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Structure of Evolving Populations of Saccharomyces Cerevisiae

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Structure of Evolving Populations of Saccharomyces Cerevisiae Proc. Natl. Acad. Sci. USA Vol. 83, pp. 7124-7127, September 1986 Population Biology Structure of evolving populations of Saccharomyces cerevisiae: Adaptive changes are frequently associated with sequence alterations involving mobile elements belonging to the Ty family (continuous culture/transposable elements/population genetics) JULIAN ADAMS* AND PAUL W. OELLERt Division of Biological Sciences, University of Michigan, Ann Arbor, MI 48109 Communicated by R. W. Allard, May 15, 1986 ABSTRACT Haploid a and diploid a/a and a/a popula- chemostats and maintained in minimal medium (14) at 30'C in tions of Saccharomyces cerevisawe evolving in laboratory envi- culture vessels of sizes ranging between 150 and 200 ml. ronments for up to 300 generations were analyzed for sequence Glucose was added as a carbon source at a concentration of rearrangements associated with the Ty family of transposable 0.08% (wt/vol). At this concentration glucose is the substrate elements. Ih contrast to results with Escherichia coli, evolving limiting growth (14). Dilution rates in the chemostats were populations of yeast exhibit a high frequency of sequence -0.2 hr-'. To detect the occurrence and selection ofadaptive rearrangements associated with mobile genetic elements. In clones, canavanine (haploid strain) or cycloheximide (dip- particular, adaptive shifts in these populations are often loids) resistance was monitored every 12-24 hr. For each associated with such sequence rearrangements. The results are sample, an aliquot of cells was frozen in 15% glycerol at most compatible with the explanation that there is direct -70'C for later analysis. The adaptive clones were identified selection for some ofthe sequence rearrangements. In addition, by fluctuations in the frequency of canavanine or cyclohex- the pattern of changes suggests that the structure of evolving imide resistance. Details of the rationale involved and of the microorganism populations may be more complex than expect- procedures and defined media used have been described ed. (14-16). DNA Manipulations and Hybridization Procedures. Cells Mobile genetic elements have now been identified in a wide were streaked from the freezer onto minimal medium with variety'of species (see refs. 1 and 2 and references therein). 0.08% (wt/vol) glucose (15) at 30'C, and five colonies were Although an evolutionary significance for such elements has then picked and grown in YEPD liquid medium (13) overnight frequently been postulated (see refs. 3 and 4 and references at 30'C. About 5 x 108 cells were harvested while the cultures therein), direct evidence for this has been hard to obtain. In were still in logarithmic phase and the DNA was isolated as particular, in asexual populations it is difficult to distinguish described (17). Ten micrograms ofDNA was digested with 30 between direct selective advantage of the transposition units of EcoRI (Boehringer Mannheim) or 25 units of Sal I property and selection of another characteristic ("hitchhik- (Boehringer Mannheim) for 12-16 hr and then the fragments ing"; ref. 5). Chao et al. (6) were able to show a direct were separated by electrophoresis on 0.7% 30-cm agarose selective advantage for TnJO transposition, but only to a "submarine" gels at 40 mA in TBE buffer (0.089 M Tris specific locus in the genome mapped at 71 minutes (7). A borate/0.089 M boric acid/0.002 M EDTA, pH 7.8; ref. 18) series ofextensive studies by Hartl and his group (8-10) were for 1900 V hr-1. The DNA was then transferred and immo- unable to show a selective advantage associated with trans- bilized on nitrocellulose filters (Schleicher & Schuell, BA85), position of TnS, though presence of this element apparently using the method of Southern (19), and hybridized with increases growth rate. In this communication we report that pJA224 plasmid DNA labeled by nick-translation with adaptive shifts in evolving populations of the yeast Sac- [a-3P]ATP (Amersham) to a specific activity of 6 x 106 charomyces cerevisiae are frequently accompanied by se- cpm/,ug of DNA, using the kit supplied by Bethesda Re- quence alterations involving the mobile elements belonging search Laboratories. pJA224 is pBR322:TyEcoRI/Sal I ob- to the Ty family (11, 12), and there is no apparent unique tained from C. Paquin and contains the 1.25-kilobase (kb) target site. The patterns of sequence alteration in these EcoRI-Sal I fragment of the TyJ element inserted in ADH2- populations are most easily explained by assuming that gc (formerly ADH3-8c; ref. 20) in place of the 0.65-kb sequence alterations bossess a direct selective advantage and EcoRI-Sal I fragment in pBR322 (21). The close similarity of are responsible for 30-50%'of the adaptive changes seen. In the hybridization spectra obtained by using this probe to addition, the patterns of sequence alteration provide impor- those obtained for the closely related strain S288C (13), using tant insight into the structure of evolving populations of an independently constructed probe (22), confirms the spec- microorganisms. ificity of our probe for Ty sequences. The lengths of the restriction fragments were determined by comparison with MATERIALS AND METHODS comigrating X DNA cleaved with HindIII (Bethesda Re- search Laboratories). Strains, Media, and Growth Conditions. Populations were inoculated with either the a haploid strain CP1AB-1A, the a/a diploid strain CP1AB, or the a/a diploid strain CP1AB- RESULTS 1AA. The genotypes of these strains have been described Haploid a and diploid a/a and a/a populations of S. cerevi- (13). They are all isogeneic to each other except for the siae, initiated from single clones, were grown in glucose- mnating type locus. Continuous cultures were operated as Abbreviation: kb, kilobase(s). The publication costs of this article were defrayed in part by page charge "Present address: Department of Genetics, Washington University, payment. This article must therefore be hereby marked "advertisement" St. Louis, MO 63110. in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 7124 Population Biology: Adams and Oeller Proc. Natl. Acad. Sci. USA 83 (1986) 7125 limited continuous cultures for up to 300 generations. Pop- our strains were derived (13). The spectra are quite remark- ulation sizes were large, on the order of4-5 x 109, and tended able as they show differences accompanying the appearance to be higher for the haploid than for the diploid populations of many of the adaptive clones. In some samples, some ofthe (14). Since evolving populations of yeast, grown under our bands, especially in the larger size classes, are darker than conditions, reproduce exclusively asexually, they may be others, suggesting two comigrating DNA fragments contain- regarded as a series of clones over time. Within each clone ing copies of Ty elements. To determine if there were any the frequency of a neutral or quasineutral mutation will further sequence rearrangements undetected by these hy- increase due to recurrent mutation, such that its frequency bridization spectra, DNA preparations from the same sam- will be directly proportional to the time elapsed since the ples of the a haploid population and the a/a population were occurrence and predominance of the clone. Thus, during cleaved with a second restriction enzyme, Sal I, and hybrid- replacement of one clone by another, the frequency of the ization spectra were obtained as before. The majority of neutral mutation will necessarily decrease, due to the lower differences revealed by the EcoRI digests is also revealed by frequency of the neutral mutation in the newly predominating the Sal I digests, as expected for sequence rearrangements clone. The occurrence of adaptive shifts was monitored by involving the Ty elements (results not shown). However, in following the dynamics of the fluctuations of canavanine one case a sequence rearrangement undetected with an resistance in the case of the haploid population and cyclo- EcoRI digest was detected with a Sal I digest. In particular, heximide resistance in the case of the diploid populations. the Sal I hybridization spectrum for the sample isolated after Canavanine resistance is neutral under our conditions and the fourth adaptive shift in the a haploid population revealed there is weak selection against cycloheximide resistance (14). the occurrence of sequence rearrangement, whereas none These are shown in figures 2 and 3 of ref. 14 for the haploid was detected with EcoRI-cleaved DNA. Thus, the hybrid- a population and the a/a diploid population and in figure 1 of ization spectra shown in Fig. 1 may underestimate the true ref. 23 for the diploid a/a population. Further details of the number of rearrangement events. procedures and rationale involved are also presented in these Hybridization spectra obtained from the same samples, papers. Four adaptive changes were identified as having using a probe for yeast sequences with no homology to the Ty occurred in the haploid population, six in the a/a population, family of elements, showed no such differences (data not and seven in the a/a population (14, 23). To detect movement shown), confirming that non-Ty sequences do not show of the Ty elements, restriction endonuclease-cleaved DNA similar changes. Although we cannot rule out the possibility preparations from samples taken after each adaptive shift that a fraction of the differences between the hybridization were hybridized to a probe for the Ty family of elements spectra is the result of the mutational loss or gain of a following the method of Southern (19). This probe consisted restriction site, it is extremely unlikely that more than a very of a pBR322-derived plasmid containing the EcoRI-Sal I small minority of changes can be explained in this way, given fragment isolated from a TyJ element (20). This fragment the concordance between the results for the EcoRI and Sal I hybridizes to TyJ and Ty2 elements but not to delta se- digests, the expected frequency of actual and potential quences.
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