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Acta Botanica Brasilica Doi: 10.1590/0102-33062020Abb0040 Acta Botanica Brasilica doi: 10.1590/0102-33062020abb0040 Two new species of the industrially relevant genus Absidia (Mucorales) from soil of the Brazilian Atlantic Forest Thalline Rafhaella Leite Cordeiro1 , Thuong Thuong Thi Nguyen2 , Diogo Xavier Lima1 , Suzana Brito Gomes da Silva1 , Catarina Ferreira de Lima1 , Joana D’Arc Alves Leitão1 , Luciana Melo Sartori Gurgel3 , Hyang Burm Lee2 and André Luiz Cabral Monteiro de Azevedo Santiago1* Received: February 11, 2020 Accepted: June 12, 2020 . ABSTRACT During a survey of Mucorales in soil from an upland forest area in Pernambuco, Brazil, two specimens were isolated and characterized based on their morphological, physiological, and molecular data (ITS and LSU rDNA). Phylogenetic analyses of the isolates revealed that the strains URM 8209 and URM 8210 are closely related to species of Absidia. URM 8209 forms conical, subglobose, and strawberry-shaped columellae and the sporangiospores are cylindrical and ellipsoid. URM 8210 produces hemispheric, subglobose, and strawberry-shaped columellae and the sporangiospores are globose, subglobose, ellipsoid, and short cylindrical. Based on evidence obtained through analysis of datasets (LSU and ITS rDNA regions), A. saloaensis sp. nov. (URM 8209) and A. multispora sp. nov. (URM 8210) are proposed here as novel species. A table with morphological characteristics of Neotropical Absidia spp. is provided. Keywords: Cunninghamellaceae, Mucoromyceta, rDNA, soil, taxonomy suspensory cells that have appendages (Hoffmannet al. Introduction 2007; Hoffmann 2010). Among mucoralean species of Absidia that have The genus Absidia is composed of cosmopolitan fungal been studied for their industrial importance, A. coerulea species commonly isolated from soil, herbivorous dung and specimens are capable of transforming saponins decaying substrates (van Tieghem 1878). Species of this that show high yield and regioselectivity to 20 (S)- genus commonly produce sporangiophores in whorls, arising protopanaxatriol (Chen et al. 2007). Absidia glauca performs from stolons that bear apophysate and pyriform sporangia biotransformation of 3-Oxo-Oleanolic acid resulting in with a deliquescent wall. Rhizoids are never opposed to hydroxylated metabolites and both species mentioned sporangiophores (Benny 2001), and columellae may be above are excellent chitosan producers used in food conical, subglobose, or aplanate, frequently showing an processing, antimicrobial production and biotransformation apical projection (van Tieghem 1878; Hoffmann et al. 2007). of steroid products (Abdel-Fattah et al. 1984; Smith et Absidia species reproduce asexually by the formation of al. 1989; Muzzarelli et al. 1994; Brzezowska et al. 1996; sporangiospores and sexually through the formation of Huszcza & Gladysz 2003 Rungsardthong et al. 2006; Dai zygospores within zygosporangia supported by opposite et al. 2009). Absidia griseola has biotransformation 1 Programa de Pós-Graduação em Biologia de Fungos, Departamento de Micologia. Universidade Federal de Pernambuco, 50670-420, Recife, PE, Brazil 2 Environmental Microbiology Lab, Department of Agricultural Biological Chemistry, College of Agriculture and Life Sciences, Chonnam National University, 61186, Gwangju, Korea 3 Instituto Agronômico de Pernambuco, 50761-000, Recife, PE, Brazil * Corresponding author: [email protected] Diagramação e XML SciELO Publishing Schema: www.editoraletra1.com.br Thalline Rafhaella Leite Cordeiro, Thuong Thuong Thi Nguyen, Diogo Xavier Lima, et al. capacity, carrying out microbial hydroxylation of Isolation and purification ofAbsidia spp. progesterone resulting in 14 -hydroxyprogesterone and 6 , 11 -dihydroxyprogesterone (Habibi et al. 2012). Absidia Five milligrams of soil were inoculated directly into Petri α fusca and A. cylindrospora are used in bioremediation dishes containing wheat germ agar culture medium (Benny β α processes due to their ability to degrade polycyclic aromatic 2008) plus chloramphenicol (80 mg.L–1), in triplicate. Growth compounds, such as hydrocarbons (Guiraud et al. 2008). was observed for seven days at room temperature (28 °C) Specimens of A. cylindrospora have also been used for under alternating light and dark conditions. Fragments of biosorption of Cadmiun, Copper and Lead metals under mycelium were removed directly from the Petri dishes under experimental conditions (Albert et al. 2018). a Leica EZ4 stereomicroscope and transferred to malt extract Hesseltine & Ellis (1964; 1966) and Ellis & Hesseltine agar plates (MEA) (Benny 2008). Slides corresponding (1965) monographed the genus Absidia and grouped its to the holotypes of A. saloaensis sp. nov. (URM 94180) species based on the shape of sporangiospores. Later, in and A. multispora sp. nov. (URM 94181) where deposited a molecular-physiology and micromorphology study of in the Herbarium URM of the Universidade Federal de Absidia, Hoffmann et al. (2007) showed that the species Pernambuco. Ex-type living cultures of A. saloaensis sp. of this genus basically consisted of three groups separated nov. (URM 8209) and A. multispora sp. nov. (URM 8210) according to the growth temperatures: (1) mesophilic where deposited in the culture collection Micoteca URM species, with ideal growth between 25 and 34 °C (includes all currently accepted Absidia s.s species), (2) mycoparasite of the Universidade Federal de Pernambuco. Pure cultures species of other mucoralean fungi, with optimal growth were also deposited in the culture collection (CNUFC) of between 14 and 25 ºC (species after being transferred to the Environmental Microbiology Laboratory Fungarium, Lentamyces), and (3) thermotolerant species, with optimal Chonnam National University, Gwangju, Korea (A. saloaensis growth between 37 and 45 °C [species after being transferred sp. nov. CNUFC B190012 and A. multispora sp. nov. CNUFC to Lichtheimia by Hoffmann et al. (2009)]. In the last 10 B190013). years, six new Absidia species have been reported worldwide: A. caatinguensis, A. jindoensis, A. koreana, A. panacisoli, A. Growth experiments stercoraria, and A. terrestris (Ariyawansa et al. 2015; Li et al. 2016; Crows et al. 2018; Wanasinghe et al. 2018; Zhang Pure cultures were grown in triplicates in MEA and et al. 2018). potato dextrose agar (PDA) and incubated at 15, 20, 25, 28, During a survey on the diversity of mucoralean 30, and 35 °C for 15 days. For morphological identification, fungi in soils of upland forest fragments in the semiarid fragments were removed from the cultures and observed area of Brazil, two specimens of Absidia that varied under a stereomicroscope (Carl Zeiss Axioscope 40) and light microscope (Leica DM500). The color designation of morphologically and genetically in comparison with the colonies was performed according to previous literature the other species of the same genus were isolated. (Maerz & Paul 1950). Based on morphological, physiological, and molecular analyses (LSU and ITS rDNA regions), two new species Molecular analysis (DNA extraction, amplification, of Absidia are being proposed here. cloning and sequencing) Materials and methods Genomic DNA was extracted from fresh fungal mycelia that were grown on cellophane at 25 °C for four days using Sampling sites the SolgTM Genomic DNA Preparation Kit (Solgent Co. Ltd., Daejeon, Korea) according to the manufacturer’s Soil samples were collected from the Brejo Nature instructions with a few modifications. The modifications o Reserve (09º00.418´ S 036º46.898´ W) located in Saloá included the DNA precipitated overnight at -20 C using municipality, Pernambuco State, Brazil. The average annual an equal volume of ice-cold 100 % isopropanol and the temperature in this region is 20 ºC, with the rainy season DNA pellet was washed twice using 500 μL of ice-cold beginning in January/February and ending in September/ 70 % ethanol. The rDNA ITS region was amplified using October and precipitation ranging between 0 to 50 mm in the ITS1 and ITS4 primers (White et al. 1990), and LROR the driest months and 50 to 100 mm in the wettest months. and LR3 were used to amplify the large subunit (LSU) The vegetation is a predominant trait of the species of the rDNA (Vilgalys & Hester 1990; Rehner & Samuels 1995). Atlantic ombrophilous and semi-deciduous forests, being The PCR products were purified using an Accuprep PCR found in the herbaceous areas composed of litter, shrubby Purification Kit (Bioneer Corp.). PCR products of the LSU vegetation, grasses, and shrubs. The soil has a podzolic region were used for direct sequencing on the ABI PRISM characteristic, with areas ranging from being clayey to 3730XL Genetic Analyzer (Applied Biosystems, California, containing granite blocks (Silva-Júnior et al. 2012). USA) (Macrogen, Daejeon, Korea). 550 Acta Botanica Brasilica - 34(3): 549-558. July-September 2020 Diagramação e XML SciELO Publishing Schema: www.editoraletra1.com.br Two new species of the industrially relevant genus Absidia (Mucorales) from soil of the Brazilian Atlantic Forest Since direct sequencing of the ITS region from PCR (GenBank accession numbers: KR030062 and KR030056), products was unsuccessful, PCR products were cloned respectively. using the pGEM-T Easy Vector System (Promega) cloning kit, following the manufacturer’s instructions. These Taxonomy clones were sequenced using primers M13F forward (5’- GTAAAACGACGGCCAGT-3’) and M13R-pUC reverse Absidia multispora T.R.L. Cordeiro, D.X. Lima, Hyang (5’-CAGGAAACAGCTATGAC-3’) by ABI PRISM 3730XL B. Lee & A.L. Santiago sp. nov. (Fig. 2A-I). Genetic Analyzer. Etymology:
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