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Population Genetics of the Wild Yeast Saccharomyces Paradoxus

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Population Genetics of the Wild Yeast Saccharomyces Paradoxus Copyright 2004 by the Genetics Society of America Population Genetics of the Wild Yeast Saccharomyces paradoxus Louise J. Johnson,*,1 Vassiliki Koufopanou,* Matthew R. Goddard,† Richard Hetherington,* Stefanie M. Scha¨fer*,2 and Austin Burt* *Department of Biological Sciences and †NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot SL5 7PY, United Kingdom Manuscript received November 4, 2002 Accepted for publication September 22, 2003 ABSTRACT Saccharomyces paradoxus is the closest known relative of the well-known S. cerevisiae and an attractive model organism for population genetic and genomic studies. Here we characterize a set of 28 wild isolates from a 10-km2 sampling area in southern England. All 28 isolates are homothallic (capable of mating-type switching) and wild type with respect to nutrient requirements. Nine wild isolates and two lab strains of S. paradoxus were surveyed for sequence variation at six loci totaling 7 kb, and all 28 wild isolates were then genotyped at seven polymorphic loci. These data were used to calculate nucleotide diversity and number of segregating sites in S. paradoxus and to investigate geographic differentiation, population Extensive incompatibilities .%0.3ف structure, and linkage disequilibrium. Synonymous site diversity is between gene genealogies indicate frequent recombination between unlinked loci, but there is no evidence of recombination within genes. Some localized clonal growth is apparent. The frequency of outcrossing relative to inbreeding is estimated at 1.1% on the basis of heterozygosity. Thus, all three modes of reproduction known in the lab (clonal replication, inbreeding, and outcrossing) have been important in molding genetic variation in this species. ANY fields in biology have progressed by the con- are escaped domestics or otherwise greatly affected by M centrated study of a select group of model sys- human activity (Vaughan-Martini and Martini 1995; tems. In population and evolutionary genetics, only a Naumov et al. 1992a). This could greatly affect their few species such as Drosophila and humans have been population genetics, severely complicating interpreta- widely adopted, and it might make sense to consider tions and reducing the extent to which lessons learned what other taxa might best complement these. The yeast with this species are likely to be widely applicable. For Saccharomyces cerevisiae has a number of characteristics example, one survey of S. cerevisiae in wineries revealed that would seem to make it ideal (Zeyl 2000): (i) It is some surprising findings, including 31% of strains het- already a well-studied model system in biochemistry, cell erozygous for a lethal mutation and 23% heterozygous biology, classical genetics, and molecular biology; (ii) or homozygous for heterothallism, i.e., an inability to genomes can be precisely altered by homologous recom- undergo mating-type switching (Mortimer 2000). The bination; and (iii) long-term experiments with large association between Drosophila and humans has posed population sizes and sensitive fitness assays are readily similar problems (Andolfatto and Przeworski 2000; possible in the laboratory. These features suggest that Wall et al. 2002). one may be more likely to be able to investigate and One way to circumvent this problem would be to study interpret the functional significance of natural DNA a close relative that has the same advantages, but not sequence variation in this species than in any other the disadvantage. S. paradoxus is (along with S. cario- eukaryote. Moreover, it has a relatively small and gene- canus) the closest known relative of S. cerevisiae (God- rich genome, reducing the size of the problem to be dard and Burt 1999). The two species appear to be solved. However, there is a problem: S. cerevisiae has biochemically indistinguishable (Barnett et al. 1990), long been associated with humans, and in collecting have the same chromosome number, and appear to be strains it is difficult to determine to what extent they largely syntenic (Naumov et al. 1992b). Growth prefer- ences in the lab are the same as for S. cerevisiae, and genetic engineering by the same homologous gene re- placement methods used in S. cerevisiae is possible (E. Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. AJ515177– Louis, personal communication). Thus, many of the AJ515216, AJ515322–AJ515352, and AJ515430–AJ515449. advantages still apply. Moreover, it has been isolated 1Corresponding author: Institute of Genetics, University of Notting- from many natural locations worldwide (e.g., Sniegow- ham, Queens Medical Centre, Nottingham NG7 2UH, United King- dom. E-mail: [email protected] ski et al. 2002) and apparently has not been widely 2Present address: Department of Infectious Disease Epidemiology, domesticated. Gene flow between S. cerevisiae and S. Imperial College, London W2 1PG, United Kingdom. paradoxus is also unlikely; hybrids can be formed, but Genetics 166: 43–52 ( January 2004) 44 L. J. Johnson et al. are almost completely sterile (Naumov et al. 1997a). cerevisiae strains with substantial variability within each species. Overall DNA sequence divergence between the two spe- The initial collection of 344 bark scrapings yielded 28 isolates. Other strains: The Centraalbureau voor Schimmelcultures ف cies is thought to be 20% (Herbert et al. 1988), and (CBS) supplied CBS 432, the type strain of S. paradoxus, and synonymous site divergence at the loci studied here is the Danish lab strain CBS 5829, here referred to as “Type” .and “Danish,” respectively .%30ف In the laboratory, the life cycle of S. paradoxus is the Two S. paradoxus isolates from the Russian Far East (FE), same as that of S. cerevisiae (Herskowitz 1988). It nor- CBS 8436 and CBS 8444, were included for comparison. These isolates differ from European S. paradoxus at allozyme loci -synonymous site diver %5ف mally reproduces mitotically as a diploid, but when (Naumov et al. 1997b) and show starved of nitrogen undergoes meiosis and produces gence from the type strain of S. paradoxus at the six sequenced four haploid spores encapsulated in an ascus. There are loci. These strains, referred to herein as FE1 and FE2, respec- two mating types, and the spores usually mate within tively, were kindly provided by Edward Louis. All S. cerevisiae the ascus upon germination, but if this does not happen, sequence data were from the Yeast Genome Project (Goffeau et al. 1996). they are able to reproduce mitotically as haploids. Hap- Phenotypic assays: To isolate individual spores for pheno- loid cells are constitutively ready to mate and can out- typic assays, all wild isolates were grown on sporulation me- cross. However, haploid mitoses are associated with a dium for 4 days, and resultant asci were enzymatically digested sophisticated mechanism of mating-type switching, with (10 min in a 50-␮l solution of 10 mg/ml sulfanotase, 10 mg/ Њ the result that cells can also mate with their clonemates, ml lyticase at 25 ). Individual spores were removed with a Zeiss micromanipulator and incubated at 25Њ for 4 days on YPD producing an entirely homozygous diploid (“autodiploi- agar to allow colony growth. Colonies were replica plated to dization”). Thus, S. paradoxus may undergo two types minimal and sporulation media and after 3 days examined of self-fertilization: intra-ascus mating and autodiploidi- for growth or surveyed by microscopy for the presence of zation. For a review of ascomycete mating systems, see tetrads. The presence of tetrads was considered indicative Nelson (1996). of mating-type switching. All media were made according to Sherman (1991). In this article we describe a preliminary investigation Molecular methods: Nine wild isolates were chosen ran- into the genetics of a single population of S. paradoxus, domly for an initial survey of sequence variation. Total DNA focusing on quantifying levels of nucleotide variation was extracted (Sherman 1991) and diluted 100-fold for use and analyzing the pattern of variation to infer mating as a PCR template. Six genes involved in mate recognition system (and, to a lesser extent, dispersal). were amplified from the nine wild isolates and from the Type strain, Danish, FE1, and FE2 isolates. Details of genes and primers are given in Table 1. All 28 wild isolates were then genotyped at polymorphic sites by restriction at the MFA1 and MATERIALS AND METHODS AGA2 loci, using enzymes Tsp451 and AseI, respectively, and by sequencing fragments of MF␣1, SAG1, STE2, and STE3. Collections: S. paradoxus was isolated from the bark of oak Microsatellite locus: Twenty S. cerevisiae microsatellite trees (Quercus, mainly Quercus robur; Naumov et al. 1998) in primer pairs (Field and Wills 1998) were tested on S. para- ف Silwood Park and Windsor Great Park. Bark scrapings ( 1g) doxus. Of these only 3 gave a PCR product with S. paradoxus, were collected from 86 oak trees on each of two dates, with and 1 was found to be polymorphic, a variable-length repeat two scrapings on opposite sides of the tree on each date. in the TFA1 gene (chromosome XI in S. cerevisiae). The wild Scrapings were aseptically transferred to acidified malt me- isolates were genotyped at this locus by polyacrylamide gel dium [5% malt extract (Sigma, Dorset, UK), 0.4% lactic acid electrophoresis of radioactively end-labeled PCR products (Sigma) w/v] in loosely capped vials and shaken for 2 days (Sambrook et al. 1989). A representative of each mobility Њ at 30 . Many types of microbe were present in the medium so group was sequenced to determine the length of each allele. a selection procedure was incorporated to isolate S. paradoxus. Statistical analysis and software used: Nucleotide diversity Dilutions of the 48-hr culture were plated on acidified malt ␲ at synonymous and nonsynonymous sites, and synonymous and incubated for 24 hr at 30Њ. The resulting colony-forming site divergence, were calculated using DnaSP (Rozas and Rozas units were visually inspected and colonies looking like S.
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