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Saccharomyces paradoxus and Saccharomyces cerevisiae reside
on oak trees in New Zealand: evidence for migration from Europe
and interspecies hybrids
Hanyao Zhang, Aaron Skelton, Richard C. Gardner & Matthew R. Goddard
School of Biological Sciences, University of Auckland, Auckland, New Zealand

Correspondence: Matthew R. Goddard,
School of Biological Sciences, University of
Auckland, Private Bag 92019, Auckland
1142, New Zealand. Tel.: 164 9 3737 599;
fax: 164 9 3737 416; e-mail:
Received 10 June 2010; revised 11 July 2010;
accepted 27 August 2010.
Final version published online 24 September
Editor: Teun Boekhout
yeast; ecology; dispersal.

Saccharomyces cerevisiae and Saccharomyces paradoxus are used as model systems
for molecular, cell and evolutionary biology; yet we know comparatively little of
their ecology. One niche from which these species have been isolated is oak bark.
There are no reports of these species from oak in the Southern Hemisphere. We
describe the recovery of both S. cerevisiae and S. paradoxus from oak in New
Zealand (NZ), and provide evidence for introgression between the species. Genetic
inference shows that the oak S. cerevisiae are closely related to strains isolated from
NZ and Australian vineyards, but that the S. paradoxus strains are very closely
related to European isolates. This discovery is surprising as the current model of
S. paradoxus biogeography suggests that global dispersal is rare. We test one idea to
explain how members of the European S. paradoxus population might come to
be in NZ: they were transported here along with acorns brought by migrants 
200 years ago. We show that S. paradoxus is associated with acorns and thus
provide a potential mechanism for the unwitting global dispersal of S. paradoxus
by humans.


Humans have a long and close association with the microbial agents responsible for the production of wine, beer and
bread (Pretorius, 2000; McGovern et al., 2004; Piskur et al.,
2006; Goddard, 2008). Almost 150 years ago, Pasteur
showed that fermentation is a biological process conducted
by microorganisms including Saccharomyces cerevisiae, and
subsequently, S. cerevisiae’s physiology, genetics and molecular biology have been scrutinized. The experimental
tractability of S. cerevisiae, and the fact that it is a eukaryote
capable of sexual reproduction, positioned it as an ideal
model for genetics and cell biology (Dujon, 1996; Landry
et al., 2006). In summary this single-celled fungus has been
used to considerably advance our biological understanding
in these areas. In addition to the wealth of molecular
information, the ease with which S. cerevisiae populations
may be stored, propagated and assayed has meant that it is
now also an upcoming model used to experimentally test
fundamental questions in population biology, ecology and
evolution (Zeyl, 2000; Greig, 2007; Replansky et al., 2008).
FEMS Yeast Res 10 (2010) 941–947

Saccharomyces cerevisiae was originally thought to be a
purely ‘domesticated’ species not found outside of a close
association with humans (Mortimer & Polsinelli, 1999; Fay
& Benavides, 2005). Thus, one potential criticism is that
S. cerevisiae might not be a good model to provide insights
into the processes operating in natural populations (Johnson et al., 2004). In an attempt to circumvent this issue,
research was focused on S. cerevisiae’s closest relative, which
has been isolated from oak trees, Saccharomyces paradoxus.
Saccharomyces cerevisiae is now known to exist in natural
populations along with S. paradoxus (Sniegowski et al.,
2002; Sampaio & Goncalves, 2008), and together, these
species are being used increasingly to test more general
ecological and evolutionary hypotheses (Greig et al., 1998;
Zeyl, 2000; Greig & Travisano, 2004; Goddard et al., 2005;
Goddard, 2008) and estimate parameters in natural populations (Johnson et al., 2004; Sweeney et al., 2004; Koufopanou et al., 2006; Ruderfer et al., 2006; Kuehne et al., 2007;
Legras et al., 2007; Reuter et al., 2007; Replansky et al., 2008;
Tsai et al., 2008; Liti et al., 2009; Schacherer et al., 2009;
Goddard et al., 2010). Although there are a growing number
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of studies in this area, the ecology of Saccharomyces species is
still relatively poorly understood compared with our molecular understanding of these species.
Population genetic analyses, including recent studies that
have compared whole-genome data for 30–60 strains, show
that there are certain lineages of S. cerevisiae that appear to
be closely associated with wine and fermentation, but that a
general diversity of S. cerevisiae exists in a number of natural
populations isolated from other niches (Fay & Benavides,
2005; Legras et al., 2007; Liti et al., 2009; Schacherer et al.,
2009). There is a reasonable amount of gene flow between
these S. cerevisiae populations on a global scale, which may
well be facilitated by interaction with humans, and the
transport of vines and other wine-related paraphernalia
(Legras et al., 2007; Liti et al., 2009; Goddard et al., 2010).
In general, S. cerevisiae is well-adapted to invade fruit niches
via ecosystem engineering, a trait that evolved long before
humans learned to harness it (Wolfe & Shields, 1997; Piskur
et al., 2006; Goddard, 2008). While S. cerevisiae has been
isolated from a range of fermenting environments, the other
main niche from which it has been isolated is the bark of,
and soil associated with, oak (Quercus sp.) trees (Sniegowski
et al., 2002; Sampaio & Goncalves, 2008).
Saccharomyces paradoxus on the other hand is rarely
isolated from fruits/ferments, which is curious, given that it
is also capable of fermentation (i.e. it is Crabtree positive).
However, S. paradoxus has also been isolated from oak bark,
sometimes contemporaneously with S. cerevisiae and other
Saccharomyces sensu stricto species (Sniegowski et al., 2002;
Sampaio & Goncalves, 2008). Recent work and wholegenome population genetic analyses show that in contrast to
S. cerevisiae, S. paradoxus’ population structure appears to be
well-described by geographic distance (Koufopanou et al.,
2006; Liti et al., 2006, 2009). Within continents, S. paradoxus
populations appear to be reasonably well-mixed, but there is a
strong genetic demarcation between strains from Europe,
America and the Far East, implying that global dispersal/gene
flow is a much weaker force for S. paradoxus compared with
S. cerevisiae (Liti et al., 2009). However, this biogeography
model is not absolute as there is one inference of an ancient
S. paradoxus intercontinental dispersal from Eurasia to North
America (Kuehne et al., 2007). In general, S. paradoxus is a
species that is perceived not to be associated with humans.
Goddard et al. (2010) recently described a genetically
distinct natural population of S. cerevisiae in New Zealand
(NZ) that appears to be dispersed on local scales at least by
insects. There is also evidence that NZ contains migrant S.
cerevisiae from Europe vectored unwittingly by humans in
oak barrels. Thus far, there are no reports of S. cerevisiae or
S. paradoxus associated with oak in the Southern hemisphere. Oak trees are not native to NZ, but were brought
here by European settlers 200 years ago and thus potentially provide a niche in which Saccharomyces yeasts may
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H. Zhang et al.

reside. Here, we test for the presence of Saccharomyces
species on oak bark in NZ.

Materials and methods
A total of 42 Quercus robur and one Quercus palustris trees
were sampled during December 2008 in the grounds of the
University of Auckland and the adjacent Alten reserve in
central Auckland (centred around 361500 59.5700 S
1741460 15.9000 E). Each tree was sampled on the North and
South side at 0.5 and 1.5 m from the ground for a total of 172
samples. Roughly 1 cm3 of bark and cambium were sampled
by hammering a sterile cork borer into the bark at each
position. In addition, surface bark samples were taken for
visualization by scanning electron microscopy (SEM). A total
of 18 acorns from three of these Q. robur trees were also
sampled. Samples were transferred to the laboratory, where a
selection procedure (comprising SelMed: 1% yeast extract, 2%
peptone, 10% glucose and 10% ethanol) designed to enrich
for Saccharomyces yeasts was applied to each sample (see
Serjeant et al., 2008 for details); it must be noted that the 30 1C
incubation step will likely select against the more cryotolerant
Saccharomyces species (Saccharomyces bayanus, Saccharomyces
kudriavzevii and Saccharomyces arboricolus) (Sampaio &
Goncalves, 2008). After a 16-day incubation period interspersed by one transfer, the samples were removed and 102
and 103 dilutions were spread onto YPD (1% yeast extract,
2% peptone, 2% glucose) and incubated for 3 days at 30 1C.
Where present, up to six yeast-like colonies were selected from
each sample and stored at  80 1C in 15% v/v glycerol.
DNA was extracted from cultures of each isolate using a
procedure that used a 5% Chelex solution. Following Goddard
(2008), the ITS1–5.8S-ITS2 (internal transcribed spacer, ITS)
regions of these colonies were initially analysed by restriction
fragment length polymorphism (RFLP) (with the restriction
endonucleases HaeIII and a more detailed analysis was undertaken for Saccharomyces sensu stricto colonies using MspI)
and then by Sanger sequencing in order to identify the
isolates to the species level. The divergent domain 1 and 2
(D1/D2) of the 26S rRNA gene was also sequenced for one
representative from each class indicated by the RFLP analyses.
Six other loci were amplified and sequenced to further
characterize the isolates. Four pairs of primers reported in
Johnson et al. (2004) were used, three of which specifically
amplify the S. paradoxus MF-a, STE2 and SAG1 loci, while
one primer pair amplifies both the S. paradoxus and the S.
cerevisiae MF-a locus. Two other primer pairs were specific
to the S. cerevisiae PAD1 and IAH1 loci. In addition, those
isolates that were diagnosed as S. cerevisiae (in whole or part
by our analyses) were typed at 10 variable repeat regions and
the MAT locus as described in Richards et al. (2009) in order
to ascertain their relatedness to other S. cerevisiae isolates
from NZ and abroad.
FEMS Yeast Res 10 (2010) 941–947


New Zealand Saccharomyces ecology

Fig. 1. Images taken under SEM. The top two images and the lower left image show potential yeast candidates. The lower right image shows a
potential Saccharomyces tetrad (sporulation structure).

The relevant sequences for the international S. paradoxus
strains generated by Liti et al. (2009) were obtained from
sgrp.html. DNA sequences were aligned and analysed within
GENEIOUS (Drummond et al., 2009); the distance, parsimony
and maximum likelihood consensus phylogenies were reconstructed from 100 to 500 bootstrap replicates. SPLITSTREE
(Huson & Bryant, 2006) was used to reconstruct the networks.

Results and discussion

diameter) as yeast cells and spores. We show these images for
the reader’s interest because of our subsequent findings.

Distribution of isolates
In total, 106 of the 172 samples (61.6%), deriving from 40 of
the 43 trees, yielded colonies on YPD agar after the enrichment procedure. We tested whether there was a significant
propensity for isolates to be more likely recovered from any
of the high/low or North/South sites using the binomial
distribution assuming an equal probability of isolation from
any site, and found there was not (P0.4).

Bark SEM
Figure 1 shows the representative SEM images of Quercus
bark samples. While this method clearly does not allow any
objective statements to be made about the presence or
absence of organisms in this niche, it does show the presence
of structures that are of the same size and shape (5 mm oval
FEMS Yeast Res 10 (2010) 941–947

Genetic identification
One to three colonies were randomly selected for identification from each bark sample that yielded colonies and
subjected to ITS RFLP analyses (a total of 158 isolates deriving
from 106 bark samples). Representatives from the 10 RFLP
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H. Zhang et al.

Fig. 2. Network of relationships between the
Saccharomyces paradoxus strains ascertained
from the concatenated sequence data. The
tree-like structure symbolizes the lack of
recombination between the main groups. The NZ
oak strains cluster strongly with the European
population. The numbers on branches are
maximum likelihood bootstrap consensus

cohorts identified had their ITS and D1/D2 26S rRNA gene
regions two-way sequenced. These sequences (accession numbers in Table 1) were compared with those present in the
NCBI database using the nucleotide BLAST-NR search tool and a
total of 10 species were revealed; the species and their percent
identity to deposits in the NCBI nucleotide database are
shown in Table 1. The presence/absence incidence of these
species among samples are also tabled: as more than one
colony may have been selected from a sample, isolates
recovered from the same sample site were not independent;
thus, the isolate count in Table 1 was collapsed to one when
more than one colony of the same species were recovered from
a given bark sample. These data should be treated with caution
as many isolates were identified solely according to their ITS
RFLP – we determined the sequence of only a few examples
from each ITS RFLP cohort.
Recalling the selective method used, the results show that
at least 10 species are present on NZ oak bark, nine of which
are Ascomycetes: Saccharomycetes (phylum: class) yeasts.
Along with S. cerevisiae and S. paradoxus, Lachancea sp.
and Torulaspora sp. have been recovered from oak bark in
the Northern hemisphere (Sampaio & Goncalves, 2008).
While both S. cerevisiae and S. paradoxus were isolated,
S. paradoxus was the more numerous of the two species in
this niche. As far as we are aware, this is the first report of
S. cerevisiae and S. paradoxus from exotic oaks in the
Southern hemisphere; note: the only other S. paradoxus
isolates from the Southern hemisphere derived from Drosophila around Rio de Jenerio (Liti et al., 2009) and soil in
South Africa (Naumov et al., 1993). The per-bark sample
recovery rate of S. paradoxus of 24% from Q. robur bark in
NZ is higher than that reported by Sampaio & Goncalves
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Table 1. The diversity of species discovered from selective enrichment of
oak (Quercus) bark samples from Auckland, NZ
Saccharomyces cerevisiae
Saccharomyces paradoxus
Pichia pastoris
Debaromyces polymorphus
Lachancea kluyveri
Torulaspora delbrueckii
Pichia membranifaciens
Candida sp.? NRRL Y-27159
Hanseniaspora osmophila
Rhodotorula mucilaginosa







The % sequence match of the divergent domains 1 and 2 of the

diagnostic 26S rRNA gene to numerous deposits in GenBank.
The incidence of species among bark samples is based on the presence/
absence data of each species in each sample after enrichment (i.e. if two
colonies from one sample were identified as being the same species, this
would simply result in a count of one for that sample).


(2008) from Canada and Germany (8%) and by Johnson
et al. (2004) from the United Kingdom (also 8%), but note
that these other studies used different enrichment protocols.
Higher rates of recovery between 23% and 80% have been
achieved from other Quercus species, though (Sampaio &
Goncalves, 2008).

To confirm the identity of the S. paradoxus and S. cerevisiae
isolates, six other loci were amplified and sequenced in six
FEMS Yeast Res 10 (2010) 941–947


New Zealand Saccharomyces ecology

randomly selected isolates. We noticed some species identification conflict between the ITS, 26S D1/D2, MF-a, MF-a,
STE and SAG loci for two NZ oak isolates. For example, the
HZ140 isolate has ITS, 26S D1/D2 and MAT sequences that
match 100% to S. cerevisiae, and also amplified fragments
from all 10 S. cerevisiae-specific microsatellite loci. However,
the STE2, SAG1, MF-a and MF-a sequences from this same
isolate were closely related to the respective S. paradoxus
sequences. Another isolate, HZ101, has ITS and 26S D1/D2
sequences that are 100% identical to S. paradoxus, but an MFa allele that is homologous to S. cerevisiae. In addition, the
IAH1 and PAD1 primers amplify alleles from HZ101 that are
homologous to S. cerevisiae, and the S. paradoxus-specific
primers fail to amplify the MF-a, STE2 and SAG1 loci.
These discrepancies were rechecked and confirmed; the
best explanation for the conflicting sequence homology
within these isolates is that they are, or have ancestors that
were, hybrids and thus contain genetic material from both
S. cerevisiae and S. paradoxus. While hybrids between these
species have been made in the laboratory (Greig et al., 2002),
there are only a few previous reports of natural hybrids
between S. cerevisiae and S. paradoxus (Naumov, 1987, 1996;
Liti & Louis, 2005; Liti et al., 2006). Our observations add to
the few inferences of natural hybrids, and thus possibly
introgression between these species. We did not ascertain the
spore viability of hybrids nor quantify the incidence of
hybrids among the remaining isolates.

Given the availability of sequence data for overseas isolates
of S. paradoxus (Liti et al., 2009) and microsatellite profiles
for NZ and overseas isolates of S. cerevisiae (Goddard et al.,
2010), we were interested in testing the global relationships
of the NZ oak Saccharomyces.
While Goddard et al. (2010) showed that NZ harbours a
distinct population of S. cerevisiae, their data also provided
tentative evidence for the presence of some migrants from
Europe. Globally, the data for S. cerevisiae show no strong
correlation with geographic distance, but are more structured around the niche of isolation (Liti et al., 2009). The
microsatellite profile of these NZ oak S. cerevisiae isolates
was compared with our database of microsatellite profiles
for NZ and international isolates (Richards et al., 2009;
Goddard et al., 2010). The genotype of the oak S. cerevisiae
strain is unique within our database, but showed a very close
match (1 bp different at two loci) to DBVPG1106, which was
isolated in Australia from wine grapes. It is worth noting
that DBVPG1106 clusters with the ‘European wine’ group
according to Liti et al.’s (2009) analyses. The S. cerevisiae NZ
oak isolate also clusters with NZ S. cerevisiae strains isolated
from the soil of an Auckland vineyard approximately 40 km
away. It appears this S. cerevisiae is closely related to other
FEMS Yeast Res 10 (2010) 941–947

strains residing in the local area and the Australasian
continent, but not other oak strains.
The existing data indicate that S. paradoxus’ population
structure is strongly described by geographic distance (Koufopanou et al., 2006; Liti et al., 2006, 2009), with discrete
populations at the continental scale. There is only one
previous inference of the intercontinental dispersal of
S. paradoxus from Eurasia to North America (Kuehne et al.,
2007). We determined the sequence at the MF-a locus for 11
of the NZ S. paradoxus strains and these were all identical.
We then determined the sequences at MF-a, STE2 and SAG1
for a subset of isolates: these sequences were also identical.
The lack of polymorphism seen in these NZ isolates suggests
that these S. paradoxus are relatively clonal in nature on local
scales and this concurs with inferences from the European
population (Koufopanou et al., 2006). We thus obtained a
single sequence at each of these four loci that is our best
estimate for alleles in the NZ oak S. paradoxus population.
We then tested the hypothesis that S. paradoxus global
diversity is principally defined by geographic distance by
reconstructing a phylogeny for the NZ and the 35 international S. paradoxus strains described by Liti et al. (2009). The
concatenated sequence data comprising the four loci
totalled 5110 bp with 20% polymorphic sites and 243
parsimony-informative characters. NZ is approximately
7000 km from the Hawaiian, 10 000 km from the Far Eastern, 12 000 km from the American and 19 000 km from the
European sample sites and thus from the S. paradoxus
populations they contain. The phylogenetic signal from all
four loci, independently and combined, places the NZ
isolates with the European group with 4 98% bootstrap
support (by distance, parsimony and likelihood methods):
this shows that the NZ isolates derive from the European
population, which is the furthest away from NZ. This result
is unsurprising, given that three (MF-a, SAG and STE) of
the NZ isolates’ four alleles are identical to alleles in the
European population. There is one unique single-nucleotide
polymorphism in the NZ isolates’ MF-a allele (thus minimizing the possibility that these are contaminants from our
strain collection, accession number HM640252), but the
remainder of the sequence is identical to an allele in the
European population. The lack of recombination within
these multilocus data on continental scales is shown in Fig.
2, which is a network generated by the neighbour net
algorithm in SPLITSTREE (Huson & Bryant, 2006). The clean
signal in the sequence data is apparent, as the network
appears tree-like, with the NZ isolates clustering strongly
with the European population. A closer examination of the
NZ strains’ relationship with the European population
shows that the NZ strains contain a unique combination of
alleles at these four loci (i.e. they represent a unique
genotype), again minimizing the likelihood that these
represent contaminants.
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Mode of global dispersal for S. paradoxus
How might members of the European S. paradoxus population come to be on trees 19 000 km away? There are clearly
many possibilities, but a very recent study by Isaeva et al.
(2009) reports that Candida railenensis (which is in the Class
Saccharomycetes) is associated with acorns of Q. robur. Thus,
it is feasible that S. paradoxus was present on/in acorns
brought here by migrants, possibly from Europe. One report
states that Quercus acorns were sent from Sydney (Australia)
and were planted during 1841–1842 in the University of
Auckland’s grounds (Barber, 1885). The origin of at least
some Q. robur planted in New South Wales may be traced
back to acorns from trees in the Royal Botanical Gardens at
Kew in the United Kingdom (Spencer, 1995). It is intriguing
to note that the NZ oak strains share alleles with European
S. paradoxus that were isolated from oaks in Windsor Great
park (Johnson et al., 2004), which is only 25 km away from
We collected and sampled acorns from some of the same
trees that we initially sampled, and subjected these to the
enrichment culture procedure. ITS RFLP and then sequence
analyses show that some of the colonies deriving from these
acorns were S. paradoxus. We went on to sequence the MF-a,
MF-a, SAG and STE alleles in one of these strains and found
alleles that were exact matches to the alleles of bark isolates.
These data show that the same genotype of S. paradoxus may
be found on the bark and acorns derived from a single tree.

Our results demonstrate that S. cerevisiae and S. paradoxus
may contemporaneously reside on oak bark in the Southern
hemisphere and extend S. paradoxus’ known geographic
range. Samples of NZ native Nothofagus failed to recover
Saccharomyces (Serjeant et al., 2008), but it would be of
interest to sample other trees native to NZ. Our inference of
hybrids supports previous data suggesting that there is gene
flow between S. cerevisiae and S. paradoxus and show that
these species may naturally hybridize and persist to some
degree (Liti et al., 2005, 2006; Muller & McCusker, 2009).
The current understanding is that S. cerevisiae’s population is generally ecologically partitioned, but that S. paradoxus is geographically partitioned. Our findings seem the
opposite of this: the NZ oak S. cerevisiae are most closely
related to other S. cerevisiae isolated locally from vineyards
and not other S. cerevisiae from overseas oak bark; the NZ
oak S. paradoxus are most closely related to S. paradoxus
from Europe – the most distant of the S. paradoxus populations, and not the Hawaiian or Far East populations, which
are closer to NZ. Together with a previous report for the
intercontinental dispersal of S. paradoxus (Kuehne et al.,
2007), our inference of interhemisphere dispersal shows that
global gene flow is not necessarily a minor force for
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H. Zhang et al.

S. paradoxus. The Australian vineyard isolate, to which the
NZ oak S. cerevisiae is closely related, clusters strongly with
the European S. cerevisiae Liti et al. (2009); the NZ oak
S. paradoxus cluster strongly with European S. paradoxus:
together, these suggest that the Australasian Saccharomyces
group may have derived from Europe via human dispersal.
We show that one possible vector for S. paradoxus dispersal
is acorns: because European migrants brought acorns to
Australasia, we speculate that this may be the source of the
NZ oak S. paradoxus population.
These data show that S. paradoxus may be globally
dispersed and this may have been aided by unwitting human
intervention. There can be few species on the face of the
planet that are not affected by human activities in some way,
and so it should not come as a surprise that S. paradoxus’
biology may also be influenced by humans, albeit to a lesser
degree than S. cerevisiae.

The authors thank A. Turner and C. Hobbis for help with
SEM imagery.

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