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Isospora Svecica Sp. N. (Apicomplexa: Eimeriidae), a New Species Of

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Isospora Svecica Sp. N. (Apicomplexa: Eimeriidae), a New Species Of Parasitology Research (2019) 118:3043–3051 https://doi.org/10.1007/s00436-019-06397-5 PROTOZOOLOGY - ORIGINAL PAPER Isospora svecica sp. n. (Apicomplexa: Eimeriidae), a new species of coccidium from the white-spotted bluethroat Luscinia svecica cyanecula (Aves: Passeriformes: Muscicapidae) Aneta Trefancová1 & Jana Kvičerová1 Received: 10 April 2019 /Accepted: 8 July 2019 /Published online: 30 August 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Using a combination of morphological and molecular data, we describe a new apicomplexan parasite, Isospora svecica sp. n., from the white-spotted bluethroat, Luscinia svecica cyanecula, from the Czech Republic. Oocysts were found in its intestinal tract. Sporulation was exogenous and took 1–3 days. The oocysts were slightly ellipsoidal, of average size 26.17 × 20.33 μm, with a smooth bilayered wall. Micropyle, oocyst residuum, and polar granules were absent. Sporocysts were bottle-shaped, of an average size of 18.82 × 8.82 μm, with a thin, colourless wall. A conspicuous knob-like Stieda body was present. Substieda body was barely visible. Sporocyst residuum was present in the form of granules of various sizes. Sporozoites were banana-shaped and contained large anterior and small posterior refractile bodies. Partial DNA sequences of three genes were obtained from oocysts of Isospora svecica sp. n., being most closely related to other isosporans described from passerines. Little is known about the parasites of the avian family Muscicapidae, including coccidia, a highly prevalent parasitic protist group in all vertebrate classes. Only six species of the genus Isospora have so far been described in Muscicapidae, together with several “Isospora sp.” that in fact most likely represent Isospora lacazei. The newly described Isospora svecica sp. n. differs morphologically from other coccidia reported from muscicapid birds, and represents the first coccidian species described from Luscinia svecica. Keywords Coccidia . Isospora . Aves . Muscicapidae . Morphology . Phylogeny Introduction revealed that the Isospora-type oocysts with SB found in the faeces of some carnivores and rodents are only The oocysts of Isospora (Apicomplexa: Coccidia: pseudoparasites, probably originating in avian hosts Eimeriorina) are often found in the faeces of various species (Barnard et al. 1974;Ernstetal.1969;Ghimire2010; of birds. For a long time, the origin of Isospora-type oocysts Levine and Mohan 1960; Trefancová et al. 2019). has been the subject of much discussion and controversy. About 150 species of Isospora have so far been described Several decades ago, the genus Isospora was split into the from passerine birds. The majority of these descriptions are genera Isospora (Eimeriidae) characterized by possessing a based solely on oocysts found in avian faeces. For most of Stieda body (SB) and infecting mainly birds and reptiles, them, molecular data are lacking. and Cystoisospora (Sarcocystidae) lacking a SB and infecting Luscinia svecica (Linnaeus, 1758) (Aves: Passeriformes: mainly mammals (Frenkel 1977; Carreno and Barta 1999; Muscicapidae) includes 10 subspecies, occurring mainly in Franzen et al. 2000; Barta et al. 2005). Moreover, it has been Asia and Europe. Two subspecies have been reported to nest in the Czech Republic, L. svecica svecica (Linnaeus, 1758) and L. svecica cyanecula (Meisner, 1804). The white- Section Editor: Panagiotis Karanis spotted bluethroat L. svecica cyanecula is a small songbird that inhabits moist areas around ponds, reed beds, sedges, * Aneta Trefancová and willows of central and southern Europe. It is a migratory [email protected] bird returning in March and April after overwintering on the Iberian Peninsula and in northern and central Africa 1 Department of Parasitology, Faculty of Science, University of South (Correia and Neto 2013). This subspecies nests twice a year, Bohemia, Branišovská 1760, 370 05 České Budějovice, Czech Republic and feeds mainly on insects and invertebrates from the 3044 Parasitol Res (2019) 118:3043–3051 ground or in clumps of vegetation, and sometimes also on Molecular and phylogenetic analyses berries. It is an endangered species within the Czech Republic, according to Czech legislation (no. 114/1992 Sb). In compar- Isosporan genomic DNA was extracted from the faecal mate- ison to its biology and ecology, little is known about its para- rial using the FastDNA® SPIN for Soil Kit (MP Biomedicals, sites. Studies on the parasitofauna not only of L. svecica but LLC, Santa Ana, CA, USA) following the manufacturer’s also of other members of the family Muscicapidae— protocol. One-step PCR was performed using the coccidia- representing an assemblage of 275 species in 48 genera—are specific primers ssuF 5′-GAAACTGCGAATGGCTCATT-3′ limited to a few reports, mostly concerning blood protists and ssuR 5′-CTTGCGCCTACTAGGCATTC-3′ amplifying (Plasmodium and Haemoproteus)(Kučera 1981; Paperna the gene encoding the small subunit of 18S rRNA, coiF 5′- et al. 2010; Sebaio et al. 2012;Peevetal.2016; Valkiūnas GGTTCAGGTGTTGGTTGGAC-3′ together with coiR 5′- et al. 2017), or helminths (Georgiev et al. 2004;Mutafchiev ATCCAATAACCGCACCAAGAG-3′ amplifying the mito- et al. 2013, 2014). To date, neither species of Isospora nor any chondrial gene for cytochrome c oxidase subunit I (COI), other coccidium have been described from L. svecica. and coiiiF 5′-AGAAAACCTAAAATCATCATGT-3′ together This study presents a morphological description of the with coiiiR 5′-AAGTGAGTTCGCATGTTTAC-3′ amplify- infective oocyst stage, molecular sequence data, and phy- ing the mitochondrial gene for cytochrome c oxidase subunit logenetic analyses of the Isospora from the faeces of the III (COIII). Primers for 18S rDNA and COI were adopted White-spotted Bluethroat L. svecica cyanecula from the from Schwarz et al. (2009) and Kvičerová et al. (2008), re- Czech Republic, which we conclude is a new species. spectively. Sequences of primers amplifying the COIII region were provided by John R. Barta (University of Guelph, Ontario, Canada). Each PCR reaction contained 2.5 μlof 10 × PCR buffer (containing 15 mM MgCl2;Qiagen, Materials and methods Hilden, Germany), 2 μl of extracted DNA, 1 μl of dNTPs (10 mM solution), 0.5 μl of each primer (25 pmol/μl; Generi Origin of the sample and coprological examination Biotech, Hradec Králové, Czech Republic), 0.2 μlof HotStarTaq Plus DNA Polymerase (Qiagen, Hilden, A single, deceased individual of the white-spotted Germany), and 18.3 μl of PCR H2O. After visualization on bluethroat, L. svecica cyanecula, was recently found in 1% agarose gel, the PCR products of expected sizes were the vicinity of the village Lužnice, 49.0772158 N, enzymatically purified with alkaline phosphatase and exonu- 14.7550169 E (South Bohemia, Czech Republic). The clease I (Thermo Fisher Scientific, Waltham, MA, USA), and bird was dissected and its intestinal tract (small intestine sequenced via the Sanger sequencing method in SEQme, s.r.o. to cloaca) was removed. Subsequently, this part of intes- (Dobříš, Czech Republic). tine with its faecal contents was placed in a 4% potassium The sequences of Isospora svecica sp. n. were examined by dichromate (K2Cr2O7) solution. The sample was stored at the BLAST algorithm (https://blast.ncbi.nlm.nih.gov/Blast. room temperature with access to air for 3 days. It was cgi) and further edited using the Sequence Scanner v2.0 then examined for the presence of coccidia by (Applied Biosystems), EditSeq 5.05, and SeqMan 5.05 centrifugation-flotation technique using a modified (DNASTAR, Inc., Madison, WI, USA) programmes. Sheather’s sugar solution (specific gravity 1.3) (Sheather Alignments were created in Geneious v9.1.3 (http://www. 1923; Modrý et al. 2015) and light microscopy. geneious.com;Kearseetal.2012). The coccidian sequences of 18S rRNA, COI, and COIII genes (mainly sequences of Isospora spp.) obtained from the NCBI GenBank database Morphological and morphometrical analyses (https://www.ncbi.nlm.nih.gov/genbank/) and during our previous studies, together with the newly obtained Detected oocysts of Isospora svecica sp.n.were sequences of our sample, were used in phylogenetic examined and described based on the morphological and analyses. The accession numbers of all sequences used in morphometrical analyses of sporulated oocysts according the analyses are shown on the resultant phylogenetic trees. to Duszynski and Wilber (1997)andBertoetal.(2014). Phylogenetic relationships were reconstructed using Fully sporulated oocysts were measured and photographed using Nomarski interference contrast on an Olympus BX53 light microscope equipped with an Fig. 1 Phylogenetic relationships inferred by the BI analysis of the 18S Olympus DP73 digital camera and Olympus cellSens rDNA sequences. Numbers at the nodes show posterior probabilities Standard 1.13 imaging software. A line drawing was cre- under the BI analysis/bootstrap values derived from ML analysis; poste- rior probabilities and bootstrap supports lower than 0.50 or 50%, respec- ated using the CorelDRAW X7 graphics suite version tively, are marked with dash (-). The family Sarcocystidae is used as an v17.0.0.491. outgroup Parasitol Res (2019) 118:3043–3051 3045 Hammondia hammondi KT184369 Toxoplasma gondii XR_001974441 1/100 H. heydorni JX220987 1/53 Cystoisospora sp. ex Meles meles KU198329 Cystoisospora canis KT184362 0,9/- C. felis KT184364 Sarcocysdae 1/92 Cystoisospora sp. ex Felis sylvestris f. catus AB519675 EU200792 (Cystoisospora spp., 1/99 C. moni C. suis U97523 Hammondia
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