FUNGI IN THE PATOS LAGOON ESTUARY AND CASSINO BEACH

FUNGOS E LEVEDURAS NO ESTUÁRIO DA LAGOA DOS PATOS

E PRAIA DO CASSINO, RS, BRASIL
ERICA S. SILVEIRA1; RUBENS CÁURIO LOBATO2; PAULO CESAR ABREU3
1
Post-Graduation Course on Biological Oceanography, Federal University of Rio Grande – FURG, Rio Grande, RS, Brazil. Mailing adress: Rua
Anchieta, nº1416, apto 302, Pelotas, RS, Brasil. Cep.: 96015.420.; tel.: (5553) 99831656, (5553)32336535).; Email: [email protected]
2
Post-Graduation Course on Biological Oceanography, Federal University of Rio Grande – FURG, Rio Grande, RS, Brazil.
3
Institute of Oceanography, Federal University of Rio Grande – FURG, Rio Grande, RS, Brazil.

ABSTRACT
FUNGI AND YEASTS IN THE PATOS LAGOON ESTUARY AND CASSINO BEACH, RS, BRAZIL
This study evaluated the spatial and temporal variability of the fungi and yeasts in the waters of the estuarine region of the
Patos Lagoon and the adjacent oceanic Cassino Beach. Water samples was sampled monthly (March 2007 to June 2008) from
three sites the richness of fungi was assessed by cultivating the samples in Sabouraud agar plates with Chloramphenicol.
Environmental variables like water temperature, salinity, pH and dissolved inorganic nutrients (phosphate ammonium, nitrite and
nitrate) were also analyzed. The most common fungal genera found were Aspergillus, Penicillium, and clusters of non-
sporulating fungi and yeasts. Fungi distribution was mainly affected negatively by salinity and positively by ammonium and
phosphate.

KEYWORDS: spatial variability, temporal variability, salinity, nutrients

RESUMO
Este estudo avaliou a variabilidade espacial e temporal dos fungos e leveduras nas águas da região estuarina da Lagoa dos
Patos e praia do Cassino. Amostras de água foram coletadas mensalmente pelo período de um ano em três pontos distribuídos
ao longo do estuário da Lagoa dos Patos e região costeira adjacente. A riqueza de fungos foi avaliada através de cultivos das
amostras em placas com ágar Sabouraud com Cloranfenicol. Variáveis ambientais como temperatura da água, salinidade, pH e
nutrientes inorgânicos dissolvidos (fosfato, amônia, nitrito e nitrato), também foram analisados. Os gêneros de fungos mais
encontrados foram Aspergillus, Penicillium, e agrupamentos de fungos não-esporulados e leveduras. A distribuição de fungos
foi afetada negativamente pela salinidade e positivamente pelas concentrações de amônia e fosfato.

PALAVRAS-CHAVE: variabilidade espacial, variabilidade temporal, salinidade, nutrientes

INTRODUCTION Fungi have a fundamental role in maintaining

ecosystems balance, considering their activity in the
Fungi are micro- or macroscopic eukaryotic decomposition of organic matter and nutrient recycling.
organisms with cell walls composed of chitin found in These microorganisms are also important in improving
all environments (terrestrial, aquatic and aerial ones). the nutritional quality of organic substrate consumed by
They reproduce asexually and/or sexually and are detritivorous organisms. Some fungi can remove or
classified as heterotrophic, with saprophagic behavior degrade inorganic and recalcitrant pollutants, in this case
(Alexoupoulos et al. 1996). Fungi are ubiquitous in the functioning as water purifiers (Schoenlein-Crusius et al.
water, but their distribution is influenced by 2004). Studies aimed at the identification of
geographical location and substrates (Jones & Alias microorganism species are important in providing a
1997, Gareth et al. 2006). better understanding of biodiversity and aquatic ecology,
Truly aquatic fungi and those that can be found in but also as alternative to obtain bioproducts and
aquatic environments differ greatly in that the aquatic biotechnological processes (Vasconcelos et al. 2003).
fungi depend on water for reproduction and have special The estuarine region of the Patos Lagoon, RS
morphological adaptations that allow the life in the water has high rates of primary productivity and a considerable
(Sparrow 1968, Dick 1970). Terrestrial fungi might use biological diversity (Seeliger & Castelo 1997). It is a
water as a vehicle for transporting their dispersal units, reproduction and nursery area of many marine fish and
or can be carried to aquatic environments by wind, crustacean species, which find protection and food in
leaching, or attached to allochthonous organic this environment. Detritivorous food chain prevails in this
substrates (Sparrow 1968, Dick 1970). ecosystem, where the biomass of higher plants is
There is scant information about fungi found in decomposed by bacteria and fungi, turning the matter
aquatic environment in South America coastal marine and energy produced by plants available to aquatic
environments. In Brazil, few studies reported the consumers (Seeliger & Castelo 1997).
occurrence of fungi (Gomes et al. 2008, Silva et al. Some studies have been conducted on the
2003) and yeasts (Faraco & Faraco 1960, Queiroz ecology of bacteria and protozoans in the Patos Lagoon
1972, Loureiro et al. 2005) in these environments. estuary and revealed that the dynamics of the bacterial

Atlântica, Rio Grande, 35(1) 45-54, 2013. DOI: 10.5088/atl.2013.35.1.45. 45

ERICA S. SILVEIRA; RUBENS CÁURIO LOBATO; PAULO CESAR ABREU

community is determined by biological factors such as MATERIAL AND METHODS

phytoplankton primary production and the bacterivory
carried out by protozoans (Abreu et al. 1992). Brepohl et Sites, Sampling and abiotic variables:
al. (1996) followed the biomass variation bacteria, Two sampling sites in the estuary of Patos
flagellates and ciliates during the degradation process of Lagoon (Museum – Oceanographic Museum of FURG,
Scirpus maritimus (macrophyte) leaves, measuring the and of Channel – at the lagoon main outflow channel)
influence of released dissolved organic matter on the and one at Cassino Beach (Beach) (Figure 1) were
community of free and attached bacteria. A large amount visited monthly, between March 2007 and June 2008.
of fungal spores was found during the decomposition of No fungi isolation was conducted in the months of July
three macrophyte species (Spartina alterniflora, Spartina and August 2007 and February and March 2008. At each
densiflora and Scirpus maritimus) in the same region site three samples of 500mL water were collected, using
(Hickenbick et al. 2004). Despite the great ecological sterilized wide mouth glass flasks (5 cm in diameter)
importance and biotechnological potential of fungi and (Wheaton model). Each flask was quickly submerged
yeasts found in aquatic environment little is known about with the mouth down, 30 cm below the surface.
their diversity and abundance in the Brazilian coastal Water temperature (thermometer Incoterm –
region, especially in the Patos Lagoon estuary. 1°– 100ºC), salinity (Hand Refractometer ATAGO S0
Therefore, this study aimed to evaluate the spatial- MILL/-E), pH (pH meter DIGIMED DMPH-3) and water
temporal variability of the fungi and yeasts community in transparency (Secchi Disk) were recorded at each
the Patos Lagoon estuary and adjacent coastal area sampling site. Subsequently, in the laboratory, the
(Cassino Beach) and possible environmental variables concentrations of the dissolved inorganic nutrients
that influence their distribution. phosphate, nitrate+nitrite (Strickland & Parson 1972)
and ammonium (Unesco 1983) were analyzed.

FIGURE 1 – Localization of sampling sites: 1 – Museum 2 – Channel 3. Beach

46 Atlântica, Rio Grande, 35(1) 45-54, 2013. DOI: 10.5088/atl.2013.35.1.45.

 FUNGI IN THE PATOS LAGOON ESTUARY AND CASSINO BEACH

Isolation and identification of fungi and yeasts Statistical analysis

Water samples were centrifuged at 4500 rpm for The averages of biotic and abiotic variables
10 minutes to remove suspended material. between these two periods (April, May and June,
Subsequently, the concentrated material was diluted in 2007 and April, May and June, 2008) were compared
Phosphate Buffer Solution (PBS), pH 7.2, at the ratios by t test. In order to test the association between the
of 1:1, 1:2, 1:3 and 1:4 (Busta et al. 1984). Fungi were number of genera and isolates per genus and abiotic
diluted in PBS (Phosphate Buffer Solution), pH 7.2, variables, a Stepwise multiple regression model was
with serial dilutions (decimal) up to 10-4. Aliquots of applied. Assumptions of the model were verified (Zar
10µl of each dilution were spread on the surface of 1996, Hammer et al. 2001).
plates containing Sabouraud agar with chloramphenicol
0,005% (Acumedia Manufactures, Inc. Lansing, RESULTS
Michigan), and placed in a bacteriological incubator at
25°C (Busta et al. 1984). This operation was repeated Water temperature was similar in the three
in duplicate for each dilution. The cultures were stations and showed a clear seasonal pattern with the
observed daily for up to 07 (seven) days. lowest value (5ºC) in July 2007 and the highest (25ºC)
The identification at the genera level was based in January 2008 (Figure 2A).
on the macro and micro morphology of the filamentous Salinity varied according to the geographic
fungi, Apart from these characteristics, the growth location of each sampling site. At the Beach sampling
velocity (time from sowing to initial view of the colony), site, salinity ranged from 20 to 33, showing lower
mycelium surface appearance and pigmentation of the monthly variations compared to the Channel and
front and back of cultures were also observed Museum sites, where salinity ranged from 0 to 33.
(Alexoupoulos et al. 1996, Barnet & Hunter 1998, Highest values were measured in autumn 2007 and
Putzke & Putzke 2002). The micro-morphological summer 2008. (Figure 2B). The pH level remained
characteristics were verified using the slide culture stable throughout the study, with a slight variation at
technique (Ridell 1950). Yeasts were not identified. each sampling site (7.0 – 8.2).

Atlântica, Rio Grande, 35(1) 45-54, 2013. DOI: 10.5088/atl.2013.35.1.45. 47

ERICA S. SILVEIRA; RUBENS CÁURIO LOBATO; PAULO CESAR ABREU

FIGURE 2 – Water temperature (A) and salinity (B) during experimental period.

48 Atlântica, Rio Grande, 35(1) 45-54, 2013. DOI: 10.5088/atl.2013.35.1.45.

 FUNGI IN THE PATOS LAGOON ESTUARY AND CASSINO BEACH

Ammonium values were similar at the three (40 µM) was measured in December 2007 (Figure 3 B).
sampling sites, with the highest value (65 µM) measured Phosphate values in samples showed different
in October 2007 at the Channel (Figure 3A). The patterns for each site. At the Beach, phosphate varied
concentrations of nitrite+nitrate were low at Beach between 0.75 and 2.0 µM with maximum in October
except for September 2007 (15µM) while the Channel 2007. The site Channel was also highly variations,
sampling site presented high concentrations between with variable between 0.75 and 3.5 µM but the
August (15 µM) and December 2007(40 µM). In the greatest values and variation was verified at the
Museum the highest concentrations of these nutrients Museum sampling site (3.3 µM) (Figure 3C).

FIGURE 3 – Concentrations of ammonium (A), nitrite+nitrate (B) and phosphate (C) during experimental period.

Atlântica, Rio Grande, 35(1) 45-54, 2013. DOI: 10.5088/atl.2013.35.1.45. 49

ERICA S. SILVEIRA; RUBENS CÁURIO LOBATO; PAULO CESAR ABREU

The following genera of filamentous fungi in samples fromApril, May and June 2007. Non-
isolates were found: Alternaria, Aspergillus, sporulated fungi were found in 07 samples with uniform
Aureobasidium, Bispora, Botryoderma, Botryotrichum, values. Penicillium was found in 04 samples, the highest
Cladosporium, Chrysosporum, Helminthosporium, number of isolates in April 2007 (Figure 4A).
Monosporium, Papilospora, Penicillium, Trichoderma, Among the isolated fungal groups, yeasts were
Trichophyton, Actinomycetes and non-sporulated found in 07 of the 11 samples from the site Channel
fungi. The most frequent fungal genera were and the highest occurrence occurred in and May 2007
Aspergillus. and Penicillium. samples, though this distribution was fairly uniform
The highest number of isolates was found at throughout the experimental period (Figure 4B).
Museum (85 isolates) (Figure 4A). The sites of Groups of non-sporulated fungi were found in
Channel and Beach presented similar amounts of 07 samples, showing elevated number of isolates in
isolates, 35 and 39 respectively (Figure 4B and 4C). May, October and December 2007 and June 2008.
Some fungi were characteristic of a single Aspergillus was found in 04 samples, being most
sampling site. For instance, the isolates of prevalent in March 2007(Figure 4B).
Botryotrichum, Cladosporium, Papulospora and The yeasts are among the major isolated fungal
Crysosporium were only found at the Beach sampling groups at the Beach sampling site. They were found
station. The Museum was the only station where in 06 of 09 samples, with the greatest number of
Trichoderma, Helminthosporium, Trichophyton and isolates in June 2007. Non-sporulated fungi were
Botryoderma were isolated; while Mucor was only found in the samples from May to November, showing
isolated at the sampling station Channel the higher the highest number of isolates in September 2007.
number of isolates Aspergillus at Museum was in May The genus Aspergillus was found distributed in 03
2007, though this organism was isolated from this station samples, showing the highest number of isolates in
during almost all the study period. Yeasts were found in October 2007 (Figure 4C).
08 samples at this site and had the highest occurrence

50 Atlântica, Rio Grande, 35(1) 45-54, 2013. DOI: 10.5088/atl.2013.35.1.45.

 FUNGI IN THE PATOS LAGOON ESTUARY AND CASSINO BEACH

FIGURE 4 – Isolates of different genera of the Museum (A), Channel (B) and Beach (C).

Atlântica, Rio Grande, 35(1) 45-54, 2013. DOI: 10.5088/atl.2013.35.1.45. 51

ERICA S. SILVEIRA; RUBENS CÁURIO LOBATO; PAULO CESAR ABREU

The statistical analysis showed significant isolates number between the stations Museum in the
correlation positive between the number of yeast innermost site, and the beach.
isolates and salinity (p = 0.0145) and pH (p = As for the pH, the optimum value for the growth
0.040199). Moreover, significant correlations positive of different types of fungi can vary greatly, but overall,
were found between the number of fungi genera and most of them seem to grow best at pH levels between 4
phosphate (p = 0.00477), nitrate (p = 0.022182) and and 7 (Alexoupoulos et al. 1996). The greatest number
pH (p = 0.024534). of fungi isolated from the sampling stations occurred in
water samples with pH values between from 7 and 7.5.
DISCUSSION The greater number of isolated fungal genera related to
higher levels of ammonia in April, May and June 2007,
The aquatic of fungi community is mainly is probably related to the fact that besides carbon fungi
composed of zoosporic fungi, aquatic hyphomycetes require nitrogen for their growth. For obtaining nitrogen,
(mainly in submerged substrates), some representatives fungi use organic or inorganic sources. The main
of basidiomycetes (usually phases of sexual organic sources are proteins, peptides and amino acids.
reproduction), ascomycetes (including phases of sexual Many fungi, however, obtain nitrogen from inorganic
reproduction) and varying amounts fungi and yeasts of sources such as nitrates and ammonium salts (Cadick
terrestrial origins (Sparrow 1968, Dick 1970). The most et al. 1994, Marzluf 1997).
commonly found taxonomic groups in submerged It is noteworthy the fact that in this study the
substrates are the ascomycetes, basidiomycetes, different sampling sites presented characteristic
chytridiomycetes and uniflagellate zoosporic fungi genera. The sampling station Beach was the only site
(Shearer et al. 2007). Besides, in polluted waters, the where Botryotrichum, Cladosporium Papulospora and
incidence of terrestrial origin fungi and yeasts is quite Crysosporium were found. The Museum was the only
high (Schoenlein-Crusius et al. 2004). site where Trichoderma, Helminthosporium,
In this study we have found 13 genera, being Trichophyton and Botryoderma were observed, while
Aspergillus and Penicillium the most frequent. These Mucor was only found at the Channel. These located
genera were also dominant in the study of fungal occurrences might be explained by the influence of
diversity conducted by Gomes et al. (2008) in the factors such as salinity, temperature, substrates
Casa Caiada Beach, Northeastern, Brazil and were availability and diversity and nutrients in the water, as
related to waters with high salinity and alkaline pH. observed elsewhere (Jones & Alias 1997).
Contaminated sediments in the Santos Bay estuarine For example, Trichoderma was found in Museum
region in Southeastern Brazil presented Penicillium only when salinity was lower than at the other stations.
simplicissimum, Aspergillus terreus, Trichoderma and Regragui & Lahlou (2005) observed that soil salinity
other filamentous fungi (Silva et al. 2003). affects the reproductive capacity of Trichoderma
The highest number of fungal isolates in this harzianum with decrease in sporulation. Papulospora,
study were registered between April and June 2007, which occurred only at the Beach, is mainly associated
and considerably smaller values were observed in the with decomposing plants. This species was also
same period of 2008. The analysis of the abiotic factors registered in a survey for identification of marine fungi in
of the two periods shows, that the salinity and pH Thailand (Gareth et al. 2006).
values were higher in 2008, whereas concentrations of When we tested the association between the
ammonia (Figure 4) were higher in 2007. number of genera and abiotic factors at the three
Salinity is a limiting growth factor of fungi sampling sites, a positive relationship was found with
(Mueller & Bills 2004), especially for those from phosphate concentration. Several studies have shown
freshwater environments. Thus, it is likely that the that an increased concentration of nutrients in the
lowest number of isolates obtained in 2008 is related water leads to a rise in fungal diversity (Sreedevi &
to higher salinity in the estuary and coastal regions. Rosamma 2008, Gullis & Suberkropp 2003a, Gullis &
Another fact that corroborates the effect of salinity in Suberkropp 2003b, Gullis & Suberkropp 2004,
this study was the spatial gradient observed in Pascoal & Cassio 2004). Increasing phosphate

52 Atlântica, Rio Grande, 35(1) 45-54, 2013. DOI: 10.5088/atl.2013.35.1.45.

 FUNGI IN THE PATOS LAGOON ESTUARY AND CASSINO BEACH

concentration was related with an enhanced activity of found in seawater. It seems that in the yeast biology
decomposing substrates by some authors (Sridhar & enables, the colonization of diverse substrates and
Bärlocher 2000, Gullis & Suberkropp 2003a). On the the survival under wide range of salinity and osmotic
other hand, Rosemond et al. (2002) found no effect of pressure, which have made the yeasts one of the
phosphate on the decomposition of leaf in water by most successful organisms in the marine
fungi. Moreover, Fernandes et al. (2009), studied the environment, even at great depths (Bass et al. 2007).
impact of multiple stressors on freshwater fungi and In summary, this study demonstrated the
found that greater exposure to phosphate led to presence of several fungi and yeasts in the waters of
changes in fungal community structure related to its the Patos Lagoon estuary and adjacent coastal area,
diversity and species abundance. with the highest number of fungal isolates in this study
The highest amount of yeasts isolates was found were registered between April and June 2007.
at the Beach sampling site. Furthermore, this study However, we emphasize the necessity of further
revealed a positive association of these organisms with studies on the biology and ecology of these
salinity; and a negative association with pH. Yeasts are organisms.
known to be a normal usual component of the oceanic
biota (Kriss et al. 1967, Fell 1967). The occurrence of ACKNOWLEDGEMENT

yeasts in coastal marine waters is well established

This work was supported by financial resources from
(Meyers & Ahearn 1974, Kohlmeyer & Kohlmeyer 1979), Brazilian National Council for Scientific and Technological
and results from its role in the decomposition of organic Development (CNPq). We thank to the reviewers and the program
substrates, nutrient recycling and biodegradation of postgraduate from Biological Oceanography, Federal University of
Rio Grande (FURG), RS, Brazil.
hydrocarbons (Meyers & Ahearn 1974, Lachance et
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54 Atlântica, Rio Grande, 35(1) 45-54, 2013. DOI: 10.5088/atl.2013.35.1.45.