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Reinvestigation of the Sperm Ultrastructure of Hypoderaeum

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Reinvestigation of the Sperm Ultrastructure of Hypoderaeum Manuscript Click here to download Manuscript Hypoderaeum conoideum Ms ParasitolRes REV.docx Click here to view linked References 1 Reinvestigation of the sperm ultrastructure of Hypoderaeum conoideum (Digenea: 1 2 2 Echinostomatidae) 3 4 5 3 6 7 4 Jordi Miquel1,2,*, Magalie René Martellet3, Lucrecia Acosta4, Rafael Toledo5, Anne- 8 9 6 10 5 Françoise Pétavy 11 12 6 13 14 7 1 Secció de Parasitologia, Departament de Biologia, Sanitat i Medi ambient, Facultat de 15 16 17 8 Farmàcia i Ciències de l’Alimentació, Universitat de Barcelona, Av. Joan XXIII, sn, 08028 18 19 9 Barcelona, Spain 20 21 2 22 10 Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Av. Diagonal, 645, 23 24 11 08028 Barcelona, Spain 25 26 3 27 12 Université Clermont Auvergne, INRA, VetAgro Sup, UMR EPIA Epidémiologie des 28 29 13 maladies animales et zoonotiques, 63122 Saint-Genès-Champanelle, France 30 31 14 4 Área de Parasitología del Departamento de Agroquímica y Medioambiente, Universidad 32 33 34 15 Miguel Hernández de Elche, Alicante, Spain 35 36 16 5 Departament de Farmàcia i Tecnologia Farmacèutica i Parasitologia, Facultat de Farmàcia, 37 38 39 17 Universitat de València, 46100 Burjassot, València, Spain 40 41 18 6 Laboratoire de Parasitologie et Mycologie Médicale, Faculté de Pharmacie, Université Claude 42 43 44 19 Bernard-Lyon 1, 8 Av. Rockefeller, 69373 Lyon Cedex 08, France 45 46 20 47 48 49 21 *Corresponding author: 50 51 22 Jordi Miquel 52 53 23 Secció de Parasitologia, Departament de Biologia, Sanitat i Medi Ambient, Facultat de 54 55 56 24 Farmàcia i Ciències de l’Alimentació, Universitat de Barcelona, Av. Joan XXIII, sn, 08028 57 58 25 Barcelona, Spain. 59 60 61 62 63 1 64 65 26 e-mail: [email protected] 1 2 27 Telephone: +34 93 4024500 3 4 5 28 Fax: +34 93 4024504 6 7 29 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 2 64 65 30 Abstract 1 2 31 Spermatological characteristics of the digenean Hypoderaeum conoideum (Echinostomatidae) 3 4 5 32 collected from Anas platyrhynchos in the Lac d'Annecy (France) were reinvestigated using 6 7 33 transmission electron microscopy. The previous study on this species only describes the 8 9 10 34 presence of two axonemes of unequal lengths, a mitochondrion, a posterior nucleus and the 11 12 35 disposition of cortical microtubules. The present ultrastructural study reveals that the mature 13 14 36 spermatozoon of H. conoideum is a filiform cell, tapered at both extremities. The sperm cell 15 16 17 37 exhibits the characteristics of digenean spermatozoa type V namely two axonemes of the 9+'1' 18 19 38 pattern of trepaxonematan Platyhelminthes, external ornamentation of the plasma membrane 20 21 22 39 associated with cortical microtubules and located in the anterior part of the proximal region of 23 24 40 the sperm cell, lateral expansions, two bundles of parallel cortical microtubules, maximum 25 26 27 41 number of cortical microtubules in the anterior part of the spermatozoon and presence of two 28 29 42 mitochondria. In addition, the sperm cell of H. conoideum shows spine-like bodies and a 30 31 43 posterior extremity with only the nucleus. The ultrastructural characters of the spermatozoon of 32 33 34 44 H. conoideum are compared with those of other digeneans belonging to the superfamily 35 36 45 Echinostomatoidea. 37 38 39 46 40 41 47 Keywords: Hypoderaeum conoideum; Echinostomatidae; Digenea; Sperm characters; 42 43 44 48 Ultrastructure. 45 46 49 47 48 49 50 Introduction 50 51 51 The Echinostomatidae constitutes a large family of digeneans currently including ten 52 53 52 subfamilies and numerous genera basically due to the large range of vertebrates acting as 54 55 56 53 definitive hosts and to their wide geographical distribution (Kostadinova 2005). Hypoderaeum 57 58 54 is a genus included within the subfamily Echinostomatinae. Individuals in this subfamily are 59 60 61 62 63 3 64 65 55 mainly characterized by the presence of a circumoral head collar ventrally interrupted but 1 2 56 uninterrupted at a dorsal level. The present study describes the sperm ultrastructure of 3 4 5 57 Hypoderaeum conoideum, which is the type species of this genus, and parasitizes the intestine 6 7 58 of birds and mammals (Kostadinova 2005). 8 9 10 59 The study of the sperm ultrastructure provides information on a large number of 11 12 60 characters potentially useful to the interpretation of relationships within the Platyhelminthes. 13 14 61 Thus, several researchers have largely studied these characters in different groups such as 15 16 17 62 monogeneans or cestodes and more recently digeneans (Bâ and Marchand 1995; Justine 1991a, 18 19 63 b, 1998, 2001; Levron et al. 2010; Quilichini et al. 2010a, 2011; Bakhoum et al. 2017; Justine 20 21 22 64 and Poddubnaya 2018). 23 24 65 The sperm ultrastructure of Echinostomatoidea is one of the most poorly analysed among 25 26 27 66 Digenean superfamilies. There are only four studies on the spermatozoon, two of them on the 28 29 67 family Fasciolidae (Fasciola gigantica and Fasciola hepatica by Ndiaye et al. 2003, 2004), and 30 31 68 the remaining on the Echinostomatidae (Echinostoma caproni by Iomini and Justine 1997 and 32 33 34 69 Hypoderaeum conoideum by Chen et al. 1996). However, Chen et al. (1996) did not describe 35 36 70 the full ultrastructural organization of H. conoideum spermatozoa, their results were poorly 37 38 39 71 illustrated. In fact, Chen et al. (1996) describes only general characters such as the presence of 40 41 72 two 9+'1' axonemes of unequal lengths, mitochondrion, nucleus and parallel cortical 42 43 44 73 microtubules. Therefore, the aim of the present study is to provide the first complete study on 45 46 74 the spermatozoon of H. conoideum through an accurate analysis of different ultrastructural 47 48 49 75 characters and their organization. 50 51 76 52 53 77 Materials and methods 54 55 56 78 Materials 57 58 59 60 61 62 63 4 64 65 79 Live adult specimens of Hypoderaeum conoideum (Bloch, 1782) were collected from the 1 2 80 digestive tract of a naturally infected mallard duck Anas platyrhynchos Linnaeus, 1758 3 4 5 81 (Anseriformes: Anatidae) captured in the Lac d'Annecy (Saint Jorioz, France) during November 6 7 82 2017. 8 9 10 83 11 12 84 Molecular analyses and specific diagnosis 13 14 85 The specific identification of the adult worms studied herein was performed by molecular 15 16 17 86 analysis as described previously by Georgieva et al. (2014). Genomic DNA was isolated from 18 19 87 an individual worm stored in absolute ethanol using Tteh Realpure Spin Kit (Durviz, Valencia, 20 21 22 88 Spain), according to the manufacturer’s instructions. A partial sequence of the NADH 23 24 89 dehydrogenase subunit 1 (ND1) gene was amplified using the primers NDJ11 (forward; 5'- 25 26 27 90 AGA TTC GTA AGG GGC CTA ATA-3') and NDJ2A (reverse; 5'-CTT CAGCCT CAG CAT 28 29 91 AAT-3') (Morgan and Blair 1995; Kostadinova et al. 2003). The PCR thermocycling profile 30 31 92 comprised initial denaturation at 95 °C for 5 min, followed by 35 cycles (30 s denaturation at 32 33 34 93 94 °C, 20 s primer annealing at 48 °C, and 45 s at 72 °C for primer extension), with a final 35 36 94 extension step of 4 min at 72 °C as described by Georgieva et al. (2014). All PCR reactions 37 38 39 95 were performed with a T100™ Thermal Cycle (Biorad, Hercules, California, USA). PCR 40 41 96 products were visualized on a 1% agarose gel. Sanger sequencing was performed, and 42 43 44 97 chromatograms were inspected visually to resolve any ambiguities. Search of similarities was 45 46 98 performed using BLASTn 47 48 49 99 (https://blast.ncbi.nlm.nih.gov/Blast.cgi?PAGE_TYPE=BlastSearch) and forward and reverse 50 51 100 sequences were aligned using EMBOSS needle tool 52 53 101 (https://www.ebi.ac.uk/Tools/psa/emboss_needle/nucleotide.html). 54 55 56 102 57 58 103 Transmission electron microscopy (TEM) 59 60 61 62 63 5 64 65 104 For the present TEM study, several live adult worms were immediately rinsed with a 0.9% 1 2 105 NaCl solution and fixed in cold (4 °C) 2.5% glutaraldehyde in a 0.1 M sodium cacodylate buffer 3 4 5 106 at pH 7.4 for a minimum of 2 h, rinsed in 0.1 M sodium cacodylate buffer at pH 7.4, post-fixed 6 7 107 in cold (4 °C) 1% osmium tetroxide with 0.9% potassium ferricyanide in the same buffer for 1 8 9 10 108 h, rinsed in Milli-Q water (Millipore Gradient A10), dehydrated in an ethanol series and 11 12 109 propylene oxide, embedded in Spurr's resin and polymerized at 60 °C for 72 h. Ultrathin 13 14 110 sections (60–90 nm thick) at the level of the seminal vesicle were obtained using a Reichert- 15 16 17 111 Jung Ultracut E ultramicrotome. Sections were placed on 200-mesh copper and gold grids. 18 19 112 Sections placed on copper grids were double-stained with uranyl acetate and lead citrate 20 21 22 113 according to the Reynolds (1963) procedure.
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