;25(7):1043-55. (PMID: 25977477) Annu Rev Genet. 2008;42:165-90. (PMID: 18983256) Nucleic Acids Res. 2023 Jan 6;51(D1):D389-D394. (PMID: 36399505) Bioinformatics. 2009 Aug 1;25(15):1972-3. (PMID: 19505945) Evolution. 2012 Feb;66(2):375-90. (PMID: 22276535) Proc Natl Acad Sci U S A. 2014 Jul 15;111(28):10257-62. (PMID: 24982177) J Anim Ecol. 2017 May;86(3):473-483. (PMID: 28211052) Science. 2005 Dec 16;310(5755):1781. (PMID: 16357252) Nucleic Acids Res. 2021 Jan 8;49(D1):D651-D659. (PMID: 33084862) PLoS Biol. 2010 Feb 23;8(2):e1000313. (PMID: 20186266) BMC Bioinformatics. 2010 Mar 08;11:119. (PMID: 20211023) Science. 2009 Aug 21;325(5943):992-4. (PMID: 19696350) Protein Sci. 2020 Jan;29(1):28-35. (PMID: 31423653) Bioinformatics. 2009 Aug 15;25(16):2078-9. (PMID: 19505943) Nat Methods. 2017 Jun;14(6):587-589. (PMID: 28481363) Proc Biol Sci. 2011 Mar 7;278(1706):760-6. (PMID: 20843842) Bioinformatics. 2018 Sep 15;34(18):3094-3100. (PMID: 29750242) Nat Methods. 2020 Nov;17(11):1103-1110. (PMID: 33020656) mBio. 2018 Mar 20;9(2):. (PMID: 29559567) Nat Commun. 2022 Nov 15;13(1):6968. (PMID: 36379955) Proc Biol Sci. 2024 Jul;291(2027):20240680. (PMID: 39079670) Proc Natl Acad Sci U S A. 2024 May 14;121(20):e2310348121. (PMID: 38709922) Proc Biol Sci. 2017 Nov 15;284(1866):. (PMID: 29093227) Proc Natl Acad Sci U S A. 2008 Sep 16;105(37):14141-6. (PMID: 18787122) Bioinformatics. 2014 Jul 15;30(14):2068-9. (PMID: 24642063) BMC Bioinformatics. 2009 Dec 15;10:421. (PMID: 20003500) Syst Biol. 2010 May;59(3):307-21. (PMID: 20525638) Bioinformatics. 2020 Apr 1;36(7):2251-2252. (PMID: 31742321) Nucleic Acids Res. 2024 Jan 5;52(D1):D756-D761. (PMID: 37904614) Microbiome. 2018 Oct 10;6(1):181. (PMID: 30305166) J Mol Biol. 1983 Jul 25;168(1):17-33. (PMID: 6410077) |
| Grant Information: | IOS2152954 US NSF; R35GM154800 US NIH; BB/W001632/1 UK BBSRC; DBI2109440 US NSF |
| Contributed Indexing: | Keywords: horizontal gene transfer; mobile genetic elements; pathogenic fungi; symbiosis |
| Entry Date(s): | Date Created: 20260921 Date Completed: 20260921 Latest Revision: 20261001 |
| Update Code: | 20261001 |
| DOI: | 10.1073/pnas.2607226123 |
| PMID: | 42766741 |
| Βάση Δεδομένων: | MEDLINE |
| ISSN: | 1091-6490 |
|---|---|
| DOI: | 10.1073/pnas.2607226123 |