title: Functional and evolutionary analysis of the genome of an obligate fungal symbiont.
abstract: Nutritional symbionts of insects include some of the most bizarre genomes studied to date, with extremely reduced size, biased base composition, and limited metabolic abilities. A monophyletic group of aphids within the subfamily Cerataphidinae have lost the bacterial symbiont common to all other Aphididae (Buchnera aphidicola), which have been replaced by a eukaryotic one, the yeast-like symbiont (YLS). As symbionts are expected to experience reduced effective population size (Ne) and largely clonal life cycles, we used this system as a model to test the hypothesis that chronically high levels of genetic drift will result in an increase in size of a eukaryotic genome. We sequenced the genome of the YLS of the aphid Cerataphis brasiliensis and observed elevated rates of protein sequence evolution and intron proliferation in YLS orthologs relative to those of its closest-sequenced relative, consistent with predictions. A moderate amount of repetitive DNA was found along with evidence of directed mutation to prevent proliferation of repetitive elements. Despite increased intron numbers, the overall genome structure appears not to have undergone massive expansion and is around 25 Mb in size. Compared with Buchnera, the YLS appears to have a much broader metabolic repertoire, though many gene families have been reduced in the YLS relative to related fungi. The patterns observed in the YLS genome suggest that its symbiotic lifestyle is permissive to intron proliferation and accelerated sequence evolution, though other factors appear to limit its overall genome expansion.
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Arizona, USA. kjvogel@uga.edu
authors.forename: Kevin J
authors.initials: KJ
authors.lastname: Vogel
authors.forename: Nancy A
authors.initials: NA
authors.lastname: Moran
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001042:Aphids / Q000235:genetics* / Q000502:physiology; D020635:Buchnera / Q000235:genetics; D019143:Evolution, Molecular; D040961:Genetic Drift; D016681:Genome, Fungal / Q000235:genetics*; D007438:Introns / Q000235:genetics; D010802:Phylogeny; D013559:Symbiosis; D015003:Yeasts / Q000235:genetics*
keywords: Cerataphidinae; effective population size; introns; repeat-induced point mutation; yeast-like symbiont
references.citation: Nucleic Acids Res. 1997 Mar 1;25(5):955-64
references.pmid: 9023104
references.citation: Proc Natl Acad Sci U S A. 2009 Sep 8;106(36):15394-9
references.pmid: 19706397
references.citation: Science. 2002 Jun 28;296(5577):2376-9
references.pmid: 12089438
references.citation: Genome Res. 2008 Dec;18(12):1979-90
references.pmid: 18757608
references.citation: J Insect Physiol. 2000 Jan;46(1):33-40
references.pmid: 12770256
references.citation: Syst Biol. 2010 May;59(3):307-21
references.pmid: 20525638
references.citation: Mol Biol Evol. 2006 Feb;23(2):450-68
references.pmid: 16280547
references.citation: Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2873-8
references.pmid: 8610134
references.citation: Trends Genet. 2001 Nov;17(11):615-8
references.pmid: 11672844
references.citation: Bioinformatics. 2009 Jul 15;25(14):1754-60
references.pmid: 19451168
references.citation: Curr Biol. 2011 Aug 23;21(16):1366-72
references.pmid: 21835622
references.citation: Genet Res. 1972 Feb;19(1):33-8
references.pmid: 5024712
references.citation: Nat Rev Microbiol. 2011 Nov 08;10(1):13-26
references.pmid: 22064560
references.citation: Genome Res. 2009 Aug;19(8):1450-4
references.pmid: 19502381
references.citation: Genetics. 2003 Dec;165(4):1651-60
references.pmid: 14704156
references.citation: BMC Bioinformatics. 2008 Nov 12;9:478
references.pmid: 19014496
references.citation: PLoS One. 2011;6(12):e28905
references.pmid: 22194947
references.citation: PLoS Biol. 2003 Oct;1(1):E21
references.pmid: 14551917
references.citation: Nucleic Acids Res. 2008 Jan;36(Database issue):D572-6
references.pmid: 17942425
references.citation: Science. 2007 Sep 7;317(5843):1400-2
references.pmid: 17823352
references.citation: Proc Natl Acad Sci U S A. 2011 Feb 15;108(7):2849-54
references.pmid: 21282658
references.citation: J Mol Evol. 2000 Jan;50(1):56-68
references.pmid: 10654260
references.citation: Mol Biol Evol. 2001 Jun;18(6):995-1000
references.pmid: 11371588
references.citation: Cytogenet Genome Res. 2005;110(1-4):462-7
references.pmid: 16093699
references.citation: Bioinformatics. 2005 Jun;21 Suppl 1:i351-8
references.pmid: 15961478
references.citation: Genome Res. 2004 May;14(5):988-95
references.pmid: 15123596
references.citation: Science. 2009 Nov 27;326(5957):1260-2
references.pmid: 19965475
references.citation: J Mol Evol. 1999 Jun;48(6):717-22
references.pmid: 10229576
references.citation: Proc Natl Acad Sci U S A. 2012 Dec 11;109(50):20655-60
references.pmid: 23185008
references.citation: Microbiol Mol Biol Rev. 1997 Mar;61(1):17-32
references.pmid: 9106362
references.citation: Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19392-7
references.pmid: 18048332
references.citation: Mol Biol Evol. 2007 Aug;24(8):1586-91
references.pmid: 17483113
references.citation: Biol Rev Camb Philos Soc. 1996 Feb;71(1):27-79
references.pmid: 8603120
references.citation: PLoS Biol. 2006 Jun;4(6):e188
references.pmid: 16729848
references.citation: Nucleic Acids Res. 2007 Jul;35(Web Server issue):W182-5
references.pmid: 17526522
references.citation: Proc Natl Acad Sci U S A. 2009 Dec 8;106(49):20818-23
references.pmid: 19926850
references.citation: Genome Biol Evol. 2009 Jun 27;1:145-52
references.pmid: 20333185
references.citation: Monogr Popul Biol. 1971;4:1-219
references.pmid: 5162676
references.citation: Appl Environ Microbiol. 2010 Jun;76(12):4076-9
references.pmid: 20418442
references.citation: Trends Genet. 2003 Apr;19(4):176-80
references.pmid: 12683967
references.citation: PLoS Genet. 2011 Nov;7(11):e1002357
references.pmid: 22102823
references.citation: Nature. 1973 Nov 9;246(5428):96-8
references.pmid: 4585855
references.citation: Proc Natl Acad Sci U S A. 2003 Jan 21;100(2):581-6
references.pmid: 12522265
references.citation: Genome Res. 2008 May;18(5):821-9
references.pmid: 18349386
references.citation: Microb Ecol. 2002 Aug;44(2):137-43
references.pmid: 12087426
references.citation: Genome Biol Evol. 2011;3:195-208
references.pmid: 21266540
references.citation: Annu Rev Genet. 1990;24:579-613
references.pmid: 2150906
references.citation: Proc Natl Acad Sci U S A. 2009 Jun 2;106(22):9063-8
references.pmid: 19451630
references.citation: J Bacteriol. 2011 Oct;193(19):5587-8
references.pmid: 21914892
references.citation: Insects. 2011 Sep 16;2(3):423-34
references.pmid: 26467737
references.citation: Genome Biol Evol. 2012;4(1):13-23
references.pmid: 22117086
references.citation: Bioinformatics. 2010 Feb 1;26(3):401-2
references.pmid: 19965881
references.citation: Trends Genet. 2001 Oct;17(10):589-96
references.pmid: 11585665
references.citation: Mutat Res. 1964 May;106:2-9
references.pmid: 14195748
references.citation: Annu Rev Entomol. 2010;55:247-66
references.pmid: 19728837
references.citation: Nature. 2010 Apr 15;464(7291):1033-8
references.pmid: 20348908
references.citation: Nature. 1953 Aug 1;172(4370):207
references.pmid: 13087162
references.citation: J Mol Evol. 2000 Sep;51(3):265-77
references.pmid: 11029071
references.citation: BMC Bioinformatics. 2004 Aug 19;5:113
references.pmid: 15318951
references.citation: Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14002-7
references.pmid: 12381784
references.citation: Nucleic Acids Res. 2012 Jan;40(Database issue):D290-301
references.pmid: 22127870
references.citation: Curr Opin Genet Dev. 2004 Dec;14(6):627-33
references.pmid: 15531157
references.citation: Bioinformatics. 2006 May 15;22(10):1269-71
references.pmid: 16543274
references.citation: PLoS Genet. 2009 Aug;5(8):e1000618
references.pmid: 19714214
references.citation: Genome Biol. 2011 Nov 23;12(11):R116
references.pmid: 22112802
references.citation: Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12944-8
references.pmid: 12235368
references.citation: PLoS Genet. 2011 Jan 06;7(1):e1001264
references.pmid: 21253567
references.citation: Science. 2003 Nov 21;302(5649):1401-4
references.pmid: 14631042
references.citation: PLoS Genet. 2009 Jul;5(7):e1000565
references.pmid: 19609354
references.citation: Nature. 2000 Sep 7;407(6800):81-6
references.pmid: 10993077
references.citation: Science. 2006 Oct 13;314(5797):267
references.pmid: 17038615
references.citation: Nature. 2010 Mar 18;464(7287):367-73
references.pmid: 20237561