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Morphological, morphometrical, and molecular characterization of Metarhabditis amsactae (Ali, Pervez, Andrabi, Sharma and Verma, 2011) Sudhaus, 2011 (Rhabditida, Rhabditidae) from India and proposal of Metarhabditis longicaudata as a junior synonym of M. amsactae

Aashaq Hussain Bhat
Aashaq Hussain Bhat
, 
Shreyansh Srivastava
Shreyansh Srivastava
, 
Aasha Rana
Aasha Rana
, 
Ashok Kumar Chaubey
Ashok Kumar Chaubey
, 
Ricardo A. R. Machado
Ricardo A. R. Machado
 y 
Joaquín Abolafia
Joaquín Abolafia
   | 14 dic 2020
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Publicado en línea: 14 dic 2020
Páginas: 1 - 23
DOI: https://doi.org/10.21307/jofnem-2020-116
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© 2020 Aashaq Hussain Bhat et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

Figure 1:

Metarhabditis amsactae (Ali, Pervez, Andrabi, Sharma and Verma, 2011) Sudhaus, 2011 (line drawing). A: Anterior region; B: Cephalic region; C: Anterior branch of the female reproductive system; D: Entire female; E: Entire male; F: Female posterior region; G: Male posterior region.
Metarhabditis amsactae (Ali, Pervez, Andrabi, Sharma and Verma, 2011) Sudhaus, 2011 (line drawing). A: Anterior region; B: Cephalic region; C: Anterior branch of the female reproductive system; D: Entire female; E: Entire male; F: Female posterior region; G: Male posterior region.

Figure 2:

Metarhabditis amsactae (Ali, Pervez, Andrabi, Sharma and Verma, 2011) Sudhaus, 2011 (light microscopy). A: Anterior region (arrow pointing to the excretory pore); B: Cephalic region; C: Vagina region; D: Female posterior region (black arrow pointing to the anus, white arrow pointing to the phasmid); E: Anterior branch of the female reproductive system (black arrow pointing to the spermatheca); F-J: Male posterior region in lateral (F-I) and ventral (J) views, at spicules (F, H) and bursa (G, I) level (black arrows pointing to the genital papillae, white arrows pointing to the phasmids).
Metarhabditis amsactae (Ali, Pervez, Andrabi, Sharma and Verma, 2011) Sudhaus, 2011 (light microscopy). A: Anterior region (arrow pointing to the excretory pore); B: Cephalic region; C: Vagina region; D: Female posterior region (black arrow pointing to the anus, white arrow pointing to the phasmid); E: Anterior branch of the female reproductive system (black arrow pointing to the spermatheca); F-J: Male posterior region in lateral (F-I) and ventral (J) views, at spicules (F, H) and bursa (G, I) level (black arrows pointing to the genital papillae, white arrows pointing to the phasmids).

Figure 3:

Metarhabditis amsactae (Ali, Pervez, Andrabi, Sharma and Verma, 2011) Sudhaus, 2011 (scanning electron microscopy). A, B: Cephalic and lip region in sublateral and frontal views, respectively; C, F: Lateral field (arrows pointing to the longitudinal incisures); D, E: Excretory pore (arrow) at ventral and lateral views, respectively; G, H: Vulva in ventral and lateral views, respectively; I: Female anus; J, K: Female posterior region in right lateral and ventral views, respectively (white arrows pointing to the phasmid); L, M; Male posterior region in ventral and lateral views (black arrows pointing to the genital papillae, white arrows pointing to the phasmids).
Metarhabditis amsactae (Ali, Pervez, Andrabi, Sharma and Verma, 2011) Sudhaus, 2011 (scanning electron microscopy). A, B: Cephalic and lip region in sublateral and frontal views, respectively; C, F: Lateral field (arrows pointing to the longitudinal incisures); D, E: Excretory pore (arrow) at ventral and lateral views, respectively; G, H: Vulva in ventral and lateral views, respectively; I: Female anus; J, K: Female posterior region in right lateral and ventral views, respectively (white arrows pointing to the phasmid); L, M; Male posterior region in ventral and lateral views (black arrows pointing to the genital papillae, white arrows pointing to the phasmids).

Figure 4:

Bayesian Inference tree from previously and the newly sequenced Metarhabditis amsactae (bold) and other closely related species based on sequences of the Internal Transcribed Spacer (ITS1-5.8S-ITS2) rDNA region. Bayesian posterior probabilities (%) are given for each clade. The scale bar shows the number of substitutions per site.
Bayesian Inference tree from previously and the newly sequenced Metarhabditis amsactae (bold) and other closely related species based on sequences of the Internal Transcribed Spacer (ITS1-5.8S-ITS2) rDNA region. Bayesian posterior probabilities (%) are given for each clade. The scale bar shows the number of substitutions per site.

Figure 5:

Bayesian Inference tree from the newly sequenced Metarhabditis amsactae (bold) and other closely related species based on sequences of the small subunit (18S) of rDNA region. Bayesian posterior probabilities (%) are given for each clade. The scale bar shows the number of substitutions per site.
Bayesian Inference tree from the newly sequenced Metarhabditis amsactae (bold) and other closely related species based on sequences of the small subunit (18S) of rDNA region. Bayesian posterior probabilities (%) are given for each clade. The scale bar shows the number of substitutions per site.

Figure 6:

Bayesian Inference tree from the newly sequenced Metarhabditis amsactae (bold) and other closely related species based on sequences of the D2/D3 domain of large subunit (28S) of rDNA region. Bayesian posterior probabilities (%) are given for each clade. The scale bar shows the number of substitutions per site.
Bayesian Inference tree from the newly sequenced Metarhabditis amsactae (bold) and other closely related species based on sequences of the D2/D3 domain of large subunit (28S) of rDNA region. Bayesian posterior probabilities (%) are given for each clade. The scale bar shows the number of substitutions per site.

Compendium of females of Metarhabditis amsactae (Ali, Pervez, Andrabi, Sharma and Verma, 2011) Sudhaus, 2011 populations and its synonyms.

Species M. amsactae M. amsactae M. amsactae as O. ciceri M. amsactae as O. hussainii M. amsactae as O. gingeri M. amsactae M. amsactae as M. longicaudata M. amsactae as M. rainai Metarhabditis sp. as M. amsactae
Reference Present study Ali et al. (2011) Shaheen et al. (2011) Shaheen et al. (2011) Pervez et al. (2012) Asif et al. (2013) Tabassum et al. (2019) Tabassum et al. (2019) Tabassum et al. (2019)
Country India India India India India India Pakistan Pakistan Pakistan
Habitat Rhizosphere of sugarcane and groundnut Rhizosphere of mungbean Rhizosphere of chickpea Rhizosphere of pigeonpea Rhizosphere of ginger Decaying matter Rhizosphere of mango tree Decomposed guava fruit Rhizosphere of chicko
L 718-1,135 658-786 964-1,018 902-989 1,418-1,813 786-902 1,366-1,684 1,769-2,078 1,546-1,694
a 10.9-21.1 19.7-22.9 20.1-22.5 24.4-25.5 18.5-21.2 19.2-23.5 14.0-18.0 11.7-20.0 15.0-18.0
b 4.5-6.6 4.1-4.8 5.7-5.9 3.8-4.3 5.1-5.3 4.1-5.0 5.5-7.8 7.0-8.0 6.0-8.0
c 8.7-14.0 8.9-12.1 10.3-12.9 10.2-12.7 12.1-13.2 9.6-11.2 12.0-16.0 12.0-18.0 13.0-19.0
c′ 2.9-5.2 4.1-4.6 3.6-4.3 3.3-4.8 4.6 3.8-4.5 2.5.-4.4 4.0-8.0 3.0-4.0
V 46-56 50-58 43a 42a 51-60 51-55 48-56 49-58 50-54
Lip region width 5-11 7-8 8-11 6-8 8-12 9-10 11-15 12a 12a
Stoma length 14-22 16-18 18-19 22-23 19-21 20-25 22-28 26-30 22-26
Corpus length 68-98 96-115 92-100 133 95-170 50a 62-106 57a 42a
Isthmus length 40-48 32-44 30-40 44-56 28-57 35-45 30a 27a 33a
Bulb length 26-34 24-35 26-31 33-45 44a 25-35 19a 16a 17a
Nerve ring-ant. end 98-153 99-112 111-134 170-179 178-203 110-143 154-190 76a 95a
Excretory pore-ant. end 110-166 109-130 134-136 166-172 187-223 121-160 148-250 98a 112a
Pharynx length 156-195 159-178 167-176 220-225 189-284 177-218 206-265 250-279 218-247
Mid-body width 43-81 32-39 39-46 32-40 75-89 26-40 78-108 92-111 88-105
Anal body width 16-28 16-17 20-28 19-23 25-28 19-22 25-33 12-30 30-36
Tail length 68-101 65-80 75-96 77-87 115-129 81-100 94-112 100-148 84-132

Compendium of males of Metarhabditis amsactae (Ali, Pervez, Andrabi, Sharma and Verma, 2011) Sudhaus, 2011 populations and its synonyms.

Species M. amsactae M. amsactae M. amsactae as O. cicero M. amsactae as O. hussainii M. amsactae as O. gingeri M. amsactae M. amsactae as M. longicaudata M. amsactae as M. rainai Metarhabditis sp. as M. amsactae
Reference Present study Ali et al. (2011) Shaheen et al. (2011) Shaheen et al. (2011) Pervez et al. (2012) Asif et al. (2013) Tabassum et al. (2019) Tabassum et al. (2019) Tabassum et al. (2019)
Country India India Pakistan Pakistan India India Pakistan Pakistan Pakistan
Habitat Rhizosphere of sugarcane and groundnut Rhizosphere of mungbean Rhizosphere of chickpea Rhizosphere of pigeonpea Rhizosphere of ginger Decaying matter Rhizosphere of mango tree Descomposed guava fruit Rhizosphere of chicko
L 653-999 594-804 754-973 855-889 673-821 683-868 1,154-1,325 1,100-1,392 1,234-1,498
a 12.7-20.7 16.6-19.3 19.4-20.8 25.0.-28.0 18.3-24.0 18.1-21.7 14.4-19.4 15.0-24.0 14.0-20.0
b 3.8-5.9 4.0-5.0 5.0-5.6 3.83-3.89 4.32-5.3 4.3-4.5 5.3-6.6 4.0-6.0 6.0-8.0
c 9.8-20.9 10.7-17.8 13.6-16.7 13.9-13.6 11.5-16.7 11.5-13.7 14.9-19.0 23.0-37.0 16.0-20.0
c′ 1.5-3.8 2.6-2.8 2.1-2.7 3.2 2.8-3.1 2.5-3.0 2.1-3.7 1.0-2.0 2.0-3.0
Lip region width 6-10 7-8 8-11 6-8 7a 9-10 11-14 ? ?
Stoma length 13-21 15-17 19 22-23 17-19 18-20 20-28 24-28 20-24
Corpus length 58-76 81-109 ? 134 71-112 72a ? ? ?
Isthmus length 35-41 27-42 ? 44-56 21-38 27a ? ? ?
Bulb length 24-35 20-36 ? 33-45 ? 23a ? ? ?
Nerve ring-ant. end 92-125 79-108 116-136 149-179 90-114 100-127 143-185 ? ?
Excretory pore-ant. end 113-144 87-114 127-138 155-168 110-142 119-141 137-179 ? ?
Pharynx length 141-175 134-169 149-172 223-228 142-187 155-190 184-256 211-256 204-236
Midbody width 40-66 31-45 39-46 30-35 32-39 26-40 64-69 54-88 70-98
Anal body width 17-27 16-20 26-30 19-21 16-19 20-24 21-40 26-34 27-32
Tail length 49-62 41-55 55-58 61-65 43-59 58-67 62-76 32-56 66-78
Spicules length (SL) 34-49 31-36 35-44 41-44 24-27 33-39 40-46 32-60 42-60
Gubernaculum length (GL) 16-28 13-17 19-20 14-18 9-10 14-20 20-34 13-23 16-22
GL/SL × 100 50-60 43-46 45-54 34-40 36 42-51 50-74 40 37-38

Nematode species, GenBank accession number, and origin of the sequences used for phylogenetic study.

GenBank accession number
Speciesa 18S rDNA 28S rDNA ITS rDNA Country Isolation source Reference
Ablechroiulus cristatus EU196013 EU195976 USA Unknown Kiontke et al. (2007)
Ablechroiulus dudichi AF083012 USA Unknown Fitch (unpublished)
Auanema rhodensis EU196004 USA Unknown Kiontke et al. (2007)
Buetschlinema nidrosiensis EU196020 USA Unknown Kiontke et al. (2007)
Bursilla belari MK359049 India Soil Palanisamy et al. (unpublished)
Bursilla sp. EF990722 USA Unknown Kiontke et al. (2007)
Caenorhabditis angaria JN636068 USA Rotting fruits Kiontke et al. (2011)
Caenorhabditis elegans Z92784 UK Unknown Sulston and Waterston (1998)
Caenorhabditis elegans X03680 USA Unknown Ellis et al. (1986)
Caenorhabditis sinica JN636142 USA Rotting fruits Kiontke et al. (2011)
Cephaloboides cf. armatus EU196005 USA Unknown Kiontke et al. (2007)
Crustorhabditis transita EU195995 USA Unknown Kiontke et al. (2007)
Cruznema tripartitum U73449 Unknown Baldwin et al. (1997)
Diploscapter coronatus AY593921 Netherlands Soil Helder et al. (2006)
Diploscapter sp. EU195959 USA Unknown Kiontke et al. (2007)
Distolabrellus veechi EF990725 USA Unknown Kiontke et al. (2007)
Haematozoon subulatum EU040125 China Soil Li et al. (unpublished)
Haematozoon subulatum AF083017 USA Unknown Fitch (unpublished)
Haematozoon subulatum EF990727 USA Unknown Kiontke et al. (2007)
Heterorhabditis bacteriophora KJ636408 Netherlands Unknown van Megen (unpublished)
Heterorhabditis downesi KU573061 Ireland Soil Maher et al. (2016)
Heterorhabditis megidis KJ636320 Netherlands Unknown van Megen (unpublished)
Litoditis marina AF083021 USA Unknown Fitch (unpublished)
Litoditis marina AM399053 Belgium Fucus sp. Derycke et al. (2008a)
Litoditis marina AM937053 Greece Decaying seaweeds Derycke et al. (2008b)
Litoditis mediterranea AF083020 USA Unknown Fitch (unpublished)
Litoditis mediterranea AM399068 New Zealand Unknown Derycke et al. (2008a)
Mesorhabditis anisomorpha AF083013 USA Unknown Fitch (unpublished)
Mesorhabditis anisomorpha EF990723 USA Unknown Kiontke et al. (2007)
Mesorhabditis longespiculosa EU196014 EU195980 USA Unknown Kiontke et al. (2007)
Metarhabditis amsactae MT872503, MT872504 MT872508, MT872509 MT873043, MT873044 India Soil Present study
Metarhabditis amsactae MT422254 Philippines Soil Dichusa et al. (unpublished)
Metarhabditis amsactae MT452472, MT452471 Philippines Soil Sangcopan and Sumaya (unpublished)
Metarhabditis amsactae MH392568, KY083045 KP834433, KP834432 India Soil Chavan et al. (unpublished)
Metarhabditis amsactae MK973071 Pakistan Soil Tabassum et al. (unpublished)
Metarhabditis blumi U13935 Germany Unknown Fitch et al. (1995)
Metarhabditis blumi MT043860 Philippines Soil Andalan et al. (unpublished)
Metarhabditis blumi MF989442 Colombia Bos indicus Chaves et al. (unpublished)
Metarhabditis blumi MT012150 Philippines Soil compost Guadalquiver (unpublished)
Metarhabditis blumi MN453373 India Soil Kandhasamy and Muthugounder (unpublished)
Metarhabditis blumi EU195965 USA Unknown Kiontke et al. (2007)
Metarhabditis blumi KM233152, KM233153 Brazil Cow Bossi et al. (2015)
Metarhabditis blumi DQ121436 South Africa Unknown Jumba and Gray (unpublished)
Metarhabditis rainai MT012135, MT012133 Philippines Soil Kabalu et al. (unpublished)
Metarhabditis rainai MT012153 Philippines Soil Buldiman et al. (unpublished)
Metarhabditis rainai JQ237848 USA Citrus groves Campos-Herrera et al. (2012)
Metarhabditis rainai AF083008 USA Unknown Fitch (unpublished)
Metarhabditis rainai EU195966 USA Unknown Kiontke et al. (2007)
Metarhabditis rainai KR011843, KR011846 Brazil Soil de Brida et al. (2017)
Metarhabditis sp. MK973071 Pakistan Soil Tabassum et al. (unplublished)
Myolaimus byersi KU180665 KU180676 Sweden Unknown Holovachov et al. (2015)
Oscheius carolinensis FJ547240 FJ547239 USA Vermicompost Ye et al. (2010)
Oscheius chongmingensis EF503692 China Soil Zhang et al. (2008)
Oscheius chongmingensis EU273599 China Soil Liu et al. (2012)
Oscheius chongmingensis MT548593 China Spodoptera frugiperda Li et al. (unpublished)
Oscheius colombianus AY751546 Colombia Cyrtomenus bergi Stock et al. (2005)
Oscheius dolichura EU196010 USA Unknown Kiontke et al. (2007)
Oscheius dolichuroides AF082998 USA Unknown Fitch (unpublished)
Oscheius dolichuroides EU195970 USA Unknown Kiontke et al. (2007)
Oscheius guentheri EU196022 USA Unknown Kiontke et al. (2007)
Oscheius indicus MF441252 India Soil Kumar et al. (2019)
Oscheius insectivorus AF083019 USA Unknown Fitch (unpublished)
Oscheius insectivorus EU195968 USA Unknown Kiontke et al. (2007)
Oscheius myriophilus AY602176 USA Unknown Kiontke et al. (2004)
Oscheius myriophilus MG742117 Thailand Soil Nitjarunkul et al. (unpublished)
Oscheius myriophilus U13936 USA Soil Fitch et al. (1995)
Oscheius necromenus KT884894 Australia Oncocladosoma castaneum Carta et al. (2018)
Oscheius onirici MG551687 Portugal Unknown Campos-Herrera (unpublished)
Oscheius onirici LN613263 Italy Soil Torrini et al. (2015)
Oscheius rugaoensis JQ002566 China Soil Zhang et al. (2012)
Oscheius rugaoensis KT884891 Japan Chamberlinius hualienensis Carta et al. (2018)
Oscheius saproxylicus MK959600 MK959601 Spain Decaying wood Abolafia and Pena-Santiago (2019b)
Oscheius tipulae EU195969 USA Unknown Kiontke et al. (2007)
Oscheius tipulae KP792649 Brazil Soil Campos-Herrera and Pu˚ža (unpublished)
Parasitorhabditis obtusa EF990724 Germany Bark beetles Kiontke et al. (2007)
Parasitorhabditis obtuse EU003189 USA Unknown Kiontke et al. (2007)
Pellioditis typica AF036946 Kenya Feces of an antelope Adams et al. (1998)
Pelodera pseudoteres EU196023 EU195997 USA Unknown Kiontke et al. (2007)
Pelodera teres AF083002 USA Unknown Fitch (unpublished)
Pelodera teres EU195979 USA Unknown Kiontke et al. (2007)
Phasmarhabditis hermaphrodita DQ639980 Scotland Nemaslug MacMillan et al. (2006)
Phasmarhabditis neopapillosa DQ639982 Scotland Arion ater MacMillan et al. (2006)
Phasmarhabditis papillosa KX267675 South Africa Deroceras reticulatum Pieterse et al. (2017)
Poikilolaimus floridensis AB370214 USA Termites Kanzaki et al. (2009)
Poikilolaimus oxycercus AF083023 USA Unknown Fitch (unpublished)
Poikilolaimus oxycercus EU195984 USA Unknown Kiontke et al. (2007)
Poikilolaimus piniperdae DQ059060 Germany Unknown Hong et al. (2005)
Poikilolaimus regenfussi AF083022 USA Unknown Fitch (unpublished)
Poikilolaimus regenfussi DQ059057 Germany Unknown Hong et al. (2005)
Protorhabditis sp. AF083001 USA Unknown Fitch (unpublished)
Protorhabditis sp. AY602168 USA Unknown Kiontke et al. (2007)
Rhabditella axei U13934 Germany Unknown Fitch et al. (1995)
Rhabditella axei AY602177 USA Unknown Kiontke et al. (2004)
Rhabditis brassicae EU196006 USA Unknown Kiontke et al. (2007)
Rhabditis sp. MN082353, MN082355 Taiwan Soil Yang et al. (2020)
Rhabditoides inermis AF082996 Unknown Fitch (unpublished)
Rhabditoides regina EF990726 USA Unknown Kiontke et al. (2007)
Rhomborhabditis regina KX385908 Mexico White grub Jiménez-Cortés et al. (2016)
Teratorhabditis mariannae EF990716 EF990721 USA Soil compost Kanzaki et al. (2008)
Teratorhabditis palmarum U13937 USA Unknown Fitch et al. (1995)

Morphometrics of Metarhabditis amsactae (Ali, Pervez, Andrabi, Sharma and Verma, 2011) Sudhaus, 2011 from India.

Characters Female Male L3
n 20 20 20
Body length (L) 939 ± 119 (718-1135) 800 ± 91 (653-999) 383 ± 55 (305-475)
a (L/MBW) 16.4 ± 2.7 (10.9-21.1) 16.7 ± 2.0 (12.7-20.7) 18.9 ± 2.0 (15.7-22.9)
b (L/NL) 5.4 ± 0.6 (4.5-6.6) 4.9 ± 0.5 (3.8-5.9) 3.4 ± 0.5 (2.7-4.3)
c (L/T) 10.9 ± 1.7 (8.7-14.0) 13.7 ± 2.7 (9.8-20.9) 7.5 ± 1.2 (6.0-10.2)
c′ (T/ABW) 4.1 ± 0.6 (2.9-5.2) 2.9 ± 0.5 (1.5-3.8) 4.8 ± 1.0 (3.0-6.0)
V (VA/L × 100) 51.2 ± 2.1 (46-56) – –
Lip region width 7.9 ± 1.4 (5-11) 7.1 ± 1.1 (6-10) 3.3 ± 0.5 (2-5)
Stoma length 18.4 ± 2.3 (14-22) 17.1 ± 2.3 (13-21) 12.8 ± 1.1 (11-15)
Stomatal tube width 5.0 ± 0.4 (2.5-3.5) 3.5 ± 0.7 (2.5-5.5) ?
Pharyngeal corpus length 74 ± 5.6 (68-98) 68 ± 4.5 (58-76) 35 ± 2.9 (30-42)
Metacorpus length 31 ± 3.9 (24-36) 30 ± 2.6 (24-33) 22 ± 2.4 (19-27)
Isthmus length 40 ± 5.5 (40-48) 39 ± 2.5 (35-41) 27 ± 2.6 (23-31)
Bulb length 29 ± 2.3 (26-34) 29 ± 2.6 (24-35) 16.8 ± 2.8 (12-24)
Pharynx length 175 ± 13.3 (156-195) 166 ± 7.3 (141-175) 101 ± 6.5 (88-112)
Nerve ring – anterior end 123 ± 15.0 (98-153) 112 ± 9.1 (92-125) 69 ± 10.9 (53-92)
Excretory pore–anterior end (EP) 137 ± 18.2 (110-166) 130 ± 9.1 (113-144) 78 ± 11.7 (56-103)
Deirid–anterior end 133 ± 16.0 (110-167) 125 ± 11.0 (107-147) ?
Neck length (stoma + pharynx, NL) 173 ± 15.0 (148-195) 163 ± 8.3 (144-176) 114 ± 6.1 (101-124)
Body width at neck base 43 ± 5.2 (32-50) 38 ± 4.2 (32-50) 18.7 ± 2.9 (14-25)
Mid-body width (MBW) 58 ± 10.4 (43-81) 48 ± 7.2 (40-66) 20.5 ± 3.3 (16-29)
Anterior genital branch or Testis 260 ± 38.2 (192-372) 198 ± 15 (188-222) –
Posterior genital branch 278 ± 27.5 (229-321) – –
Vagina length 24.5 ± 4.1 (17-30) – –
Vulva–anterior end (VA) 480 ± 64 (380-579) – –
Rectum length 31 ± 6.4 (22-42) – 15.0 ± 4.0 (9-23)
Anal body width (ABW) 22 ± 2.7 (16-28) 20.9 ± 2.5 (17-27) 11.2 ± 2.2 (9-17)
Tail length (T) 87 ± 10.5 (68-101) 63 ± 8.2 (49-62) 52 ± 5.9 (48-58)
Spicules length – 41 ± 7.5 (34-49) –
Gubernaculum length – 19.6 ± 3.5 (16-28) –
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