Transcription, translation, and the evolution of specialists and generalists.
We used DNA microarrays to measure transcription and iTRAQ 2D liquid chromatography-mass spectrometry/mass spectrometry (a mass-tag labeling proteomic technique) to measure protein expression in 14 strains of Escherichia coli adapted for hundreds of generations to growth-limiting concentrations of either lactulose, methylgalactoside, or a 72:28 mixture of the two. The two ancestors, TD2 and TD10, differ only in their lac operons and have similar transcription and protein expression profiles. Changes in transcription and protein expression are observed at 30-250 genes depending on the evolved strain. Lactulose specialists carry duplications of the lac operon and show increased transcription and translation at lac. Methylgalactoside specialists are galS(-) and so constitutively transcribe and translate mgl, which encodes a transporter of methylgalactoside. However, there are two strains that carry lac duplications, are galS(-), and show increased transcription and translation at both operons. One is a generalist, the other a lactulose specialist. The generalist fails to sweep to fixation because its lac(+), galS(+) competitor expresses the csg adhesin and sticks to the chemostat wall, thereby preventing complete washout. Transcription and translation are sometimes decoupled. Lactulose-adapted strains show increased protein expression at fru, a fructose transporter, without evidence of increased transcription. This suggests that fructose, produced by the action of beta-galactosidase on lactulose, may leach from cells before being recouped. Reduced expression, at "late" flagella genes and the constitutive gat operon, is an adaptation to starvation. A comparison with two other long-term evolution experiments suggests that certain aspects of adaptation are predictable, some are characteristic of an experimental system, whereas others seem erratic.
Zhong
Shaobin
S
Department of Plant Pathology, North Dakota State University, North Dakota, USA.
Miller
Stephen P
SP
Dykhuizen
Daniel E
DE
Dean
Antony M
AM
D000595:Amino Acid Sequence; D000704:Analysis of Variance; D001426:Bacterial Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D005075:Biological Evolution; D016000:Cluster Analysis; D004926:Escherichia coli / Q000145:classification* / Q000187:drug effects / Q000235:genetics*; D018628:Gene Dosage / Q000187:drug effects; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial / Q000187:drug effects; D005798:Genes, Bacterial / Q000235:genetics; D007553:Isotope Labeling; D007792:Lactulose / Q000494:pharmacology; D008756:Methylgalactosides / Q000494:pharmacology; D008969:Molecular Sequence Data; D009068:Movement / Q000187:drug effects; D009876:Operon / Q000235:genetics; D010455:Peptides / Q000737:chemistry; D010802:Phylogeny; D014176:Protein Biosynthesis / Q000187:drug effects / Q000235:genetics*; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D015203:Reproducibility of Results; D014158:Transcription, Genetic / Q000187:drug effects; D001616:beta-Galactosidase / Q000737:chemistry / Q000235:genetics / Q000378:metabolism
D001426:Bacterial Proteins; D008756:Methylgalactosides; D010455:Peptides; D012333:RNA, Messenger; D007792:Lactulose; D001616:beta-Galactosidase
Nat Rev Genet. 2003 Jun;4(6):457-69
12776215
J Bacteriol. 2001 May;183(9):2834-41
11292803
PLoS Genet. 2008 Aug 22;4(8):e1000163
18725932
Environ Microbiol. 1999 Feb;1(1):45-52
11207717
Mol Microbiol. 2005 Jul;57(1):1-8
15948944
Mol Ecol. 2008 Apr;17(7):1850-70
18312278
Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):1072-7
12538876
Proc Natl Acad Sci U S A. 2007 May 15;104 Suppl 1:8649-54
17494741
Genetics. 1989 Sep;123(1):19-28
2680755
Genetics. 1963 Feb;48:157-69
13954911
Physiol Biochem Zool. 2005 May-Jun;78(3):299-315
15887077
Proc Natl Acad Sci U S A. 1999 Aug 17;96(17):9721-6
10449761
Microbiology (Reading). 2008 Sep;154(Pt 9):2887-2895
18757823
Genetics. 2008 Feb;178(2):1049-60
18245349
J Biol Chem. 2003 Nov 21;278(47):46446-51
12963713
Cold Spring Harb Symp Quant Biol. 1961;26:239-45
14480575
Biochim Biophys Acta. 1962 Jan 22;55:152-63
14448925
Mol Microbiol. 1995 Nov;18(4):661-70
8817489
Mol Biol Evol. 2008 Jan;25(1):101-10
17998255
Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12170-5
11027315
Genetics. 1989 Nov;123(3):441-54
2513251
Evolution. 1993 Feb;47(1):1-12
28568084
Nature. 2000 Oct 12;407(6805):736-9
11048718
Nature. 1998 Jul 2;394(6688):69-72
9665128
Proc Natl Acad Sci U S A. 2004 Aug 10;101(32):11719-24
15289609
Genetics. 1995 Jan;139(1):19-33
7705623
J Bacteriol. 1994 Aug;176(16):5101-7
8051023
Genome Biol. 2003;4(9):117
12952525
Mol Cell Proteomics. 2004 Dec;3(12):1154-69
15385600
Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8
9843981
Mol Cell Proteomics. 2002 Apr;1(4):323-33
12096114
Adv Microb Physiol. 2008;53:169-229
17707145
Genetics. 2004 Aug;167(4):2015-26
15342537
Crit Rev Biochem Mol Biol. 2005 Mar-Apr;40(2):93-113
15814430
Mol Biol Evol. 1998 Jul;15(7):789-97
9656481
Mol Microbiol. 1996 May;20(3):467-73
8736526
Proteomics. 2005 Oct;5(15):4012-24
16130168
Microbiol Rev. 1985 Sep;49(3):270-97
3930934
Methods Mol Biol. 2003;224:61-78
12710666
Genetics. 2008 Mar;178(3):1653-60
18245823
Proc Natl Acad Sci U S A. 2007 Oct 23;104(43):17004-9
17942681
Nucleic Acids Res. 2006 Jan 05;34(1):1-9
16397293
Genetics. 1991 May;128(1):23-7
1829427
Genetics. 1994 Aug;137(4):903-17
7982572
RNA. 2008 Sep;14(9):1907-17
18658123
Annu Rev Genet. 1992;26:131-58
1482109
PLoS One. 2008 Jun 11;3(6):e2397
18545680
Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9232-7
12878731
Microbiology (Reading). 2005 Jul;151(Pt 7):2487-2497
16000739
Heredity (Edinb). 2008 May;100(5):471-7
18449959
Genetics. 2002 Sep;162(1):485-99
12242256
Nature. 2006 Mar 9;440(7081):242-5
16525476
Trends Microbiol. 2003 Oct;11(10):457-61
14557028
J Exp Bot. 2006;57(7):1501-8
16574745
Proc Biol Sci. 2003 Aug 7;270(1524):1645-50
12908987
Genome Biol. 2008 Apr 10;9(4):R72
18402659