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Five New Species of Yeasts from Fresh Water and Marine Habitats in the Florida Everglades

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Five New Species of Yeasts from Fresh Water and Marine Habitats in the Florida Everglades Antonie van Leeuwenhoek (2011) 99:533–549 DOI 10.1007/s10482-010-9521-6 ORIGINAL PAPER Five new species of yeasts from fresh water and marine habitats in the Florida Everglades Jack W. Fell • Adele Statzell-Tallman • Gloria Scorzetti • Marcelo H. Gutie´rrez Received: 16 August 2010 / Accepted: 5 October 2010 / Published online: 22 October 2010 Ó Springer Science+Business Media B.V. 2010 Abstract Yeast populations in the Shark River sp. nov. (CBS 10880T) in the Rhodosporidium Slough of the Florida Everglades, USA, were exam- toruloides clade (Microbotryomycetes, Sporidiobol- ined during a 3-year period (2002–2005) at six ales) and Cryptococcus mangaliensis sp. nov. (CBS locations ranging from fresh water marshes to marine 10870T) in the Bulleromyces clade (Agaricomycoti- mangroves. Seventy-four described species (33 asco- na, Tremellales). mycetes and 41 basidiomycetes) and an approxi- mately equal number of undescribed species were Keywords Yeast Á New species Á Candida Á isolated during the course of the investigation. Cryptococcus Á Rhodotorula Á Florida Everglades Serious human pathogens, such as Candida tropical- is, were not observed, which indicates that their presence in coastal waters is due to sources of pollution. Some of the observed species were wide- spread throughout the fresh water and marine habi- Introduction tats, whereas others appeared to be habitat restricted. Species occurrence ranged from prevalent to rare. The Everglades, which is the largest subtropical Five representative unknown species were selected wetland in the United States, occurs in the south- for formal description. The five species comprise two eastern state of Florida. The system spans from the ascomycetes: Candida sharkiensis sp. nov. (CBS fresh water Lake Okeechobee south to Florida Bay, 11368T) and Candida rhizophoriensis sp. nov. (CBS which is a lagoonal estuary. Water moves from north 11402T) (Saccharomycetales, Metschnikowiaceae), to south as a slow river that is 97 km wide and over and three basidiomycetes: Rhodotorula cladiensis 160 km long. Over the past 100 years, the water flow sp. nov. (CBS 10878T) in the Sakaguchia clade has been channeled and diverted as South Florida has (Cystobasidiomycetes), Rhodotorula evergladiensis undergone changes to accommodate urban growth and agricultural practices. With national attention to loss of natural environments, attempts are being made J. W. Fell (&) Á A. Statzell-Tallman Á G. Scorzetti Rosenstiel School of Marine and Atmospheric Science, to restore parts of the Everglades ecosystem. Con- University of Miami, 4600 Rickenbacker Causeway, currently, environmental studies are in progress to Key Biscayne, Fl 33149, USA examine the ecological changes that occur during the e-mail: [email protected] restoration process. M. H. Gutie´rrez One of these studies, the Florida Coastal Ever- Universidade de Concepcion, Concepcion, Chile glades Long Term Ecological Research (LTER) is 123 534 Antonie van Leeuwenhoek (2011) 99:533–549 monitoring (http://fcelter.fiu.edu/) the Shark River subtropical moist environment with distinct wet Slough (SRS, Fig. 1), which is a major distributor of (June–Nov) and dry (Dec–May) seasons and a fresh water within the Everglades. The upper reaches seasonally driven freshwater sheet flow. The Shark of the SRS are a fresh water habitat dominated by a River Slough initiates in a fresh water marsh and sawgrass community, whereas the lower reaches are terminates in a mangrove habitat in Florida Bay and characterized by an estuarine mangrove habitat. The the Gulf of Mexico. Collections were made at six sites water sheet flow is seasonally driven with greater (Fig. 1) that are maintained and routinely sampled for intrusions of estuarine waters during the dry season. physical and biological data by the Florida Interna- As part of the LTER studies, we are examining the tional University (FIU) National Science Foundation yeast populations and communities associated with (NSF) Long Term Ecological Research (LTER) the different habitats in the SRS. One of the charac- program. Detailed information for each site can be teristics of the SRS yeast communities is the presence obtained at the Florida Coastal Everglades LTER web of novel species (Statzell-Tallman and Belloch 2008). site: http://fcelter.fiu.edu/. In the following report, a formal description of five Stations SRS 1a, 2 and 3 are located in freshwater new species from the Florida Everglades ecosystem wetlands dominated by sawgrass (Cladium jamai- and their relationships to ecological conditions and cense) interspersed with spike rushes (Eleocharis other members of the yeast community are presented. cellulosa) and maidencane (Panicum hemitomon). Stations SRS 4, 5 and 6 are in the slough with tidally driven oceanic inputs within a habitat of red (Rhizo- Methods phora mangle) and black (Avicennia germinanus) mangrove trees. At SRS 4 the trees have a dwarf Sample collection and isolation stature (*2–4 m high), at SRS 5 an intermediate stature (*6 m), whereas at SRS 6 the trees are tall Sampling sites were in the Shark River Slough (SRS, (*12 m). The tidal influence is apparent from the Fig. 1), which is on the southwest corner of the variations in salinity at the different times of collec- Florida Everglades. The entire region is located in a tion. Specifically, the salinities at the stations over Fig. 1 Location of the six sampling sites (SRS1a-6) in the Shark River Slough in Florida Everglades 123 Antonie van Leeuwenhoek (2011) 99:533–549 535 times of our collections were; SRS 1a: 0 ppt, SRS 2 liquid media. Culture tube lids were tight to avoid and SRS 3: 0–2 ppt, SRS 4: 0–17 ppt, SRS 5: contamination. Based on multiple controls with cells 0–30 ppt and SRS 6: 12–33 ppt. inoculated in tubes with glucose media, neither oxygen Eight collections were taken in the Shark River depletion (as indicated by growth rates) nor gas build Slough. All stations were sampled during five collec- up, were recorded. The tubes were placed on a roller tions: Collection (C) 1-July 2002, C2-November 2002, drum modified to accept the microcentrifuge tubes. C3-February 2003, C4-June 2003 and C8-September Readings were taken after 3 days, 1, 2 and 3 weeks. 2004. The remaining three collections were: C5-October 2003 at station SRS 1a, 2, 3, 4 and 6, C7-April 2004 at Phylogenetic analysis stations SRS 1a and 4, and C9-March 2005 at stations SRS 3, 4, 5 and 6. The samples from inland stations 1a, DNA extraction followed the methods of Fell et al. 2 and 3 were collected from a motorboat or from an (2000). Alternatively, DNA was directly amplified airboat during periods of low water. Within a few days, from a light cell suspension in water, as the DNA stations 4, 5 and 6, which were consistently in deeper template, in 50 ml PCR reactions with a HotMaster water, were sampled from a motorboat. Surface waters Kit (Eppendorf North America, Westbury, NY). (30 cm below the surface) in the SRS were collected in Molecular sequence analysis of the D1/D2 domains sterile, one liter Nalgene bottles. Three samples were of the LSU and the ITS1, 5.8S and ITS2 rRNA gene collected at each station to increase the accuracy of the regions followed the procedures of Fell et al. (2000) estimate of population variability. The samples were and Scorzetti et al. (2002). Trees, based on the D1/D2 kept at 5–12°C until processed, usually within 24 h. LSU rDNA region were constructed based on like- Preliminary sampling results showed widely variable lihood analysis (heuristic search, stepwise addition) total numbers of cfu at each station. Consequently, a with bootstrap values calculated with 1000 replicates. series of aliquots (10, 25, 50 and 100 ml) was filtered through 0.45 lm pore size cellulose acetate Millipore filters for each sample. The filters were placed on Results and discussion enrichment agar in 50 mm Millipore petri dishes. The enrichment medium (5.0 ml) consisted of 2% glucose, Yeasts were isolated from eight collections at six 1% peptone and 0.5% yeast extract agar, with 0.02% stations in the Shark River Slough (SRS) from July chloramphenicol to retard bacterial growth. The plates 2002 to June 2005. Seventy-four previously described were incubated at 17°C. Incubation of samples from species, and an approximately equal number of high nutrient waters require temperatures below undescribed species, were isolated during the course ambient to slow the growth of filamentous fungi, of the investigation. The described species, including which are prevalent in these environments. The the five previously undescribed species that we resulting colonies were counted and streaked onto selected to describe in this study, consisted of 35 enrichment agar for purity within 7–10 days of sample ascomycetes and 44 basidiomycetes (Table 1). The filtration. The isolates were grown in duplicate in 1 ml habitat distribution of these yeast species included of glucose peptone yeast extract (GPY) broth in 2 ml sawgrass stations (Stas. 1a–3): ascomycetes seven microcentrifuge tubes on a roller drum for 24–48 h. species, basidiomycetes 17 spp; mangrove stations A separate collection was made north of the SRS in (Stas 4–6) ascomycetes 15 spp, basidiomycetes 8 spp; the mangroves of the Florida Everglades National mixed sawgrass and mangrove stations ascomycetes Park at Chatham Bend (25°410N, 85°10W) on 10/23/ 13 spp. and basidiomycetes 19 spp. 1996. Many of the species, particularly those species, which were restricted to sawgrass or mangrove Morphological and physiological analyses habitats, were only encountered
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