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Population Dynamics of a Lac- Strain of Escherichia Coli During Selection for Lactose Utilization

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Population Dynamics of a Lac- Strain of Escherichia Coli During Selection for Lactose Utilization Copyright 0 1994 by the Genetics Society of America Population Dynamics of a Lac- Strain of Escherichia coli During Selection for Lactose Utilization Patricia L. Foster Department of Environmental Health, Boston University School of Public Health, Boston University School of Medicine, Boston, Massachusetts 021 18 Manuscript received February 25, 1994 Accepted for publication June 18, 1994 ABSTRACT During selectionfor lactose utilization,Lac' revertants of FC40, a Lac- strainof Escherichia coli, appear at a high rate. Yet, no Lac' revertants appear in the absence of lactose, or in its presenceif the cells have another, unfulfilled requirement for growth. This study investigatesmore fully the population dynamics of FC40 when incubated in the absence of a carbon source or when undergoing selection for lactose utilization. In the absence of a carbon source, the viable cell numbers do not change over 6 days. When incubated in liquid lactose medium, Lac- cells do not undergo any measurable increase innumbers or in turbidity for at least 2 days. When FC40 is plated on lactose minimum medium in the presence of scavenger cells,the upper limit to the amount of growth of Lac- cells during 5 days is one doubling, and there is no evidence for turnover (i.e., a balance between growthand death).The presence of a minority population that could form microcolonies was not detected. The implications of these results, plus the fact that the appearance of Lac' revertants during lactose selection is nearly constant with time, are discussed in reference to several models that have been postulated to account for adaptive mutations. T is generally believed that all spontaneous mutations had another, unfulfilled growth requirement (CAIRNS I arise at random as a result of errors made during and FOSTER1991). normal DNA replication. However, an increasing body The fact that FC40 produces far more revertants after of evidence suggests that spontaneous mutations can plating than during priorgrowth allowedus to study the also arise among populations of cells subjected to nu- requirements for post-plating mutation, and also to dis- tritional deprivation (reviewed in FOSTER1993). Further- miss relatively easilycertain trivial explanations for our more, in some cases the process appears to be "adaptive" results. Such explanations fall into two main classes: (1) in the sense that the only mutations that arise are those deviations from the classical Luria-Delbriickdistribution that provide a growth advantage to the cell (CAIRNS et al. obtained from a fluctuation test can be due to depar- 1988; HALL 1990; CAIRNSand FOSTER1991; STEELEand tures from the assumptions about cell growth and mu- JINKS-ROBERTSON1992). tation thatunderlie the distribution (TESSMAN1988; In previous publications (CAIRNSand FOSTER1991; CHARLESWORTHet al. 1988; LENSKIet al. 1989; STEWART FOSTERand CAIRNS1992) we described a case ofadaptive et al. 1990; SARKAR 1991); (2) mutations that arise during mutation in a strain of Escherichia coli, FC40, that can- selection could be the result of growth of non-mutant not metabolize lactose because of a frameshift mutation cells on the selective plates (PARTRIDGEand MORGAN affecting the lac2 gene. Fluctuation tests showed that 1988; LENSKIet al. 1988; LENSKIand MITTLER1993a). many ofthe Lac' mutants that appearedearly after FC40 The first explanation is unlikely to be importantwith was plated onto minimum lactose plates had the clonal FC40. STEWARTet al. (1990) modeled several factors that distribution expected if the mutations givingrise to might produce deviations from the Luria-Delbruck dis- them occurred during the nonselective growth of the tribution toward the Poisson, namely poor growth of cultures priorto plating (LURIA andDELBR~CK 1943; LEA mutant cells during nonselective growth, poor plating and COULSON1949). However, new Lac' colonies con- efficiencyof mutants, and a generation-independent tinued to appear at a constant rate and these had the component of the mutation rate. The firstof these Poisson distribution expected if mutations were occur- proved not to be true upon testing-Lac' revertants of ring on the selective plates. From these results we con- FC40 did not differ from Lac- cells in their growth rate cluded that 90-95% of the Lac+ revertants that were on glycerol (CAIRNS and FOSTER1991). Even the most detected during a week that the cells were on lactose extreme examples of poor plating efficiency considered plates were due to mutations that occurredafter the cells by STEWARTet al. (1990) did not produce a distribution had beenplated. These revertants did not arise if lactose in which 90% of the mutants appeared to be part of a was not present, norin the presence of lactose if the cells Poisson component. In addition, these models would Genetics 138: 253-261 (October, 1994) 254 P. L. Foster not account for the fact thatLac’ revertants continued For the experiment presented in Figure 3, the amount of to appear at a constant rate,and that the late appearing time required for starving cells to achievetwo generations was mutants had a Poisson distribution. The last hypothe- determined. A saturated culture of FC333 in minimum glyc- erol medium was incubated with shaking for a week. Every day sis, thatthere is a timedependentbut generation- an aliquot was diluted 1:lO into fresh minimum glycerolme- independent component of mutation, is indistinguish- dium, and growth was monitored with a Klett colorimeter. The able from ours. lag period increased by about 15 min each day, but the sub- We had also considered it improbable that the Lac’ sequent growth rates were the same. revertants of FC40 that arose after platingwere due to In the experiment presented in Figure 4, plates were re- spread by adding 50 pl of saline to the surface and spreading growth of Lac- cells on the plates. We would have de- with a glass spreader held stationary while the plates were spin- tected the 50-100-fold increase in the population that ning on a turntable. This technique was sufficient to disrupt would be necessary to produce the Lac’ mutants at preexisting Lac’ colonies of as few as four cells, which could the generation-dependent mutation rate (CAIRNS and be detected as colonies that subsequently appeared in a spiral pattern. 1991; FOSTER1993). However, it has been argued FOSTER The allelic status of rpoS was determined by the H,O, that the true amountof cell growth might be obscured “bubbling assay” described previously (ZAMBRANO et al. by the death of some of thecells, and that the surviving 1993). Briefly, a drop of H20, was placed on patches of cells cells, or a subpopulation of them, might have a high grown on LB plates and the degree of bubbling (indicating mutation rate (LENSKIand MITTLER1993a,b). Cell death catalase activity) compared to cells carrying rpoS+, rpoS819 and rpoS::kan alleles that were patched onto the same plates could also account for the failure to recover Lac’ mu- (all strains obtained from R. KOLTER). tants in the absence of selection for them (PARTRIDGE Statisticalmethods: Results are presented as means ? and MORGAN1988; LENSIUand MITTLER1993a,b). In this the standard error of the mean (SEM) , which was calculated as paper these and similar concerns are addressedby de- ( s2/n)where s2 is the variance. The 95% confidence intervals can be derived fromthe SEM by multiplying by 2 (large samples) tailing the population dynamics FC40of in the presence or by t with n - 1 d.f. (small samples) (ZUWAXIF 1970). To and absence of lactose. make more precise comparisons between means,the sampling data in Tables 1-3 and from CAIRNSand FOSTER(1991) were assumed to be normallydistributed with approximately equal MATERIALSAND METHODS variances, and used in one- or two-factor analysis of variance Bacterial strains and plasmids: All the strains used have a (ANOVAR). The error meansquare (= the residual vari- common parent, P9OC (COULONDREand MILLER1977). FC40 ance or the error variance) was then used as the variance in and the scavenger strain, FC29, havebeen previously described one- or two-tailed t tests to compare means. Thus, the 95% (CAIRNS and FOSTER1991). Briefly, FC40 isrifampicin-resistant confidence limits for the difference between two means is t X (Rif)and has an F’ carrying a lad-lacZ fusion with a + 1 base [s2/( n, + n,)] where s2 = the error mean square, n1 and n, pair frameshiftmutation, lacI33, in the lad coding sequence are for the means being compared, and t is taken with the (&OS and MILLER1981). FC29 is rifampicin-sensitive (Rip) degrees of freedom of the error mean square. and has anF’ carrying a deletion allele of 1acZ. FC281 is FC40 but rcfll7::Tn10; FC333is as FC40 but Rif and strepto- RESULTS mycin-resistant (Strep‘) and was derived from a spontaneous Strep‘ mutant of P9OC. All genetic manipulations used stand- FC40 cells neither grow nor die during lactose selec- ard techniques (MILLER1972). tion: The first question is can FC40 grow with lactose as Media: Bacteriawere cultivated as previously described a carbon source, i.e., how “leaky” is the lac allele? The (CAIRNS andFOSTER 1991). Liquid minimum medium or mini- mum plates were M9 (MILLER1972) with 20 pg/ml thiamine amount of @galactosidase produced by the mutant is and 0.1% lactose(Difco; filter-sterilized), 0.1 5% glycerol low, about 2.5 Miller units, compared to200-300 Miller (Sigma; filter-sterilized),or no carbon source. 0.001% gelatin units produced by a full Lac’ revertant. However, 2.5 was added to liquid minimum media.LB was as in MILLER (1972). units is not 0 (as measured, for example, in FC29, that Lactose MacConkey (Difco) plates were prepared according to has a deletion in ZacZ) . In addition, agar supplies some the manufacturer’s instructions. Antibiotic concentrations were: nutrients and both FC40 and FC29 will produce small 100 pg/ml rifampicin, 100 pg/ml streptomycin, 50 pg/ml car- benicillin, 10 pg/ml tetracycline in minimum medium and 20 colonies if plated at low density on minimum lactose pg/ml tetracycline in rich medium.
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