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Mitochondrial and Nuclear Ribosomal DNA Dataset Supports That Paramphistomum Leydeni (Trematoda: Digenea) Is a Distinct Rumen Fl

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Mitochondrial and Nuclear Ribosomal DNA Dataset Supports That Paramphistomum Leydeni (Trematoda: Digenea) Is a Distinct Rumen Fl Ma et al. Parasites & Vectors (2015) 8:201 DOI 10.1186/s13071-015-0823-4 RESEARCH Open Access Mitochondrial and nuclear ribosomal DNA dataset supports that Paramphistomum leydeni (Trematoda: Digenea) is a distinct rumen fluke species Jun Ma1,2, Jun-Jun He1, Guo-Hua Liu1, Dong-Hui Zhou1, Jian-Zhi Liu3, Yi Liu2 and Xing-Quan Zhu1,2,4* Abstract Background: Rumen flukes parasitize the rumen and reticulum of ruminants, causing paramphistomiasis. Over the years, there has been considerable debate as to whether Paramphistomum leydeni and Paramphistomum cervi are the same or distant species. Methods: In the present study, the complete mitochondrial (mt) genome of P. leydeni was amplified using PCR-based sequencing and compared with that of P. cervi. The second internal transcribed spacer (ITS-2) of nuclear ribosomal DNA (rDNA) of P. leydeni specimens (n = 6) and P. cervi specimens (n = 8) was amplified and then sequenced. Phylogenetic relationship of the concatenated amino acid sequence data for 12 protein-coding genes of the two rumen flukes and selected members of Trematoda was evaluated using Bayesian inference (BI). Results: The complete mt genome of P. leydeni was 14,050 bp in size. Significant nucleotide difference between the P. leydeni mt genome and that of P. cervi (14.7%) was observed. For genetic divergence in ITS-2, sequence difference between P. leydeni and P. cervi was 3.1%, while no sequence variation was detected within each of them. Phylogenetic analysis indicated that P. leydeni and P. cervi are closely-related but distinct rumen flukes. Conclusions: Results of the present study support the proposal that P. leydeni and P. cervi represent two distinct valid species. The mt genome sequences of P. leydeni provide plentiful resources of mitochondrial markers, which can be combined with nuclear markers, for further comparative studies of the biology of P. leydeni and its congeners from China and other countries. Keywords: Paramphistomum leydeni, Paramphistomum cervi, Mitochondrial genome, Nuclear ribosomal DNA, Phylogenetic analysis Background require aquatic snails as intermediate hosts and the pre- Species of Paramphistomum (Trematoda: Digenea), known parasitic stages of miracidia and stages in snails (sporocyst, as the ‘rumen flukes’ or ‘amphistomes,arethepathogensof’ redia and cercaria) are similar to those of liver flukes, such paramphistomiasis of ruminants, such as cattle, buffalo, as Fasciola hepatica [13]. Cercaria escape from snails and sheep, goat and deer [1-5]. Although rumen flukes are con- attach to aquatic plants forming infectious metacercaria. sidered neglected parasites, they are widely distributed in Ruminants acquire infection through ingestion of infectious many continents of the world, (e.g., Asia, the Americas, metacercaria attached to plants. Infection with adult Para- Europe, Africa and Oceania) [1,2,4,6-12]. Rumen flukes mphistomum can cause chronic clinical signs, such as ema- ciation, anemia, diarrhea and edema [8]. The immature paramphistomes might migrate through intestine towards * Correspondence: [email protected] 1State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of rumen, reticulum, abomasums, bile duct and gallbladder. Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research The migration could lead to significant morbidity in rumi- Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province nants, even death. 730046, PR China 2College of Veterinary Medicine, Hunan Agricultural University, Changsha, Paramphistomum leydeni and Paramphistomum cervi Hunan Province 410128, PR China are common rumen flukes in many countries [1,2], Full list of author information is available at the end of the article © 2015 Ma et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Ma et al. Parasites & Vectors (2015) 8:201 Page 2 of 9 particularly in Argentina [3]. Various host animals are Sichuan Province; and Shaoyang City, Hunan Province, often infected concurrently with P. leydeni, P. cervi and China. Samples were washed in physiological saline exten- other paramphistomums globally, and the host or geo- sively, fixed in 70% (v/v) ethanol and preserved at −20°C graphical preference of the two rumen flukes has not been until use. documented. In spite of the economic loss and morbidity Because the specimens were kept in 70% ethyl alcohol, it of paramphistomiasis, over the years, there has been a sig- was difficult to acquire the accurate morphological data of nificant controversy as to whether P. leydeni and P. cervi the paramphistomums, thus molecular identification was represent the same or distinct fluke species. The tax- performed to ascertain the identities of the two para- onomy of P. leydeni and P. cervi is still unclear [1]. Al- mphistomums. Total genomic DNA of each sample was though the amphistome species are morphologically very extracted separately by sodium dodecyl sulfate (SDS)/pro- similar [2], reports have documented that P. leydeni and teinase K digestion system [24] and mini-column purifica- P. cervi are morphologically distinct species based on mor- tion (Wizard-SV Genomic DNA Purification System, phological features of the adult (e.g., genital opening type, Promega) according to the existing instructions. pharynx type, ventral pouch and tegumental papillae ab- ITS-2 rDNA of individual Paramphistomum speci- sent or present) [13,14]. Furthermore, some studies have mens was amplified by PCR and sequenced according to shown that Cotylophoron cotylophorum was re-classified established methods [25-27], and the identity of individ- as P. leydeni [1,2,5]. P. leydeni,aswellasParamphisto- ual Paramphistomum specimens was ascertained by mum hiberniae, Paramphistomum scotiae and Cotylo- comparison with corresponding sequences available in phoron skriabini, was regarded as established synonym of GenBank [2]. P. cervi [5,14-17]. Molecular tools, using genetic markers in mitochon- Long-range PCR-based sequencing of mt genome drial (mt) DNA and in the internal transcribed spacer The primers (Table 1) were designed to relatively con- (ITS) regions of nuclear ribosomal DNA (rDNA), have served regions of mtDNA nucleotide sequences from been used effectively to identify trematode species P. cervi and other closely-related taxa. The mt DNA was [18-21]. For rumen flukes, Yan et al. (2013) reported that amplified from one specimen of P. leydeni collected from mtDNA might be an useful molecular marker for studies a goat in Nimu County, Tibet Autonomous Region, China. of inter- and intra-specific differentiation of the Para- The full mt genome of P. leydeni was amplified in 4 over- mphistomidae [21]. Additionally, the ITS-2 rDNA has lapping long fragments between cox3andatp6(approxi- also proved to be a valuable marker for identification of mately 3.5 kb), between atp6tocox1 (approximately 4 kb), amphistomes [1,2]. Advancements in long PCR-coupled between cox1torrnS (approximately 2.6 kb) and between sequencing and bioinformatic methods are providing ef- rrnLtocox3 (approximately 5.5 kb) (Table 1). PCR reac- fective approaches to probe into the biology of these para- tions were conducted in a total volume of 50 μlusing sites [22,23]. Therefore, in the present study, the complete 4 mM MgCl2, 0.4 mM each of dNTPs, 5 μl10×LATaq mt genome of P. leydeni, and ITS-2 rDNA sequences of buffer, 5 mM of each primer, 0.5 μl LA Taq DNA polymer- P. leydeni and P. cervi were sequenced, analyzed and com- ase (Takara, Dalian, China) and 2 μl DNA templates in a pared to test the hypothesis that P. leydeni and P. cervi are thermocycler (Biometra, Göttingen, Germany). The PCR two genetically distinct species. cycling conditions began with an initial denaturation at 92°C for 2 min, then 12 cycles of denaturation at 92°C for Methods 20 s, annealing at 55–62°C for 30 s and extension at 60°C Ethics statement for 3–5min,followedby92°Cdenaturationfor2min,plus This study was approved by the Animal Ethics Commit- 28 cycles of 92°C for 20 s (denaturation), 55–62°C for 30 s tee of Lanzhou Veterinary Research Institute, Chinese (annealing) and 66°C for 3–5 min, with 10 min of the final Academy of Agricultural Sciences. Adult specimens of extension at 66°C. A cycle elongation of 10 s was added Paramphistomum were collected from bovids and for each cycle. A negative control containing nuclease-free caprids, in accordance with the Animal Ethics Procedures water was included in every amplification run. Each ampli- and Guidelines of the People’s Republic of China. con (4 μl) was evidenced by electrophoresis in a 1.2% agar- ose gel, stained with Gold View I (Solarbio, Beijing, China) Parasites, total genomic DNA extraction and the and photographed by GelDoc-It TSTM Imaging System ascertainment of specimen identity (UVP, USA). Amplified products were sent to Genewiz Adult specimens of Paramphistomum were collected, Company (Beijing, China) for sequencing using ABI3730 post-mortem, from the rumens of naturally infected sequencer from both directions using the primer walking goats in Nimu County, Tibet Autonomous Region; from strategy [28]. Sequencing results
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