Eimeria grayi, Jacobson & Ossiboff & Paquet-Durand & Childress & Barrett & Marlin & McAllister & Walden, 2022

Jacobson, Elliott R., Ossiboff, Robert J., Paquet-Durand, Isabelle, Childress, April L., Barrett, Heather, Marlin, Jacob, McAllister, Chris T. & Walden, Heather D. S., 2022, A New Coccidian (Apicomplexa: Eimeriidae) in the Critically Endangered Central American River Turtle (Dermatemys Mawii) in Belize, Journal of Parasitology 108 (1), pp. 92-99 : 95-96

Eimeria grayi n. sp.

( Figs. 2–5 )

Description of sporulated oocyst: Oocyst shape (n - 15): ellipsoidal; smooth, thin-walled; L x W: 30.4 (26–35) x 15.2 (13–17), L/W: 2.0 (1.7–2.5); M, OR, PG: all absent. Distinctive feature of oocyst: 3 conical projections (2.1–3.5 long) present on 1 end, with the oocyst wall forming a broadly pointed end on the opposite pole.

Description of sporocyst and sporozoites: SP: (n - 4); shape: elongate–ellipsoidal, with a smooth single-layered wall; L x W: 13.7 x 7.5 (12–19 x 6–12), L/W 1.8 (1.7–2.2); SR: sporocyst residuum, coarsely granular, and scattered; SZ: banana-shaped, 14.2 x 3.6 (14–15 x 3–4) in situ; N visible, slightly posterior to midpoint of SZ. Distinctive feature of SP: slightly pointed at 1 end with a distinct SB, SR of only a few globules, and a SRB in each SZ.

Taxonomic summary

Type host: Central American river turtle, Dermatemys mawii Gray, 1847 ( Testudines : Dermatemydidae ). Collected 11 August and 11 November 2018. Host photovouchers: University of Florida (UF) 191862-191866.

Type and only locality: Belize Foundation for Research and Environmental Education , Mile Marker 58 , Southern Highway , Belize, Central America (16 ° 33.326 ' N, 88 ° 42.423 ' W).

Prevalence: 1/3 (33%) based on oocyst identification in samples; 3/3 (100%) based on PCR and sequencing of the 18S rRNA and ITS genes.

Materials deposited: Photosyntype of a sporulated oocyst is deposited in the Harold W. Manter Laboratory of Parasitology (HWML), University of Nebraska, as HWML 206401.

ZooBank registration: urn:lsid:zoobank.org:act:B7C62C80- DF94-49F0-A73F-586C1FB2B578.

Etymology: The specific epithet is named in honor of the British naturalist, John Edward Gray (1800–1875), who described the host in 1847.

Molecular biology: All 3 fecal samples had similar content of the 18S rRNA and ITS genes. After primer editing, a 347-bp segment of the 18S rRNA gene was determined for the hicatee coccidian (GenBank accession MW538581 ). BLASTn results identified 99.4% sequence identity to several apicomplexan organisms, including Caryospora -like sp. US3 ( MN450817 ) from a green sea turtle ( Chelonia mydas ), Caryospora cheloniae genotype 1 ( KT361639 ) from Ch. mydas , and multiple lizard Schellackia spp. The hicatee coccidian was 99.7% identical to a 347-bp segment of the 18S rRNA gene of the reference sample of E. mitraria (GenBank accession MW538549 ). An 841-bp segment of the ITS region was determined for the hicatee coccidian and reference sample of E. mitraria (GenBank accessions MW538550 and MW538533 , respectively), with 75.2% sequence identity to each other. Bayesian phylogenetic analysis placed the hicatee coccidian in a clade with Eimeria collieie , E. mitraria , Eimeria arnyi , and 2 coccidians of green sea turtles ( Ca. cheloniae and Caryospora-like sp. US3) with a posterior probability of 0.89 ( Fig. 6 ).

Remarks

The oocysts being passed by the hicatee possessed multiple conical projections with 3 projecting from 1 pole and a broaderbased projection from the opposite pole ( Figs. 2–5 ). To date, the 7 previously described oocysts of Testudines having mitra-like conical projections or irregular surfaces from at least 1 end of their oocyst are (1) Eimeria amazonensis from the red-footed tortoise, Chelonoidis (formerly Geochelone ) carbonaria from Brazil ( Lainson et al., 2008); (2) Eimeria hynekprokopi from the Indochinese box turtle, Cuora galbinifrons from Vietnam (Široký and Modrý, 2010); (3) Eimeria iversoni from a captive Galapagos tortoise, Chelonoidis sp. ( McAllister et al., 2014); (4) Eimeria jirkamoraveci in the Neotropical chelid turtle Mesoclemmys (previously Batrachemys ) heliostemma (Široký et al., 2006); (5) E. mitraria originally described from the Asian Chinese threekeeled pond turtle, Mauremys (formerly Chinemys ) reevesii and subsequently described in multiple species of aquatic turtles on 3 continents ( Laveran and Mesnil, 1902; Duszynski and Morrow, 2014); (6) Eimeria motelo from the yellow-footed tortoise, Chelonoidis (formerly Geochelone ) denticulata , from Peru (Hurkováet al., 2000); and (7) Eimeria stylosa in the red-eared slider from Texas ( McAllister and Upton, 1989). Overall, oocysts of E. grayi are considerably larger than other coccidians with surface projections ( Table I ).

Figures

Figure 2. Light microscopic photomicrograph of sporulated oocyst of Eimeria grayi n. sp. Oocyst showing 3 surface projections (arrows) at 1 pole.

Figure 3. Light microscopic photomicrograph of sporulated oocyst of Eimeria grayi n. sp. Oocyst showing 2 of 3 surface projections (arrows) at 1 pole and a broader-based projection (arrowhead) from the opposite pole.

Figure 4. Light microscopic photomicrograph of sporulated oocyst of Eimeria grayi n. sp. Oocyst showing 2 of 3 surface projections (arrows) at 1 pole, a broader-based projection (arrowhead) from the opposite pole, as well as the location of the sporocyst residuum (SR).

Figure 5. Composite line drawing of a sporulated mitra-shaped oocyst of Eimeria grayi n. sp.

Figure 6. Evolutionary relationships of Eimeria grayi n. sp. inferred by Bayesian analysis of partial 18S rRNA sequences. Posterior probabilities are shown at branch points. Toxoplasma gondii (EF472967) was selected as the outgroup. Eimeria grayi n. sp. is bolded and underlined.