Fungal Ecology 28 (2017) 33e43

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Fungal Ecology
journal homepage: www.elsevier.com/locate/funeco

Diversity and biogeographical patterns of yeast communities in

Antarctic, Patagonian and tropical lakes
Luciana R. Branda~o a, 1, Aline B.M. Vaz a, 1, Lilia C. Espírito Santo a, Raphael S. Pimenta b,
Paula B. Morais b, Diego Libkind c, Luiz H. Rosa a, Carlos A. Rosa a, *
a
Departamento de Microbiologia, ICB, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
b
Universidade Federal do Tocantins, Campus Universitario de Palmas, CEP 77.001-090 Palmas, Tocantins, Brazil
c
Laboratorio de Microbiología Aplicada y Biotecnología, Instituto de Investigaciones en Biodiversidad y Medioambiente, UNComahue-CONICET, Bariloche,
Rio Negro, Argentina

a r t i c l e i n f o a b s t r a c t

Article history: We investigated the distribution patterns of yeast communities in freshwater lakes along a latitudinal
Received 29 January 2016 gradient in order to evaluate yeast biogeography at intercontinental (501e8000 km), regional (0
Received in revised form e500 km) and local (0e1 km) geographical scales. We identified 285 yeast isolates belonging to 64
24 March 2017
species based on sequence analysis of the ITS-5.8S region and the D1/D2 domains of the large subunit of
Accepted 12 April 2017
rRNA genes. Distance decay analysis showed a significant negative slope curve at the intercontinental
scale. At the intercontinental and regional scales, the dissimilarity of the yeast communities was
Corresponding Editor: Kevin K. Newsham correlated with geographical distance, with community similarity decreasing with increasing distance.
The physiological profiles of the yeast communities from tropical and Patagonian lakes were similar but
Keywords: were different from those of Antarctic lakes. This is the first report of latitudinal patterns of lake yeast
Biogeography diversity along a gradient extending from Antarctic to tropical environments.
Distance decay © 2017 Elsevier Ltd and British Mycological Society. All rights reserved.
Diversity
Freshwater
Yeasts

1. Introduction limitations (Anderson et al., 2006; Martiny et al., 2011).

Micro-organisms are diverse and abundant, and have been
Biogeography is the study of organisms' distribution patterns in regarded by some as cosmopolitan because they exhibit short
geographical space, both in contemporary terms and in the context generation times, large population sizes and long distance dispersal
of their evolution and development over time, and the processes (Fenchel and Finlay, 2004). Molecular taxonomy, which allows the
determining the distribution of biodiversity (Meadows, 2004; accurate identification of microbial species, has revealed that
O'Malley et al., 2007). A central goal of biogeography is to under- micro-organisms exhibit unique biogeographical distribution pat-
stand the mechanisms that generate and maintain diversity, such as terns. Previous biogeographical studies have described the vari-
dispersal, speciation, extinction and species interactions (Martiny ability and composition of communities of bacteria and yeasts in
et al., 2006). Distance decay analysis assumes that the similarity soil and plants (Taylor et al., 2006; Vishniac, 2006; Maksimova
of communities decreases as the distance between them increases et al., 2009; Kachalkin and Yurkov, 2012; Yurkov et al., 2015,
(Nekola and White, 1999) and is used to demonstrate how selec- 2016), bacterioplankton in lakes, and microfungi associated with
tion, drift, dispersal and mutation shape biogeographical patterns palm, fungal endophytes and other organisms (Taylor et al., 2000;
(Hanson et al., 2012). The distance decay relationship can be Vaz et al., 2014; Hyde et al., 2016). These studies show that the
influenced by environmental conditions and/or dispersal distribution of a microbial species can be influenced by geograph-
ical distance, historical factors (geology, evolution and island
biogeography), time since niche colonization and/or environmental
factors, depending on the scale analysed.
* Corresponding author. Departamento de Microbiologia, ICB, Universidade Some studies have attempted to determine yeast distribution
Federal de Minas Gerais, Belo Horizonte, 31270-901, Minas Gerais, Brazil.
E-mail address: [email protected] (C.A. Rosa).
patterns. Yeasts form part of the microbiota of most, if not all,
1
These authors contributed equally to this work. natural ecosystems and can be cosmopolitan or endemic to specific

http://dx.doi.org/10.1016/j.funeco.2017.04.003
1754-5048/© 2017 Elsevier Ltd and British Mycological Society. All rights reserved.
34 ~o et al. / Fungal Ecology 28 (2017) 33e43
L.R. Branda

habitats or regions (Starmer and Lachance, 2011; Lachance et al., Antarctic Specially Managed Area (ASMA) in Admiralty Bay, King
2016). Environmental conditions, such as temperature, pH, light George Island, South Shetland Islands (Table 1), during the austral
and concentration of readily available nutrients are some of the summer season between December 2008 and January 2009. The
ecological factors that determine the metabolic activity, growth, five lakes sampled in the ASMA represent different environmental
survival and biodiversity of yeasts (Libkind et al., 2009; Yurkov conditions: Agat Point and Wanda Lakes are influenced by marine
et al., 2015). Yurkov et al. (2015) reported that at the community water and Machu Picchu, Stanhouse and Refuge II Lakes are sub-
level, geographical region and type of substrate (phylloplane vs. jected to long periods of ice and snow-cover in the winter. Water
soil) determine yeast species distribution in birch forests in Russia. temperature and pH were measured in situ using an YSI 650 multi-
Nagahama (2006) reported yeast distribution in nine deep-sea parameter display system (YSI Environmental, USA). Three water
environments in the Pacific Ocean and found that Rhodotorula samples (500 mL) were collected in sterile bottles from five sites
sphaerocarpa (¼Rhodosporidium sphaerocarpum), Cyberlindnera spaced approximately 50 m apart and were transported on ice to
saturnus (¼Williopsis saturnus) and Candida pseudolambica (Pichia the laboratory within 24 h of sampling for processing.
clade), were isolated from all deep-sea sites, while other species,
such as Kluyveromyces nonfermentans, occurred only at some sites. 2.1.2. Patagonian lake
Several yeast species associated with plants and insects have Steffen Lake is located in Argentinian Patagonia in the Nahuel
geographical distributions that mirror their host's distribution Huapi National Park (Table 1). It has an area of 6.3 km2 and an
(Starmer and Lachance, 2011; Lachance et al., 2016). average depth of 76.8 m. The lake is of glacial origin, is oligotrophic,
Surveys of the geographical distribution of aquatic yeast species has a high transparency (Secchi disk: 13 m), and has limited human
are sparse, with most being focused on the influence of water influence. A native Andean Patagonian forest composed of Notho-
pollution (Nagahama, 2006). Few species of yeast appear to be fagus spp. surrounds the lake. Mean annual surface water temper-
specifically associated with aquatic habitats. Debaryomyces hansenii ature is c. 17  C (Quiro
 s, 1988). Three water samples (300e400 mL)
is the most common ascomycetous yeast isolated from marine were collected in sterile bottles from four sites located approxi-
waters. This yeast is considered to be a ubiquitous species because mately 200 m apart on a transect along the lake. The samples were
it is found in different environments and regions. Other ubiquitous transported on ice to the laboratory within 24 h for processing.
species frequently associated with aquatic habitats such as Aur- Water temperature was measured in situ and pH was measured in
eobasidium pullulans, Rhodotorula mucilaginosa and Vishniacozyma the laboratory with a 3310 Jenway pH meter (Staffordshire, UK).
victoriae (¼ Cryptococcus victoriae) are also found in different re-
gions and environments (de García et al., 2007; Branda ~o et al., 2011; 2.1.3. Tropical Brazilian lakes
Vaz et al., 2011; Yurkov et al., 2015). Some species are endemic to Samples were obtained from three tropical lakes in Brazil
specific regions: for example, Metschnikowia australis is associated (Table 1). Dom Helvecio Lake is located in the Ecological State Park
with algae, marine invertebrates and seawater in Antarctica of Rio Doce, which comprises an area of 36,113 ha and constitutes
(Lachance, 2011; Godinho et al., 2013), suggesting that the the largest relict area of Atlantic rain forest in Minas Gerais state.
ecological distribution of aquatic yeast communities could be The lake has a surface area of 6.87 km2 and is considered to be the
influenced by geographical patterns and the local conditions of largest and deepest lake of the middle Rio Doce lake system. It is
each environment. one of the deepest natural lakes in Brazil, with an average depth of
In the present study, we investigated the spatial distribution of 32.5 m. The lake is oligotrophic, warm, monomictic and has one
cultivable yeasts on a geographical transect from polar to tropical circulation period, usually between May and August (Matsumura-
lakes. This gradient included lakes in Antarctica, southern Tundisi and Tundisi, 1995). Three water samples (100 mL) were
Argentina and southeastern and northern Brazil. We explored collected in sterile bottles from six sites located approximately
whether environmental and/or geographical distances explained 100 m apart on a transect along the lake. Samples were transported
yeast community composition at three different geographical to the laboratory on ice within 24 h for processing. Temperature
scales (intercontinental, regional and local) and between different was measured in situ and pH was measured in the laboratory with a
lakes. HI 211 combined meter (Hanna instruments, Rhode Island, USA).
Rico and de Dentro Lakes are located in Cant~ ao State Park (9100 S,
2. Material and methods 50100 W), a protected area located in the west of the Tocantins
state, which represents an ecotone area among the Cerrado,
2.1. Characteristics of the lakes and sampling sites Amazon forest and Pantanal ecosystems (Santos and Lolis, 2007). A
dense Amazonian forest surrounds the lakes and, in the rainy
2.1.1. Antarctic lakes season (OctobereApril), the whole plain is flooded as the water
Water samples were collected from five different lakes in the level rises by 7e10 m (Pinheiro and Dornas, 2009). The presence of

Table 1
Description of study sites and diversity indexes of yeasts included in the present study.

Environment Lakes Geographical Total yeast Temperature Mean Number Number of Number of Shannon
coordinates counts ( C)b pH of isolates yeast species singletons index (H0 )
(CFU L1)a

Tropical Lago Rico 9 210 S, 50 000 W 721.6 ± 918.0 23.5 6.9 50 19 6 2.60
Brazil Lago de Dentro 9 210 S, 49 580 W 373.3 ± 426.2 23.0 7.1 56 19 6 2.38
Dom Helve cio 19 290 S, 19 480 W 774.1 ± 590.2 24.4 6.2 52 17 3 2.57
Patagonian, Argentina Steffen 41 310 S, 71 330 W 52.2 ± 35.5 17.0 7.0 51 17 5 2.43
Antarctic Stanhouse 62 040 S, 58 220 W 53 ± 25.1 0.2 9.1 16 5 1 1.94
Refúgio II 62 040 S, 58 250 W 5.6 ± 2.85 4.2 8.5 14 1 1.99
Wanda 62 040 S, 58 190 W 37.71 ± 9.0 1.8 7.4 8 3 e 1.77
Machu Picchu 62 050 S, 58 190 W 20.8 ± 17.9 0.7 7.1 22 8 1 2.07
Agat Point 62 110 S, 58 260 W 73.5 ± 58.4 2.8 7.5 15 4 e 1.76
a
Mean ± standard deviation.
b
Temperature values are point measurements.
 ~o et al. / Fungal Ecology 28 (2017) 33e43
L.R. Branda 35

many lakes (about 800) and the flooding regime makes the region 2.4. Analysis of ecological data
similar to the Pantanal biome. Three water samples (100 mL) were
collected in sterile bottles from five sites approximately 30 m apart Species accumulation curves were used to determine whether a
on a transect along the lakes. Samples were transported to the sufficient number of samples had been obtained from each envi-
laboratory on ice within 24 h for processing. The temperature and ronment (Colwell et al., 2004). The extrapolated richness was
pH of the water were measured in situ using a digital sampler estimated using the nonparametric estimator Chao2 (Colwell and
(Horiba U-22, Fukuoka, Japan). Coddington, 1994) and the richness was compared using a heat
map, in which the similarities were computed based on a
dendrogram. Yeast diversity in each lake was measured using the
2.2. Yeast isolation
Shannon (H0 ) index (H ¼ -Sni/n ln (ni/n), where ni is the number of
individuals of the taxon i and n is the total number of individuals
Samples of subsurface water (10e30 cm depth) from each lake
(Ryan et al., 1995). The Kruskal-Wallis test was used to test for
were filtered through sterile nitrocellulose membranes (0.45 mm,
differences in the numbers of CFUs between lakes.
47 mm diameter) with a Nalgene filtration device (Nalgene™,
b-diversity was evaluated using the rate of distance decay,
Rochester, USA) and vacuum pump. The membranes were placed
which assumes that community similarity decreases with
on the surface of yeast extract-malt extract agar medium (YMA,
increasing geographical distance (Nekola and White, 1999). The
0.3% yeast extract, 0.3% malt extract, 0.5% peptone, 1% dextrose, 2%
yeast community similarity based on the Jaccard index was
agar, pH 4.0), containing chloramphenicol at 200 mg L1. Petri
regressed against geographical distance (ln-transformed) and the
dishes were incubated at 15  C (for samples from Antarctic and
distance decay relationship was calculated as the slope of least-
Steffen lakes) and at 20  C (for those from tropical lakes) for 3e7
squares linear regression (Nekola and White, 1999). The
days. Yeast colony forming units (CFUs) were counted for quanti-
geographical distance was logarithmically transformed owing to
tative analysis. Each morphotype was purified by repeatedly
the large distances between the lakes (Martiny et al., 2011; Vaz
streaking on YMA medium. When possible, at least three randomly
et al., 2014). Geographical distance between the sampling sites
selected colonies of each morphotype were selected and stored
was classified as either intercontinental (501e8000 km), regional
at 80  C prior to identification.
(0e500 km) or local (0e1 km). In addition, we tested whether the
slope of the distance decay curve of each sampling site was
2.3. Yeast identification significantly different from zero using a randomisation procedure
with 1000 iterations. The yeast richness was compared between
All yeast isolates were grouped based on colony morphology, lakes using the heatmap.2 function in R, using ‘complete’ (com-
physiological tests and sequence analyses. The physiological char- plete-linkage) as the clustering method.
acteristics of all isolates were tested according to assimilation To investigate the relationship between yeast community sim-
patterns of carbon and nitrogen sources. Fifty-one physiological ilarity and the geographical distance and environmental charac-
tests were performed, viz. glucose fermentation, assimilation of teristics, we applied the ranked partial Mantel test (Goslee and
carbon compounds (acetate, cellobiose citrate, D-arabinose, D- Urban, 2007; Martiny et al., 2011; Vaz et al., 2014). Principal
glucitol, D-gluconate, D-glucosamine, D-mannitol, D-ribose, D- component analysis (PCA) of the environmental variables (pH and
xylose, DL-actate, ethanol, erythritol, ethyl acetate, galactitol, temperature) was performed and the dissimilarities were
galactose, glucitol, glucose, glycerol, hexadecane, inulin, iso- computed for the first component. Correlations were examined
propanol, lactose, L-arabinose, L-rhamnose, L-sorbose, maltose, with the Spearman correction, with the P values being based on
melibiose, melezitose, methanol, myo-inositol, ribitol, N-acetyl-D- 10,000 permutations.
glucosamine, raffinose, salicin, soluble starch, succinate, sucrose, Multiple regression matrices (MRM) were used to determine the
trehalose and xylitol), utilization of nitrogen compounds (lysine, relative importances of geographical distance and environmental
nitrite and nitrate), growth in amino-acid-free medium, growth at variables to the similarities of the yeast communities (Goslee and
30  C, growth on YMA with 10% sodium chloride and 50% glucose, Urban, 2007). To reduce the effect of spurious relationships be-
resistance to acetic acid, acid production (solubilisation of CaCO3) tween variables, we performed the MRM test, removed the non-
and the formation of starch-like compounds (Kurtzman et al., significant variables and then repeated the test (Martiny et al.,
2011). The response for each test was assigned a value of 0 (no 2011). Temperature and pH were identical at the collection points
growth), 0.5 (weak or variable) or 1 (positive). in each Antarctic lake and were hence not included in the tests at
Isolates with identical morphological and physiological char- the local scale. We tested the significance of each model by per-
acteristics were grouped together and subjected to PCR finger- forming 10,000 permutations.
printing with the core sequences of the primer (GTG)5 (Libkind The yeasts were grouped according to their physiological char-
et al., 2003). Yeast strains with identical PCR fingerprint patterns acteristics and agglomerative hierarchical clustering using the
were grouped together and putatively considered to belong to the function hclust (Oksanen, 2009). All analyses were performed using
same species (Sampaio et al., 2001; Brand~ ao et al., 2011). At least the R package (R Development Core Team, 2012).
50% of the yeast isolates of each molecular group were identified by
sequencing. Species identification was performed by sequence 3. Results and discussion
analysis of the ITS-5.8S region and the D1/D2 variable domains of
the large subunit of rRNA genes as described previously (Kurtzman 3.1. Diversity analysis
and Robnett, 1998). DNA extraction was performed according to
Branda ~o et al. (2011). The amplified DNA was concentrated, cleaned The heatmap analysis confirmed that the lakes were colonized
and sequenced in an ABI 3130 Genetic Analyzer automated by distinct sets of yeast species according to the environment
sequencing system using BigDye v3.1 and POP-7 polymer. The se- studied. Sporobolomyces japonicus, Pichia kudriavzevii, Papiliotrema
quences obtained were compared with those in the GenBank laurentii and A. pullulans occurred mainly in de Dentro and Rico
database using the Basic Local Alignment Search Tool (BLAST; lakes in tropical Brazil. M. australis was prevalent in Agat point and
https://www.ncbi.nlm.nih.gov/pubmed/2231712) (Altschul et al., Wanda lakes in Antarctica, while Leucosporidium muscorum,
1990). V. victoriae and R. mucilaginosa dominated in Stanhouse, Machu
36 ~o et al. / Fungal Ecology 28 (2017) 33e43
L.R. Branda

Picchu and Refuge II lakes (Fig. 1). The distance decay analysis intercontinental scale (slope ¼ 0.004, P < 0.001) (Fig. 2). At the
showed a significant negative slope curve when compared at the local scale, the distance decay was also significant for polar

Fig. 1. Heatmap of yeast richness in temperate (Argentinian Patagonian), tropical (Brazilian) and polar (Antarctic) lakes.
 ~o et al. / Fungal Ecology 28 (2017) 33e43
L.R. Branda 37

Fig. 2. Distance decay relationship for the yeast communities. Pairwise community similarities were calculated using the Jaccard index and plotted against the natural logarithms of
the distances among study sites. The lines denote significant (P < 0.001) linear regressions at the intercontinental scale (green) and at local scales in tropical (blue, Brazil) and polar
(red, Antarctic) environments.

(slope ¼ 0.003, P ¼ < 0.001) and tropical (slope ¼ 0.005, and de Dentro Lake (R2 ¼ 17%, P < 0.05) (Table 3). The geographical
P ¼ < 0.001) lakes (Fig. 2). Using ranked partial Mantel tests, yeast distance influenced the yeast community similarity for both lakes,
community dissimilarity was highly significantly correlated with while pH value was significant only for de Dentro Lake. Water pH
geographical distance at the intercontinental scale (r ¼ 0.26, varied from 6.80 to 7.22 in de Dentro Lake and the negative ß value
P < 0.001). At the regional scale, there was a marginally significant in the MRM analysis suggests that the yeast community similarity
correlation between yeast communities in tropical Brazil increases as pH decreases (Table 3). However, this influence of pH
(r ¼ 0.096, P < 0.058) (Table 2). These findings are consistent with on yeast community similarity was not observed for the other lakes.
the strong effect of geographical distance on yeast community Further studies on organic matter fractionation in these lakes may
structure indicated by the MRM analysis (Table 3). Two mecha- be important to understand acidification processes in freshwater
nisms can explain the decline in similarity between yeast com- environments. However, our results suggest that pH value could be
munities and increasing geographical distance. Firstly, an important factor in selecting the yeast communities across de
environmental conditions become increasingly different as dis- Dentro Lake.
tance between sampling sites increases. If the yeast species within a We compared the yeast communities based on the physiological
community are adapted to specific lake conditions, then commu- profiles of the species and the nutritional profile of the yeast
nities would be expected to become increasingly different with community found in each lake. We found two distinct groups based
distance since species are sorted according to their niche re- on similar physiological profiles (Fig. 3). One group consisted of
quirements. Secondly, several yeast species have restricted yeast communities from tropical and Patagonian lakes and another
dispersal and tend to colonize sites with similar ecological condi- group contained yeast communities from Antarctic lakes. Most
tions (Vaz et al., 2014). Therefore, for these species, a distance decay species were able to assimilate more than 25 carbon compounds,
relationship would emerge even without differences in lake con- presenting a wide nutritional profile. These species could compete
ditions or yeast nutritional requirements. for nutrients more efficiently in environments with limited avail-
MRM analysis showed the factors that best explain the corre- able nutritional sources, such as in the Antarctic lakes and Steffen
lation. Distance, pH and temperature were statistically significant Lake. Cosmopolitan species such as A. pullulans, D. hansenii and
terms in the model at an intercontinental scale. The ß value shows R. mucilaginosa had broad nutritional profiles and were found in all
that the similarity increased as the distance and pH decreased and lakes. Saccharomyces eubayanus, Lachancea nothofagi, Rhodotorula
temperature increased. Temperature did not play a significant role colostri, Rhodotorula fujisanensis and M. australis had limited
(P > 0.05) at the local level and was removed from the final model nutritional profiles and were restricted to lakes of cold regions
(Table 3). At the local scale, when each lake was analysed sepa- (Patagonia and Antarctica).
rately, the proportion of the variability explained by the MRM We demonstrated that yeast communities in Antarctic, Patago-
models was statistically significant when compared with the nian and Brazilian tropical lakes are not randomly distributed.
samples from the transects across Rico Lake (R2 ¼ 21%, P < 0.005) These lakes constitute unique ecosystems that select yeast
 38
Table 2
Partial Mantel test results, where Spearman r represents the correlation between the yeast community dissimilarity and either geographic distance or environmental distance.

Correlation between yeast Controlling for: Intercontinental Regional scales

communities
Tropical Brazil Argentinian Antarctica
Patagonia

r P r P r P r P

Geographic distance Environmental distance 0.26 <0.001 0.096 0.058 e e 0.022 0.64
Environmental distance Geographic distance 0.00071 0.49 0.031 0.67 e e 0.059 0.14

The environmental variables were first examined using a principal components analysis that considered temperature and pH of each lake. The P values are one-taled and based on 10,000 permutations.

L.R. Branda
~o et al. / Fungal Ecology 28 (2017) 33e43
Table 3
Results of the multiple regressions on matrices (MRM) analysis for the yeast communities by spatial scale.

Intercontinental Local Tropical Brazil Argentinian Patagonia Antarcticab

a
Tropical Brazil Antarctica DH LR LD STF ST MP RF WA AP
R2 ¼ 0.05 R2 ¼ 0.2*b R2 ¼ 0.17**c R2 ¼ 0.09 R2 ¼ 0.002 R2 ¼ 0.002 R2 ¼ 0.012 R2 ¼ 0.001 R2 ¼ 0.002

Ln (geographic distance) 0.26 0.09 0.02 0.03 0.44* 0.44** 0.09 0.04 0.02 0.11 0.03 0.04
pHd 0.18 0.01 0.06 0.23 0.02 0.56** 0.17 e e e e e
Temperature 0.1 0.04 0.008 e e e e e e e e e

Levels of significance denoted by: * P < 0.01, ** P < 0.001.

a
Lakes: DH: Dom Helve cio, LR: Lago Rico, LD: Lago de Dentro, STF: Steffen, AP: Agat Point, WA: Wanda, MP: Machu Picchu, RF: Refuge II, ST: Stanhouse.
b
P  0.01.
c
P  0.001: The variation (R2) of the community similarity that is explained by the remaining variables and the partial regression coefficients (b) of the final model are reported. If the partial regression is reported, then its
significance level (one-way tests) is P < 0.05.
d
The pH and temperature did not vary in the five Antarctic lakes and were hence not analysed for in the MRM analysis. There was only one lake on Patagonian (Argentina) ecosystem and it was not possible to do the MRM
analysis for this local scale.
 ~o et al. / Fungal Ecology 28 (2017) 33e43
L.R. Branda 39

cio, Lago de Dentro and Lago Rico),

Fig. 3. Dendrogram representing the similarity of the physiological profiles of the yeast communities from tropical Brazilian (Dom Helve
Argentinian Patagonian (Steffen) and Antarctic (Refuge II, Stanhouse, Wanda, Agat Point and Machu Picchu) lakes.

communities that are able to tolerate stressful conditions and occurrence of this yeast species only in Agat Point and Wanda Lakes
nutrient availabilities. We observed a distance decay relationship at further supports the view that M. australis is of marine origin, since
all intercontinental scales that could be explained by dispersion these lakes are fed by seawater.
limitations and/or environmental selection. The influence of the V. victoriae has been previously isolated from lichens, mosses
environment or geographical distance in this relationship varied and soil (Thomas Hall et al., 2002). This species was the most
between the distance scales. Furthermore, yeast communities in frequent species obtained from different substrates in Antarctica
lakes, mainly those of Antarctica and Patagonia, showed species (Vaz et al., 2011; Santiago et al., 2016) and is found in other cold
with restricted nutritional profiles, suggesting habitat specificity environments, such as the Calderone Glacier in Italy (Branda et al.,
for these yeasts. 2010), ice from subglacial environments in Arctic habitats (Butinar
et al., 2007) and a Patagonian lake in Argentina (Branda ~o et al.,
3.2. Yeast occurrence and diversity 2011). However, this yeast could be more widespread, since its
occurrence has been reported in other regions, for instance in rice
We obtained and identified 285 yeast isolates belonging to 36 leaves in Thailand (Tantirungkij et al., 2015), or in soil in Mediter-
genera and 64 species (Table 4). The yeast species most commonly ranean forests (Yurkov et al., 2015). Two C. parapsilosis isolates were
isolated were A. pullulans, Pa. laurentii, D. hansenii, L. muscorum, M. obtained from Stanhouse Lake. This species is an opportunistic
australis, P. kudriavzevii, Moesziomyces aphidis, Rhodotorula babje- pathogen and is common in aquatic environments polluted by
vae, Rh. mucilaginosa, S. japonicus and V. victoriae. Basidiomycetous sewage (Nagahama, 2006). The occurrence of this yeast species in
yeasts were predominant in all lakes, representing 65.6% of the Stanhouse Lake could be associated with guano from seabirds, the
total isolates. These yeasts are often found associated with the effect of the oceanic tide or the presence of humans due to tourism
phyllosphere of terrestrial plants and their occurrence in tropical in the Antarctic Peninsula (Chryssanthou et al., 2011).
and temperate aquatic environments might be the result of run-off R. babjevae was the most frequent species obtained from the
from surrounding plant substrates (Branda ~o et al., 2011; Starmer temperate Steffen Lake in Argentina. This species has a wide
and Lachance, 2011). Basidiomycetous yeasts are more nutrition- geographical distribution, since it has been isolated from several
ally versatile and tolerant to extreme environmental conditions different substrates in Europe, America and Asia (Sampaio, 2011)
compared with ascomycetous yeasts (Branda ~o et al., 2011), which and from freshwater (Libkind et al., 2003) and marine environ-
could explain their frequent occurrence in Antarctic lakes. M. aus- ments (Gadanho et al., 2003). L. muscorum, the second most
tralis was isolated only from Agat Point and Wanda Lakes. This yeast frequently isolated species in this environment, has been previ-
is indigenous to Antarctic marine habitats (Lachance, 2011) and has ously isolated from lakes and glaciers in Patagonian Argentina (de
been isolated from marine sediment, seawater and thalli of the García et al., 2007; Libkind et al., 2009; Brand~ ao et al., 2011).
algal species Adenocystis utricularis, Desmarestia anceps and Pal- Most yeasts isolated from Steffen Lake were allochthonous species
maria decipiens (Vaz et al., 2011; Godinho et al., 2013). The and may be associated with plants and plant-related substrates
40 ~o et al. / Fungal Ecology 28 (2017) 33e43
L.R. Branda

Table 4
Identification, number of isolates and origin of the yeast species isolated from the lakes studied.

Yeast species No. of isolates Tropical Brazil Patagonian Argentina Antarctic

DHa LR LD STF SH MP AP WA RF

Apiotrichum porosum 2 2
Aureobasidium pullulans 11 4 1 5 1
Candida glabrata (Nakaseomyces clade) 1 1
Candida melibiosica (Metschnikowiaceae clade) 1 1
Candida michaeli (Yamadazyma clade) 1 1
Candida parapsilosis (Lodderomyces/C. albicans clade) 2 2
Candida tropicalis (Lodderomyes/C. albicans clade) 1 1
Candida sp.A UFMG-CM-Y3404 1 1
Candida sp.B UFMG-CM-Y3427 (Diutina clade) 1 1
Cyberlindnera saturnus 1 1
Cystofilobasidium capitatum 1 1
Cystofilobasidium infirmominiatum 1 1
Debaryomyces hansenii 11 8 2 1
Exophiala heteromorpha 4 4
Filobasidium magnum 2 2
Hannaella luteola 3 1 2
Hannaella pagnoccae 5 2 3
Hannaella siamensis 3 2 1
Holtermanniella festucosa 2 2
Holtermanniella nyarrowii 1 1
Holtermanniella wattica 3 3
Kodamaea ohmeri 1 1
Kabatiella microsticta 2 1 1
Lachancea nothofagi 2 2
Leuconeurospora pulcherrima 3 1 2
Leucosporidium creatinivorum 2 2
Leucosporidium fragarium 7 2 5
Leucosporidium muscorum 11 1 9 1
Leucosporidium scottii 1 1
Meira argovae 1 1
Metschnikowia australis 16 10 6
Meyerozyma guilliermondii 7 2 3 1 1
Moesziomyces antarcticus 1 1
Moesziomyces aphidis 12 12
Mrakiella aquatica 4 3 1
Naganishia adeliensis 9 9
Papiliotrema flavescens 3 1 2
Papiliotrema laurenti 11 3 2 6
Papiliotrema leoncinii 2 2
Papilotrema taeanensis 2 2
Pichia fabianii 1 1
Pichia kudriavzevii 23 5 2 16
Pseudozyma hubeiensis 5 1 4
Rhodotorula babjevae 11 11
Rhodotorula colostri 1 1
Rhodotorula fujisanensis 5 5
Rhodotorula mucilaginosa 22 7 6 2 2 2 3
Rhodotorula taiwanensis 2 2
Rhodotorula toruloides 3 3
Rhodosporidiobolus odoratus 1 1
Rhodosporidiobolus ruineniae 1 1
Rhynchogastrema aquatica 1 1
Rhynchogastrema complexa 3 1 2
Saccharomyces eubayanus 1 1
Saitozyma podzolica 3 3
Sporobolomyces japonicus 19 18 1
Sympodiomycopsis yantaiensis 1 1
Tremella globispora 3 2 1
Ustilago esculenta 2 1 1
Vishniacozyma carnescens 1 1
Vishniacozyma victoriae 16 8 1 7
Wickerhamiella slavikovae 2 1 1
Wickerhamomyces sp. UFMG-CM-Y3346 2 2
Wickerhamomyces sydowiorum 1 1
Total 285 52 54 54 50 16 22 15 8 14
a cio, LR: Lago Rico, LD: Lago de Dentro, STF: Steffen, SH: Stanhouse, MP: Machu Picchu AP: Agat Point, WA:Wanda, RF: Refuge II.
DH: Dom Helve

surrounding this environment. followed by S. japonicus, R. mucilaginosa and Pa. laurentii. Most
Tropical lakes, which were located in protected areas and have yeast species obtained from Brazilian tropical lakes have been
limited human influence had the highest number of yeast isolates, previously isolated from other tropical freshwater environments. P.
with P. kudriavzevii (23 isolates) being the most frequent species, kudriavzevii is often found in aquatic environments with high levels
 ~o et al. / Fungal Ecology 28 (2017) 33e43
L.R. Branda 41

Table 5
P values from Kruskal-Wallis analyses showing statistical differences between yeast counts (CFU1L) in the lakes studied.

Environments Tropical Brazil Patagonian Argentina Antarctica

DH LR LD STF AP WA MP RF ST
a
Tropical Brazil DH n.s. n.s. 0.022 0.006 0.001 <0.001 <0.001 0.011
LR n.s. n.s. n.s. 0.005 <0.001 n.s.
LD n.s. n.s. 0.026 <0.001 <0.001 n.s.
Patagonian Argentina STF n.s. n.s. n.s. 0.0006 n.s.
Antarctica AP n.s. n.s. 0.022 n.s.
WA n.s. n.s. n.s.
MP n.s. n.s.
RF 0.015
ST
a cio, LR: Lago Rico, LD: Lago de Dentro, STF: Steffen, AP: Agat Point, WA: Wanda, MP: Machu Picchu, RF: Refuge II, ST: Stanhouse. n.s.: not significant
Lakes: DH: Dom Helve
(P > 0.05).

of organic matter from industrial and domestic waste, but this yeast similar to those found in studies of Patagonian glacial meltwaters
is often found in soil, on fruits and various natural environments from the Frías, Castan ~ o Overo and Río Manso glaciers, located on
(Nagahama, 2006; Kurtzman, 2011), and is also considered to be an Mount Tronador in the Nahuel Huapi National Park in North-
opportunistic pathogen (Kurtzman, 2011). The high frequency of western Patagonia, Argentina (de García et al., 2007). Antarctic
this species in de Dentro and Dom Helvecio Lakes could be also lakes are also subjected to long periods of ice and snow-cover and
attributed to faecal contamination by animals (Branda ~o et al., 2010). dramatic changes of photosynthetic activity between the winter
The opportunistic pathogenic species Candida tropicalis was also and summer seasons (Brunati et al., 2009). The Antarctic lakes in
isolated from de Dentro lake, but this species is frequently isolated our study do not have surrounding vegetation, which could explain
from rotting wood (Cadete et al., 2012), and so this isolate was the correspondingly low yeast counts and Shannon values (Table 1).
possibly not of human or animal origin. The low yeast densities observed in the Argentinian lake studied
A. pullulans, Pa. laurentii, D. hansenii, Meyerozyma guilliermondii here may be related to the meltwater rivers draining from the lake
and R. mucilaginosa are widely distributed in nature and were that are oligotrophic and characterized by low nutrient concen-
isolated from more than three lakes, suggesting cosmopolitan trations (de García et al., 2007; Libkind et al., 2009). In addition, the
distributions. These species have been previously isolated from community of plants surrounding this lake is composed mainly of
worldwide aquatic environments (Libkind et al., 2003; Nagahama, Nothofagus species and is of low diversity. The low diversity of plant
2006; Butinar et al., 2007; Vaz et al., 2011) and could have been species around the lake could also explain the low yeast densities,
introduced with allochthonous organic matter. since the yeast occurrence in water bodies reflects inputs from
Based on analyses of the sequences of the D1/D2 domains of terrestrial sources such as soil and plant debris. High UV radiation
rRNA, we found four isolates that could represent three new spe- exposure might also play a role in reducing the frequencies of
cies. Two isolates identified as Wickerhamomyces sp. UFMG-CM- yeasts in Antarctic and Patagonian lakes, in particular in the sub-
Y3346 (GenBank accession number KJ608555) showed one to two surface waters studied here (Libkind et al., 2009; Brand~ ao et al.,
nucleotide differences from several yeast strains deposited in 2011).
GenBank. These strains could represent a new Wickerhamomyces The Shannon diversity values of the lakes studied are shown in
species lacking a formal description. The strain identified as Table 1. The highest diversity values were for tropical Brazilian and
Candida sp.A UFMG-CM-Y3404 (GenBank accession number temperate Argentinian lakes, and were similar to those found for
KR815866) belongs to the Metschnikowiaceae clade and had 85% the Nahuel Huapi Lake in Patagonia (Branda ~o et al., 2011) and a
identity with Candida pimensis and Candida picachoensis and 89% tropical Brazilian lake surrounded by Atlantic rain forest in Brazil
identity with Candida picinguabensis. One isolate, identified as (Medeiros et al., 2008). These results support the hypothesis that
Candida sp.B UFMG-CM-Y3427 (GenBank accession number aquatic environments surrounded by dense and diverse vegetation
KR815865), differed by two nucleotide substitutions from Candida support diverse yeast communities (Branda ~o et al., 2011).
sp. BG02-7-16-015A-2-1 and likely represents the same species. The sampling did not capture the richness of yeasts in the
This new species is phylogenetically related to the clade Diutina temperate and tropical lakes studied, demonstrated by the lack of
(Khunnamwong et al., 2015). The species Wickerhamiella slavikovae, asymptote for the corresponding species accumulation curves
Hannaella pagnoccae and Papiliotrema leoncinii were recently (Supplementary Fig. 1). Moreover, the extrapolated richness using
described by Hagler et al. (2013), Landell et al. (2014) and Pagani the Chao2 estimator indicated that our sampling effort was enough
et al. (2016), respectively, using isolates from this study. All new to account for 67%, 73% and 79% of the yeast species in tropical,
species that we isolated originated from tropical lakes. polar and temperate lakes, respectively. More samples are thus
Mean total yeast counts in each lake are shown in Table 1. Water needed to estimate the actual diversity of yeasts in these lakes
samples collected in Antarctica yielded lower numbers of yeast (Colwell et al., 2004). However, in Antarctic lakes the curve
colonies than the Brazilian and Patagonian lakes (Table 5), with the approximated an asymptote (Supplementary Fig. 1), indicating that
highest yeast counts being obtained from tropical Brazilian lakes. increasing sampling will not significantly increase the number of
Yeast diversity and density in aquatic environments may thus have species found. This finding might be owing to the geographical
been influenced by biotic factors, including allochthonous sources isolation and inhospitality of Antarctica.
like soil and plant debris (Nagahama, 2006; Branda ~o et al., 2010,
2011) and abiotic factors such as pH, temperature and UV radia- Acknowledgments
tion (Brunati et al., 2009).
The highest yeast densities obtained from tropical lakes could be This work was funded by Conselho Nacional de Desenvolvi-
related to the occurrence of a dense and diverse plant community  gico (CNPq: PROANTAR-407230/2013-
mento Científico e Tecnolo
surrounding the lakes. The yeast density of Antarctic lakes was 0 and 457499/2014-1) and Fundaça ~o de Amparo a
 Pesquisa do
42 ~o et al. / Fungal Ecology 28 (2017) 33e43
L.R. Branda

Estado de Minas Gerais (APQ-01525-14). We thank the editor and Antonie Leeuwennhoek 73, 331e371.
Kurtzman, C.P., Fell, J.W., Boekhout, T., Robert, V., 2011. Methods for the isolation,
two anonymous reviewers for their constructive comments, which
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