Convergent evolution of metabolic roles in bacterial co-symbionts of insects.
A strictly host-dependent lifestyle has profound evolutionary consequences for bacterial genomes. Most prominent is a sometimes-dramatic amount of gene loss and genome reduction. Recently, highly reduced genomes from the co-resident intracellular symbionts of sharpshooters were shown to exhibit a striking level of metabolic interdependence. One symbiont, called Sulcia muelleri (Bacteroidetes), can produce eight of the 10 essential amino acids, despite having a genome of only 245 kb. The other, Baumannia cicadellinicola (gamma-Proteobacteria), can produce the remaining two essential amino acids as well as many vitamins. Cicadas also contain the symbiont Sulcia, but lack Baumannia and instead contain the co-resident symbiont Hodgkinia cicadicola (alpha-Proteobacteria). Here we report that, despite at least 200 million years of divergence, the two Sulcia genomes have nearly identical gene content and gene order. Additionally, we show that despite being phylogenetically distant and drastically different in genome size and architecture, Hodgkinia and Baumannia have converged on gene sets conferring similar capabilities for essential amino acid biosynthesis, in both cases precisely complementary to the pathways conserved in Sulcia. In contrast, they have completely divergent capabilities for vitamin biosynthesis. Despite having the smallest gene set known in bacteria, Hodgkinia devotes at least 7% of its proteome to cobalamin (vitamin B(12)) biosynthesis, a significant metabolic burden. The presence of these genes can be explained by Hodgkinia's retention of the cobalamin-dependent version of methionine synthase instead of the cobalamin-independent version found in Baumannia, a situation that necessitates retention of cobalamin biosynthetic capabilities to make the essential amino acid methionine.
McCutcheon
John P
JP
Center for Insect Science, University of Arizona, Tucson, AZ 85721, USA. jmccutch@email.arizona.edu
McDonald
Bradon R
BR
Moran
Nancy A
NA
D020561:Alphaproteobacteria / Q000235:genetics* / Q000378:metabolism; D000596:Amino Acids / Q000096:biosynthesis; D000818:Animals; D001483:Base Sequence; D004734:Energy Metabolism / Q000235:genetics*; D019143:Evolution, Molecular; D041965:Flavobacteriaceae / Q000235:genetics* / Q000378:metabolism; D020563:Gammaproteobacteria / Q000235:genetics* / Q000378:metabolism; D023061:Gene Order; D006430:Hemiptera / Q000382:microbiology*; D008969:Molecular Sequence Data; D040901:Proteomics; D016415:Sequence Alignment; D017422:Sequence Analysis, DNA; D013559:Symbiosis; D014805:Vitamin B 12 / Q000096:biosynthesis
D000596:Amino Acids; D014805:Vitamin B 12
Appl Environ Microbiol. 2005 Dec;71(12):8802-10
16332876
Proc Natl Acad Sci U S A. 1997 Oct 28;94(22):11819-26
9342321
Annu Rev Entomol. 2004;49:243-70
14651464
Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W609-12
16845082
Proc Natl Acad Sci U S A. 2003 Jan 21;100(2):581-6
12522265
Genome Res. 2005 Aug;15(8):1023-33
16077009
Science. 2002 Jun 28;296(5577):2376-9
12089438
Nucleic Acids Res. 2002 Jun 1;30(11):2478-83
12034836
Nature. 2002 Aug 22;418(6900):865-9
12192407
Nat Prod Rep. 2002 Aug;19(4):390-412
12195810
Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9388-93
12886019
Science. 1995 Jul 28;269(5223):496-512
7542800
J Biol Chem. 2003 Oct 17;278(42):41148-59
12869542
BMC Evol Biol. 2007 Oct 01;7:181
17908294
Science. 1999 Mar 5;283(5407):1476-81
10066161
Cell Mol Life Sci. 2000 Dec;57(13-14):1880-93
11215515
J Bacteriol. 1995 Nov;177(22):6371-80
7592411
Nature. 2005 Feb 3;433(7025):537-41
15690044
BMC Genomics. 2009 Feb 10;10:78
19208259
Biol Rev Camb Philos Soc. 1989 Nov;64(4):409-34
2696562
Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19392-7
18048332
Mol Biol Evol. 2007 Aug;24(8):1586-91
17483113
PLoS Biol. 2006 Jun;4(6):e188
16729848
Mol Phylogenet Evol. 2003 Dec;29(3):380-95
14615181
Trends Genet. 2003 Apr;19(4):176-80
12683967
Annu Rev Microbiol. 1996;50:137-81
8905078
Science. 2006 Oct 13;314(5797):312-3
17038625
Annu Rev Genet. 2008;42:165-90
18983256
PLoS Genet. 2009 Jul;5(7):e1000565
19609354
Nature. 2000 Sep 7;407(6800):81-6
10993077
Science. 2006 Oct 13;314(5797):267
17038615
Arthropod Struct Dev. 2003 Oct;32(2-3):189-99
18089004
Science. 2005 Mar 25;307(5717):1969-72
15790858
Nature. 2005 Nov 3;438(7064):90-3
16267554
Nucleic Acids Res. 2005 Jan 20;33(2):511-8
15661851