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Morphological Re-Description and 18 S rDNA Sequence Confirmation of the Pinworm Aspiculuris tetraptera (Nematoda, Heteroxynematidae) Infecting the Laboratory Mice Mus musculus

Rewaida Abdel-Gaber
Rewaida Abdel-Gaber
, 
Fathy Abdel-Ghaffar
Fathy Abdel-Ghaffar
, 
Saleh Al Quraishy
Saleh Al Quraishy
, 
Kareem Morsy
Kareem Morsy
, 
Rehab Saleh
Rehab Saleh
 e 
Heinz Mehlhorn
Heinz Mehlhorn
   | 03 giu 2018
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Article Category: research-article
Pubblicato online: 03 giu 2018
Pagine: 117 - 132
DOI: https://doi.org/10.21307/jofnem-2018-026
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© 2018 Rewaida Abdel-Gaber et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Fig. 1

A–G, Line drawings of different body parts of Aspiculuris tetraptera. A, Lateral view of female worm with mouth opening surrounded by three lips with cephalic papillae (CP) and amphids (AM), muscular esophagus (E), esophageal bulb region (EOB), intestine (IN), rectum (R) with rectal gland (RG), anal opening (AN) and ending with a long tapered tail (T). Note, transverse annulated (TA) cuticle, and the genital system characterized with a uterus filled with numerous eggs (EG), ovijector apparatus (OA), vagina (VA) and vulval opening (VU) surrounded by two fleshy vulval lips (VL). B, Lateral view of male worm with mouth opening surrounded by three lips with cephalic papillae (CP) and amphids (AM), followed by muscular esophagus (E), esophageal bulb region (EOB), intestine (IN), rectum (R) with rectal gland (RG), anal opening (AN), and ending with a long tapered tail (T). Note, transverse annulated (TA) cuticle, and the genital system with testes (TE), cloacal opening (CO) surrounded by precloacal papillae (PCP), adcloacal papillae (ACP), postadcloacal papillae (PACP), median postadcloacal papillae (MPACP), and posterior papillae (PP). C–G, High magnifications of: C, Face view of anterior extremity of female worm mouth opening (MO) surrounded by three lips (L) with cephalic papillae (CP) and amphids (AM) with cervical alae (CA). D, Face view of anterior extremity of male worm mouth opening (MO) surrounded by three lips (L) with cephalic papillae (CP) and amphids (AM) with cervical alae (CA). E, Ovejector region (OA) of female showing vulva opening (VU), two fleshy vulval lips (VL), muscular vagina (VA), and eggs collected (EG) from uterus. F, Posterior end of male worm showing the cloacal opening (CO) with caudal papillae of precloacal papillae (PCP), adcloacal papillae (ACP), postadcloacal papillae (PACP), median postadcloacal papillae (MPACP), and posterior papillae (PP). G, Morula (M) surrounded by egg shell (ES).
A–G, Line drawings of different body parts of Aspiculuris tetraptera. A, Lateral view of female worm with mouth opening surrounded by three lips with cephalic papillae (CP) and amphids (AM), muscular esophagus (E), esophageal bulb region (EOB), intestine (IN), rectum (R) with rectal gland (RG), anal opening (AN) and ending with a long tapered tail (T). Note, transverse annulated (TA) cuticle, and the genital system characterized with a uterus filled with numerous eggs (EG), ovijector apparatus (OA), vagina (VA) and vulval opening (VU) surrounded by two fleshy vulval lips (VL). B, Lateral view of male worm with mouth opening surrounded by three lips with cephalic papillae (CP) and amphids (AM), followed by muscular esophagus (E), esophageal bulb region (EOB), intestine (IN), rectum (R) with rectal gland (RG), anal opening (AN), and ending with a long tapered tail (T). Note, transverse annulated (TA) cuticle, and the genital system with testes (TE), cloacal opening (CO) surrounded by precloacal papillae (PCP), adcloacal papillae (ACP), postadcloacal papillae (PACP), median postadcloacal papillae (MPACP), and posterior papillae (PP). C–G, High magnifications of: C, Face view of anterior extremity of female worm mouth opening (MO) surrounded by three lips (L) with cephalic papillae (CP) and amphids (AM) with cervical alae (CA). D, Face view of anterior extremity of male worm mouth opening (MO) surrounded by three lips (L) with cephalic papillae (CP) and amphids (AM) with cervical alae (CA). E, Ovejector region (OA) of female showing vulva opening (VU), two fleshy vulval lips (VL), muscular vagina (VA), and eggs collected (EG) from uterus. F, Posterior end of male worm showing the cloacal opening (CO) with caudal papillae of precloacal papillae (PCP), adcloacal papillae (ACP), postadcloacal papillae (PACP), median postadcloacal papillae (MPACP), and posterior papillae (PP). G, Morula (M) surrounded by egg shell (ES).

Fig. 2

Phylogenetic tree generated by neighbor-joining analyses of the partial SSU rDNA sequence of Aspiculuris tetraptera and oxyurid species with the strongest BLAST matches and in part with some ascarid species. GenBank accession numbers are given after the species names. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. Oxyurid parasite examined in the present study is bolded.
Phylogenetic tree generated by neighbor-joining analyses of the partial SSU rDNA sequence of Aspiculuris tetraptera and oxyurid species with the strongest BLAST matches and in part with some ascarid species. GenBank accession numbers are given after the species names. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. Oxyurid parasite examined in the present study is bolded.

Nematoda species used in the phylogenetic analysis of Aspiculuris tetraptera in the present study.

Parasite species Order/family Host species Source Accession no. Sequence length (bp) Divergence Percent identity (%)
Cosmocerca japonica Ascaridida/Cosmocercidae Rana ornativentris GenBank LC052782 749 5.2 89.0%
Parascaris equorum Ascaridida/Ascarididae Africa lion and wolf GenBank JN617987 814 5.2 89.0%
Cucullanus extraneus Rhabditida/Cucullanidae Pomacanthus maculosus GenBank KT192060 1,150 4.9 90.0%
Pseudanisakis rajae Rhabditida/Acanthocheilidae Elasmobranchs GenBank JN392470 903 4.9 90.0%
Enterobius vermicularis Oxyurida/Oxyuroidae Human children GenBank HQ646164 2,867 5.2 91.0%
Skrjabinema kamosika Oxyurida/Oxyuroidae Capricornis crispus GenBank AB699691 898 4.9 91.0%
Aspiculuris tianjinensis Oxyurida/Heteroxynematidae Mus musculus domesticus GenBank KT175733 967 3.2 92.0%
Aspiculuris tetraptera Oxyurida/Heteroxynematidae M. musculus domesticus GenBank KT175725 936 1.4 97.0%
Aspiculuris dinniki Oxyurida/Heteroxynematidae Myodes glareolus GenBank KT175736 995 0.6 98.0%
A. tetraptera Oxyurida/Heteroxynematidae M. glareolus GenBank KT175728 954 0.6 98.0%
A. tetraptera Oxyurida/Heteroxynematidae M. glareolus GenBank KT175729 964 0.6 98.0%
A. tetraptera Oxyurida/Heteroxynematidae M. musculus musculus GenBank KJ143615 419 0.1 99.0%
A. tetraptera Oxyurida/Heteroxynematidae M. musculus musculus GenBank KJ143618 419 0.1 99.0%
A. tetraptera Oxyurida/Heteroxynematidae M. musculus musculus GenBank KJ143617 419 0.1 99.0%
A. tetraptera Oxyurida/Heteroxynematidae M. musculus musculus GenBank KJ143616 419 0.1 99.0%
A. tetraptera Oxyurida/Heteroxynematidae M. musculus musculus GenBank EF464551 3,676 0.1 99.0%
A. tetraptera Oxyurida/Heteroxynematidae M. musculus musculus GenBank EU263107 1,032 0.1 99.0%

Main morphological features and measurements of female Aspiculuris tetraptera compared with previous studies.

Related species Aspiculuris ackerti Aspiculuris artigasi Aspiculuris versterae Aspiculuris tetraptera Aspiculuris ackerti A. tetraptera A. tetraptera A. tetraptera Aspiculuris huascaensis Aspiculuris tianjinensis A. tetraptera A. tetraptera A. tetraptera
Parameters Kruidenier and Mehra (1959) Araujo (1965) Hugot (1980) Hugot (1980) Miller and Schmidt (1982) Kohn and Macedo (1984) Pinto et al. (1994) Landaeta-Aqueveque et al. (2007) Falcón-Ordaz et al. (2010) Liu et al. (2012) Khalil et al. (2014) Abdel-Gaber and Fol (2015) (Present study)
Host species Neotoma albigtda Mus musculus Mastomys natalensis M. natalensis Neotoma cinerea Haemulon sciurus M. musculus M. musculus M. musculus Clethrionomys rufocanus M. musculus M. musculus M. musculus
Host locality Coconimo, Arizona Sao Paulo, Brazil Onderstepoort, South Africa Maracay, Venezuela Colorado, Idaho, USA Rio de Janeiro, Brazil Río de Janeiro, Brazil Santiago, Chile Hidalgo, Mexico Tianjin, China Cairo, Egypt Cairo, Egypt Cairo, Egypt
Site of infection Intestine Intestine Caecum Caecum Caecum Intestine Intestine Caecum and upper colon Intestine Intestine Caecum Caecum Caecum and upper colon
Body length 5.5–6.8 (6.2) 3.534–5.394 1.95 1.2 5.46–8.97 (7.41) 3.60–4.61 (4.18) 3.1–3.6 3.53–4.51 (3.53–4.51) 3.024–3.528 (3.219 ± 0.150) 5.38–7.00 (6.46) 3.55–4.12 (3.83 ± 0.403) 3.2–3.6 (3.5 ± 0.1) 2.9–3.4 (3.1 ± 0.1)
Body width 0.197–0.232 (0.210) 0.153–0.234 0.15 0.08 0.225–0.391 (0.330) 0.20–0.30 (0.27) 0.175–0.245 0.230–0.270 (0.260 ± 0.01) 0.099–0.153 (0.120 ± 0.016) 0.282–0.447 (0.352) 0.199–0.288 (0.244 ± 0.062) 0.21–0.26 (0.24 ± 0.01) 0.19–0.23 (0.20 ± 0.01)
Esophageal length 0.290–0.348 (0.317) 0.252–0.336 0.49 0.43 0.305–0.465 (0.387) 0.25–0.29 (0.27) 0.331–0.433 0.400–0.450 (0.425 ± 0.01) 0.312–0.351 (0.322 ± 0.012) 0.417–0.480 (0.461) 0.328–0.382 (0.35 ± 0.038) 0.33–0.39 (0.27 ± 0.01) 0.30–0.34 (0.32 ± 0.01)
Esophageal width 0.042–0.052 (0.044) 0.048–0.057 – – 0.045–0.080 (0.061) – – – – – – 0.17–0.19 (0.18 ± 0.01) 0.14–0.16 (0.15 ± 0.01)
Esophageal bulb length 0.145–0.171 (0.158) 0.129–0.159 0.14 0.16 0.150–0.225 (0.177) 0.12–0.15 (0.13) – 0.140–0.160 (0.152 ± 0.006) 0.090–0.111 (0.103 ± 0.005) 0.123–0.167 (0.152) 0.108 (0.108 ± 0) 0.12–0.15 (0.140 ± 0.01) 0.10–0.13 (0.11 ± 0.01)
Esophageal bulb width 0.068–0–0.087 (0.080) 0.087–0.111 0.095 0.13 0.080–0.150 (0.107) 0.08–0.12 (0.10) – – 0.054–0.087 (0.063 ± 0.008) 0.088–0.137 (0.118) 0.081 (0.081 ± 0) 0.07–0.11 (0.09 ± 0.01) 0.05–0.09 (0.07 ± 0.01)
Distance from anterior extremity Nerve ring 0.155–0.185 (0.168) 0.120–0.168 0.14 0.13 0.162–0.238 (0.202) 0.15 0.158–0.216 0.12–0.162 (0.140 ± 0.013) 0.081–0.0105 (0.093 ± 0.007) 0.121–0.157 (0.134) 0.144–0.147 (0.145 ± 0.002) – 0.078–0.090 (0.085 ± 0.002)
Excretory pore – 0.756–1.056 0.53 0.9 0.82–1.67 (1.10) 0.81–0.89 (0.86) 0.734–0.936 0.860–0.950 (0.888 ± 0.032) 0.555–0.675 (0.590 ± 0.038) 1.09–1.23 (1.17) – – 0.564–0.780 (0.680 ± 0.02)
Vulval opening 2.1–2.5 (2.3) 1.457–2.015 0.85 1.65 1.52–2.89 (2.49) 1.54–2.36 (1.76) 1.1–1.4 1.61  ± 0.038 (1.55–1.67) 1.204–1.428 (1.269 ± 0.066) 2.07–2.43 (2.27) 1.56–1.86 (1.71 ± 0.21) – 1.112–1.630 (1.406 ± 0.03)
Tail length 0.232–0.690 (0.445) 0.444–0.660 0.435 0.55 0.088–0.110 (0.101) 0.36–0.40 (0.39) 0.360–0.486 0.347–0.537 (0.477 ± 0.06) 0.330–0.372 (0.358 ± 0.016) 0.92–1.14 (1.05) 0.382–0.405(0.393 ± 0.016) 0.34–0.48 (0.42 ± 0.01) 0.30–0.42 (0.39 ± 0.01)
Eggs length 0.097–0.106 (0.101) 0.084–0.090 0.09 0.095 0.093–0.110 (0.102) 0.075–0.090 (0.084) 0.72–0.90 0.084–0.092 (0.087 ± 0.005) 0.054–0.069 (0.061 ± 0.003) 0.092–0.096 (0.094) 0.115–0.129 (0.122 ± 0.008) 0.05–0.07 (0.06 ± 0.01) 0.04–0.06 (0.05 ± 0.01)
Eggs width 0.0390.047 (0.044) 0.036–0.039 0.04 0.045 0.038–0.055 (0.045) 0.038–0.051 (0.045) 0.036 –0.053 0.043–0.052 (0.046 ± 0.005) 0.018–0.030 (0.022 ± 0.003) 0.051–0.058 (0.054) 0.054–0.072 (0.06 ± 0.008) 0.03–0.05 (0.04 ± 0.01) 0.02–0.04 (0.03 ± 0.01)

Main morphological features and measurements of male Aspiculuris tetraptera compared with previous studies.

Related species Aspiculuris ackerti Aspiculuris artigasi Aspiculuris versterae Aspiculuris tetraptera A. ackerti A. tetraptera A. tetraptera A. tetraptera Aspiculuris huascaensis Aspiculuris tianjinensis A. tetraptera A. tetraptera A. tetraptera
Parameters Kruidenier and Mehra (1959)Araujo (1965) Hugot (1980) Hugot (1980) Miller and Schmidt (1982) Kohn and Macedo (1984) Pinto et al. (1994) Landaeta-Aqueveque et al. (2007) Falcón-Ordaz et al. (2010) Liu et al. (2012) Khalil et al. (2014) Abdel-Gaber and Fol (2015) (Present study)
Host species Neotoma albigtda M. musculus Mastomys natalensis Mastomys natalensis Neotoma cinerea Haemulon sciurus M. musculus M. musculus M. musculus Clethrionomys rufocanus M. musculus M. musculus M. musculus
Host locality Coconimo, Arizona Sao Paulo, Brazil Onderstepoort, South Africa Maracay, Venezuela Colorado, Idaho, USA Rio de Janeiro, Brazil Río de Janeiro, Brazil Santiago, Chile Hidalgo, Mexico Tianjin, China Cairo, Egypt Cairo, Egypt Cairo, Egypt
Site of infection Intestine Intestine Caecum Caecum Caecum Intestine Intestine Caecum and upper colon Intestine Intestine Caecum Caecum Caecum and upper colon
Body length 4.41–4.87 (4.64) 2.945–3.472 1.59 2.7 3.01–6.35 (5.03) 2.90–3.60 (3.22) 2.4–3.1 2.65–3.95 (3.393 ± 0.427) 2.16–2.69 (2.48 ± 0.172) 3.69– 5.12 (4.69) 2.55–2.57 (2.56 ± 0.014) 2.73–3.87 (3.21 ± 0.1) 2.23–3.29 (2.79 ± 0.1)
Body width 0.162–0.174 (0.168) 0.156–0.180 0.10 0.11 0.137–0.293 (0.236) 0.15–0.20 (0.17) 0.17–0.21 0.17–0.25 (0.202 ± 0.2) 0.078–0.114 (0.096 ± 0.01) 0.204–0.388 (0.307) 0.088 (0.088 ± 0) 0.18–0.23 (0.20 ± 0.1) 0.16–0.20 (0.18 ± 0.1)
Esophageal length 0.264–0.271 (0.267) 0.213–0.243 0.310 0.38 0.260–0.480 (0.343) 0.18–0.27 (0.23) 0.288–0.360 0.320–0.390 (0.375 ± 0.02) 0.291–0.294 (0.272 ± 0.013) 0.343–0.397 (0.384) 0.439–0.450 (0.44 ± 0.007) 0.38–0.45 (0.41 ± 0.1) 0.32–0.40 (0.39 ± 0.1)
Esophageal width 0.039–0.040 (0.039) 0.036–0.054 – – 0.033–0.060 (0.051) – – – – – – 0.06–0.11 (0.08 ± 0.01) 0.05–0.09 (0.07 ± 0.01)
Esophageal bulb length 0.145–0.155 (0.150) 0.105–0.135 0.10 0.14 0.113–0.183 (0.157) 0.10-0.12 (0.11) – 0.110–0.140 (0.133 ± 0.01) 0.090–0.110 (0.097 ± 0.006) 0.074–0.142 (0.122) 0.244 (0.24 ± 0) 0.14–0.19 (0.16 ± 0.1) 0.13–0.17 (0.15 ± 0.1)
Esophageal bulb width 0.071–0.079 (0.075) 0.075–0.096 0.08 0.09 0.065–0.120 (0.090) 0.06–0.08 (0.07) – – 0.040–0.063 (0.051 ± 0.006) 0.059–0.123 (0.098) 0.077–0.088 (0.08 ± 0.007) 0.07–0.09 (0.08 ± 0.01) 0.04–0.07 (0.05 ± 0.01)
Distance from anterior extremity Nerve ring 0.158 0.108–0.144 0.09 0.10 0.150–0.213 (0.186) 0.11–0.13 (0.12) 0.115–0.140 0.115–0.145 (0.129 ± 0.013) 0.072–0.093 (0.080 ± 0.008) 0.116–0.133 (0.123) 0.088 (0.088 ± 0) – 0.065–0.082 (0.078 ± 0.001)
Excretory pore – 0.600–0.876 0.325 0.78 0.69–1.21 (0.96) 0.69–0.78 (0.73) 0.619 0.750 –0.910 (0.854 ± 0.056) 0.495–0.579 (0.545 ± 0.035) 0.93–1.03 (1.01) 0.144–0.147 (0.145 ± 0.002) – 0.392–0.547 (0.491 ± 0.03)
No. of Caudal papillae 11 5 5 5 10 12 12 12 12 12 12 12 12
Tail length 0.238–0.280 (0.259) 0.147–0.183 0.12 0.17 0.049–0.117 (0.092) 0.10-0.12 (0.11) 0.144–0.172 0.162–0.187 (0.178 ± 0.009) 0.075–0.114 (0.102 ± 0.013) 0.181–0.245 (0.220) 0.12–0.144 (0.132 ± 0.01) 0.13–0.15 (0.14 ± 0.1) 0.11–0.14 (0.12 ± 0.1)
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