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

Bhat, Aashaq Hussain; Srivastava, Shreyansh; Rana, Aasha; Chaubey, Ashok Kumar; Machado, Ricardo A. R.; Abolafia, Joaquín

doi:10.21307/jofnem-2020-116

Figures & Tables

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 (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 (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).

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 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 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	43^a	42^a	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	12^a	12^a
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	50^a	62-106	57^a	42^a
Isthmus length	40-48	32-44	30-40	44-56	28-57	35-45	30^a	27^a	33^a
Bulb length	26-34	24-35	26-31	33-45	44^a	25-35	19^a	16^a	17^a
Nerve ring-ant. end	98-153	99-112	111-134	170-179	178-203	110-143	154-190	76^a	95^a
Excretory pore-ant. end	110-166	109-130	134-136	166-172	187-223	121-160	148-250	98^a	112^a
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	7^a	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	72^a	?	?	?
Isthmus length	35-41	27-42	?	44-56	21-38	27^a	?	?	?
Bulb length	24-35	20-36	?	33-45	?	23^a	?	?	?
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
Species^a	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)	–

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

Figures & Tables

Figure 1:

Figure 2:

Figure 3:

Figure 4:

Figure 5:

Figure 6:

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

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

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

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

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