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Morphological, Molecular, and Ultrastructural Characterization of Rozella Rhizoclosmatii, a New Species in Cryptomycota

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Morphological, Molecular, and Ultrastructural Characterization of Rozella Rhizoclosmatii, a New Species in Cryptomycota fungal biology 121 (2017) 1e10 journal homepage: www.elsevier.com/locate/funbio Morphological, molecular, and ultrastructural characterization of Rozella rhizoclosmatii, a new species in Cryptomycota Peter M. LETCHERa,*, Joyce E. LONGCOREb, C. Alisha QUANDTc, Domingos da Silva LEITEd, Timothy Y. JAMESc, Martha J. POWELLa aDepartment of Biological Sciences, The University of Alabama, Tuscaloosa, AL 35487, USA bSchool of Biology and Ecology, University of Maine, Orono, ME 04469, USA cDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA dDepartamento de Genetica, Evoluc¸ao~ e Bioagentes, Universidade Estadual de Campinas, Campinas, SP, 13082-862, Brazil article info abstract Article history: Rozella is a genus of unwalled endoparasites of a variety of hosts including Oomycota (Stra- Received 10 June 2016 menopiles), Blastocladiomycota and Chytridiomycota (Fungi), and one green alga (Coleo- Received in revised form chaete, Chlorophyceae). It currently includes more than 20 formally described species, 15 August 2016 and no new species of Rozella have been described since 1987. We discovered a new Rozella Accepted 19 August 2016 species parasitizing Rhizoclosmatium globosum (Chytridiales, Chytridiomycota) and investi- Available online 4 September 2016 gated its morphology, ultrastructure, and phylogenetic position. Herein named as Rozella Corresponding Editor: rhizoclosmatii sp. nov., the organism induces hypertrophy of the host. Its zoospore is ultra- Gordon William Beakes structurally similar to that of Rozella allomycis, although it has a unique zoospore ultrastruc- tural feature, a lattice of perpendicular rods about the nucleus. The 18S rDNA molecular Keywords: sequence of R. rhizoclosmatii is similar to that of the previously sequenced ‘Rozella ex Rhizo- Lattice closmatium’. This is the first study to inclusively characterize a new species of Rozella with Morphology morphological, ultrastructural and molecular data. As this is only the second Rozella spe- Nomenclature cies to be examined ultrastructurally, and because it is parasitic on a member of Chytridio- Parasitism mycota and not Blastocladiomycota, this research supports the conservative nature of Taxonomy zoospore ultrastructure to help define the genus. Zoospore ª 2016 British Mycological Society. Published by Elsevier Ltd. All rights reserved. Introduction R. septigena as the lectotype. The genus is characterized by an endobiotic, holocarpic, unwalled, inoperculate thallus Cornu (1872) described the genus Rozella and included four with one or more discharge papillae; zoospores (often elon- species: Rozella monoblepharidis polymorphae Cornu, Rozella rhi- gate) with a single posterior flagellum; and thick-walled, pidii spinosi Cornu, Rozella apodyae brachynematis Cornu, and smooth or spiny resting spores (Sparrow 1960). At present, Rozella septigena Cornu. Clements & Shear (1931) designated more than 20 species have been described, but descriptions * Corresponding author. Tel.: þ1 205 348 8208; fax: þ1 205 348 1786. E-mail addresses: [email protected] (P. M. Letcher), [email protected] (J. E. Longcore), [email protected] (C. Alisha Quandt), [email protected] (D. daS. Leite), [email protected] (T. Y. James), [email protected] (M. J. Powell). http://dx.doi.org/10.1016/j.funbio.2016.08.008 1878-6146/ª 2016 British Mycological Society. Published by Elsevier Ltd. All rights reserved. 2 P. M. Letcher et al. are incomplete for several species. To date, only one species of on nutrient agar plates where we had added discharging Rozella,(Rozella allomycis Foust) has been characterized with host material. This assured that zoospores of host and para- morphological (Foust 1937), ultrastructural (Held 1975) and site were simultaneously present. We observed and recorded molecular data (James et al. 2006). Two strains of Rozella (JEL stages of development with a Nikon Eclipse E400 compound 347 Rozella ex Rhizoclosmatium and Rozella ex Pythium, from microscope and photographed developmental stages with a gross enrichment culture) have been characterized with mo- a Spot RT3 digital camera. Attempts to cryopreserve (Boyle lecular data only (James et al. 2006; Lazarus & James 2015). et al. 2003) the dual culture failed with only the host reviving Rozella is considered a member of the recently erected and after thawing. circumscribed phylum Cryptomycota (M.D.M. Jones & T.A. Richards) emend Karpov & Aleoshin in the superphylum Opis- DNA extraction, purification, and amplification thosporidia Karpov, Aleoshin & Mikhailov (Lara et al. 2010; Jones et al. 2011a, 2011b; Karpov et al. 2014), ¼ Rozellomycota Using a dissecting pin, approximately 100 thalli of Rhizoclosma- Doweld (2013). Cryptomycota encompasses numerous envi- tium globosum infected with the Rozella parasite were individu- ronmentally derived phylotypes as well as species of Rozella ally moved to a centrifuge tube. DNA Extraction was (Lazarus & James 2015) and the amoebae parasites Paramicro- performed using the MO BIO PowerLyzer PowerSoil DNA Isola- sporidium (Corsaro et al. 2014a) and Nucleophaga (Corsaro et al. tion Kit (MO BIO Laboratories) following the manufacturer’s 2014b, 2016). Recent research (Lazarus & James 2015; Corsaro instructions. Amplification of the 18S region of nuclear rDNA et al. 2016) has shown that Rozella strains, the amoebae para- (18S) was obtained using two sets of primers; the Rozella pref- sites, and related environmental DNA sequences occur as erential, Rozella 1F and Rozella 1R (Lazarus & James 2015), and a monophyletic lineage whose constituents derive primarily the eukaryotic specific, SSUI and SSU II (Corsaro et al. 2014b). from soil and freshwater habitats but also from some marine PCR was conducted with the Rozella primers in 25 mL reactions habitats. Karpov et al. (2014) defined boundaries among line- with the following recipe: 0.2 mL ExTaq DNA polymerase m m m ages of the clade which they considered sister to the true (Takara), 10.2 LH2O, 3.2 L Bovine Serum Albumin, 3.2 L m m fungi, erecting the superphylum Opisthosporidia, which com- ExTaq Buffer, 2.6 L ExTaq 2 mM MgCl2, 2.6 L ExTaq 10 mM prises the phyla Cryptomycota, Microsporidia, and Aphelidea. dNTPs, 1 mL each primer, and 1 mL DNA. The thermocycler pro- Expanding our knowledge of the diversity of Rozella, herein tocol for this amplification was 94 C for 3 min; 35 cycles at we report a strain of Rozella isolated from a fen water sample, 94 C for 1 min, 55 C for 30 s, 72 C for 1 min; 72 C for characterize its thallus morphology and zoospore ultrastruc- 7 min. The iProof high fidelity DNA polymerase (Bio-Rad Lab- ture, place it in a molecular phylogenetic context, and desig- oratories) and modified protocol were used for the SSU I/II nate it as a new species, Rozella rhizoclosmatii. This is the first primers with the following recipe for a 12.5 mL reaction: m m m new species of Rozella described since 1987 (Karling 1987) 0.16 L iProof polymerase, 6.84 LH2O, 3 L iProof Buffer, m m m and the first new species characterized on the basis of com- 0.7 L MgCl2, 0.3 L 2.5 mM dNTPs (Qiagen), 0.25 L each bined morphological, ultrastructural and molecular data. As primer, and 1 mL DNA. The PCR conditions were as follows: this is only the second Rozella species to be examined ultra- 98 C for 3:00 min; 35 cycles at 98 C for 30 s, 55 C for 30 s, structurally, and because it is parasitic on a member of Chytri- 72 C for 1:00; 72 C for 7 min. PCR products were purified using diomycota and not Blastocladiomycota, this research ExoSAP (Promega) and sequenced at the University of Michi- supports the conservative nature of zoospore ultrastructure gan DNA Sequencing Core. A consensus sequence of the prod- to help define the genus. ucts from both sets of primers was then generated and used in downstream phylogenetic analyses. Materials and methods Phylogenetic analysis Isolation and light microscopy A sequence of 18S of JEL 863 was added to a database including 18S from isolates and sequences included in Fig 2, clade XII in In the summer of 2015 we collected Sphagnum and organic de- Lazarus & James (2015) plus the Rozella ex Rhizoclosmatium bris monthly from the fen edge of Perch Pond (Penobscot clade and additional related isolates. Combined sequences County, Maine, USA), baited collections with spruce pollen were aligned with Clustal X (Thompson et al. 1997) and manu- and chitin, and surveyed for Rozella spp. Rhizoclosmatium globo- ally edited in BioEdit (Hall 1999). The combined data had 1267 sum, which had previously been found to be a host of Rozella characters with 219 parsimony informative sites after unin- (James et al. 2006), was consistently present on baits but we formative characters were excluded in PAUP* (Swofford found it infected with Rozella only from our Aug. 10 collection. 2002). Maximum parsimony (MP) phylogenetic trees were con- We brought the host and parasite into dual culture (desig- structed with PAUPRat (Sikes & Lewis 2001) and support À nated as JEL 863) on mPmTG (0.4 g L 1 peptonized milk, values were generated as heuristic searches with 500 repli- À À À 0.4 g L 1 tryptone, 2 g L 1 glucose, 10 g L 1 agar with cates, each with 10 random-addition replicates. Maximum À À 200 mg L 1 Penicillin G and 200e500 mg L 1 Streptomycin likelihood (ML) trees were constructed as described in Velez added after autoclaving). To facilitate infection of the host in et al. (2011). MrModeltest 2.3 (http://mrmodeltest.joydown- numbers great enough to harvest for transmission electron load.com/) was used to determine the best fit model of base microscopy and molecular analysis we examined infected substitution, and GARLI 0.951 (Zwikl 2006) was used to identify material with a stereo microscope (40Â) and, with a sterile the ML tree. ML branch support was assessed with 500 boot- needle, picked up and moved mature infected thalli to areas strapping replicates. Sequence similarity between isolates of A new species in Cryptomycota 3 interest was assessed via pairwise alignment in BioEdit.
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