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Repeated, Selection-Driven Genome Reduction of Accessory Genes in Experimental Populations
Genome reduction has been observed in many bacterial lineages that have adapted to specialized environments. The extreme genome degradation seen for obligate pathogens and symbionts appears to be dominated by genetic drift. In contrast, for free-living organisms with reduced genomes, the dominant force is proposed to be direct selection for smaller, streamlined genomes. Most variation in gene content for these free-living species is of “accessory” genes, which are commonly gained as large chromosomal islands that are adaptive for specialized traits such as pathogenicity. It is generally unclear, however, whether the process of accessory gene loss is largely driven by drift or selection. Here we demonstrate that selection for gene loss, and not a shortened genome, per se, drove massive, rapid reduction of accessory genes. In just 1,500 generations of experimental evolution, 80% of populations of Methylobacterium extorquens AM1 experienced nearly parallel deletions removing up to 10% of the genome from a megaplasmid present in this strain. The absence of these deletion events in a mutation accumulation experiment suggested that selection, rather than drift, has dominated the process. Reconstructing these deletions confirmed that they were beneficial in their selective regimes, but led to decreased performance in alternative environments. These results indicate that selection can be crucial in eliminating unnecessary genes during the early stages of adaptation to a specialized environment.
Vyšlo v časopise: Repeated, Selection-Driven Genome Reduction of Accessory Genes in Experimental Populations. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002651
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002651Souhrn
Genome reduction has been observed in many bacterial lineages that have adapted to specialized environments. The extreme genome degradation seen for obligate pathogens and symbionts appears to be dominated by genetic drift. In contrast, for free-living organisms with reduced genomes, the dominant force is proposed to be direct selection for smaller, streamlined genomes. Most variation in gene content for these free-living species is of “accessory” genes, which are commonly gained as large chromosomal islands that are adaptive for specialized traits such as pathogenicity. It is generally unclear, however, whether the process of accessory gene loss is largely driven by drift or selection. Here we demonstrate that selection for gene loss, and not a shortened genome, per se, drove massive, rapid reduction of accessory genes. In just 1,500 generations of experimental evolution, 80% of populations of Methylobacterium extorquens AM1 experienced nearly parallel deletions removing up to 10% of the genome from a megaplasmid present in this strain. The absence of these deletion events in a mutation accumulation experiment suggested that selection, rather than drift, has dominated the process. Reconstructing these deletions confirmed that they were beneficial in their selective regimes, but led to decreased performance in alternative environments. These results indicate that selection can be crucial in eliminating unnecessary genes during the early stages of adaptation to a specialized environment.
Zdroje
1. KuoCMoranNAOchmanH 2009 The consequences of genetic drift for bacterial genome complexity. Genome Res 19 1450 1454
2. LynchM 2006 Streamlining and simplification of microbial genome architecture. Annu Rev Microbiol 60 327 349
3. LawrenceJGOchmanH 1998 Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA 95 9413 9417
4. WelchRABurlandVPlunkettGRedfordPRoeschP 2002 Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 99 17020 17024
5. LanRReevesPR 2000 Intraspecies variation in bacterial genomes: the need for a species genome concept. Trends Microbiol 8 396 401
6. MoranNAMiraA 2001 The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol 2 research0054
7. MoranNA 2002 Microbial minimalism: Genome reduction in bacterial pathogens. Cell 108 583 586
8. OchmanHMoranNA 2001 Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292 1096 1099
9. McCutcheonJPMoranNA 2011 Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10 13 26
10. DufresneAGarczarekLPartenskyF 2005 Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol 6 R14
11. GiovannoniSJTrippHJGivanSPodarMVerginKL 2005 Genome streamlining in a cosmopolitan oceanic bacterium. Science 309 1242 1245
12. FrostLSLeplaeRSummersAOToussaintA 2005 Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3 722 732
13. CramerNKlockgetherJWrasmanKSchmidtMDavenportCF 2011 Microevolution of the major common Pseudomonas aeruginosa clones C and PA14 in cystic fibrosis lungs. Environ Microbiol 13 1690 1704
14. ErnstRKD'ArgenioDAIchikawaJKBangeraMGSelgradeS 2003 Genome mosaicism is conserved but not unique in Pseudomonas aeruginosa isolates from the airways of young children with cystic fibrosis. Environ Microbiol 5 1341 1349
15. SmithEEBuckleyDGWuZSaenphimmachakCHoffmanLR 2006 Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103 8487 8492
16. MaurelliATFernándezREBlochCARodeCKFasanoA 1998 “Black holes” and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc Natl Acad Sci USA 95 3943 3948
17. NilssonAKoskiniemiSErikssonSKugelbergEHintonJ 2005 Bacterial genome size reduction by experimental evolution. Proc Natl Acad Sci USA 102 12112 12116
18. BarrickJEYuDSYoonSHJeongHOhTK 2009 Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461 1243 1247
19. ZhongSKhodurskyADykhuizenDEDeanAM 2004 Evolutionary genomics of ecological specialization. Proc Natl Acad Sci USA 101 11719 11724
20. CooperVSSchneiderDBlotMLenskiRE 2001 Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J Bacteriol 183 2834 2841
21. DelmotteNKniefCChaffronSInnerebnerGRoschitzkiB 2009 Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci USA 106 16428 16433
22. LeeM-CChouH-HMarxCJ 2009 Asymmetric, bimodal trade-offs during adaptation of Methylobacterium to distinct growth substrates. Evolution 63 2816 2830
23. VuilleumierSChistoserdovaLLeeM-CBringelFLajusA 2009 Methylobacterium genome sequences: a reference blueprint to investigate microbial metabolism of c1 compounds from natural and industrial sources. PLoS ONE 4 e5584
24. ChouH-HChiuH-CDelaneyNFSegrèDMarxCJ 2011 Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science 332 1190 1192
25. MoranNAMcLaughlinHJSorekR 2009 The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323 379 382
26. NovichkovPSWolfYIDubchakIKooninEV 2009 Trends in prokaryotic evolution revealed by comparison of closely related bacterial and archaeal genomes. J Bacteriol 191 65 73
27. HarrisonPWLowerRPJKimNKDYoungJPW 2010 Introducing the bacterial ‘chromid’: not a chromosome, not a plasmid. Trends Microbiol 18 141 148
28. GourionBRossignolMVorholtJA 2006 A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth. Proc Natl Acad Sci USA 103 13186 13191
29. Notley-McRobbLKingTFerenciT 2002 rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J Bacteriol 184 806 811
30. FinkelSE 2006 Long-term survival during stationary phase: evolution and the GASP phenotype. Nat Rev Microbiol 4 113 120
31. MarxC 2008 Development of a broad-host-range sacB-based vector for unmarked allelic exchange. BMC Res Notes 1 1
32. OkuboYSkovranEGuoXSivamDLidstromME 2007 Implementation of microarrays for Methylobacterium extorquens AM1. Omics 11 325 340
33. MarxCJLidstromME 2002 Broad-host-range cre-lox system for antibiotic marker recycling in gram-negative bacteria. Biotechniques 33 1062 1067
34. VasiFTravisanoMLenskiRE 1994 Long-term experimental evolution in Escherichia coli. II. Changes in life-history traits during adaptation to a seasonal environment. Am Nat 144 432 456
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