Há somente uma espécie de <i>Hepatozoon</i> infectando caimans brasileiros? Taxonomia integrativa desvendando essa diversidade parasitária

Úngari, L. P.; Netherlands, E. C.; Santos, A. L. Q.; Viana, L. A.; da Silva, R. J.; O’Dwyer, L. H.

L. P. Úngari ^**e-mail: letspungari@hotmail.com; leticia.p.ungari@gmail.com

Universidade Estadual Paulista – UNESP, Instituto de Biociências, Departamento de Biodiversidade e Bioestatística, Setor de Parasitologia, Botucatu, SP, Brasil

Universidade de São Paulo – USP, Departamento de Parasitologia, Instituto de Ciências Biomédicas, São Paulo, SP, Brasil

https://orcid.org/0000-0002-2982-9336

E. C. Netherlands

University of the Free State, Department of Zoology and Entomology, Bloemfontein, South Africa

https://orcid.org/0000-0003-1856-0586

A. L. Q. Santos

Universidade Federal de Uberlândia – UFU, Faculdade de Medicina Veterinária, Laboratório de Ensino e Pesquisa em Animais Silvestres, Uberlândia, MG, Brasil

https://orcid.org/0000-0002-2807-4592

L. A. Viana

Universidade Federal do Amapá – UNIFAP, Departamento de Ciências Biológicas e da Saúde, Laboratório de Estudos Morfofisiológicos e Parasitários, Macapá, AP, Brasil

https://orcid.org/0000-0002-0932-0479

R. J. da Silva

Universidade Estadual Paulista – UNESP, Instituto de Biociências, Departamento de Biodiversidade e Bioestatística, Setor de Parasitologia, Botucatu, SP, Brasil

https://orcid.org/0000-0002-3426-6873

L. H. O’Dwyer

Universidade Estadual Paulista – UNESP, Instituto de Biociências, Departamento de Biodiversidade e Bioestatística, Setor de Parasitologia, Botucatu, SP, Brasil

https://orcid.org/0000-0002-9367-368X

*e-mail: letspungari@hotmail.com; leticia.p.ungari@gmail.com

Figuras (5)
Tabelas (2)

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Figure 1
Consensus phylogram of hemogregarines based on 18S rDNA sequences. The topology trees were inferred by Bayesian (BI) and Maximum Likelihood (ML) methods (represented by ML tree). The isolates Isospora wiegmanniana (KU180242) and Lankesterella minima (AF080611) were used as an out-group.

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Figure 2
A-E. Morphological data on Hepatozoon caimani (genotype C3) in two caimans blood smears from Mato Grosso State, Brazil. A-B) Gamonts with cytoplasmic vacuoles; C-D) Mature gamonts and gamonts with cytoplasmic vacuoles (arrow); D) Gamonts; E) Gamont with whitish cytoplasm and capsule stained in dark-purple. Scale bar: 20µm

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Figure 5
A-D. Morphological data on Hepatozoon sp. (genotype A2) in four caimans blood smears from Mato Grosso State, Brazil. A) Free-gamont infecting the erythrocyte; B) Trophozoite; C) Immature gamonts with cytoplasmic granules; D) Mature gamonts. Scale bar 20µm.

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Figure 3
A-I. Morphological data on Hepatozoon caimani (genotype C1) in 14 caimans blood smears from Mato Grosso State, Brazil. A) Free-gamonts; B) Stout immature gamonts; C) Immature gamonts with cytoplasmic and nuclei chromatin granules loosely arranged across thee parasites cytoplasm; D) Late immature gamonts with slender and spread chromatin nuclear through the cytoplasm; E-F) Mature gamonts; G) Early-stage meront in the caiman´s spleen; H-I) Meronts with merozoites in the spleen. Scale bar 20µm.

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Figure 4
A-H. Morphological data on Hepatozoon sp. (genotype A1) in 11 caimans blood smears from Mato Grosso State, Brazil. A) Free-gamonts; B) Stout immature gamonts with cytoplasmic vacuoles; C) Immature gamont with dispersed nuclear chromatin; D) Mature gamonts; E) Micromeronts in the liver; F) meronts with merozoites in the liver; G) granule-mass structure meront, considered as an early stage of development; H) macromeronts with macromerozoites in the spleen. Scale bar 20µm

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Table 1
The shaded matrix (lower) shows the percentage of similarity of the 18S rDNA nucleotide sequences and the non-shaded matrix (upper) shows the p-distance (pair-wise distance) between the Hepatozoon sequences isolated from caiman hosts and compared to sequences available on GenBank.

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Table 2
Hepatozoon spp. measurements (mean ± standard deviation) of blood and tissue stages in crocodilians, Caiman crocodilus, from Brazil.

	1.	2.	3.	4.	5.	6.
1. Hepatozoon caimani (C1)		0.010	0.006	0.014	0.013	0.010
2. Hepatozoon caimani (C2)	98.98%		0.009	0.012	0.011	0.011
3. Hepatozoon caimani (C3)	99.39%	99.39%		0.016	0.018	0.014
4. Hepatozoon sp. (B)	98.78%	98.45%	98.54%		0.014	0.010
5. Hepatozoon sp. (A1)	98.78%	98.78%	98.35%	98.61%		0.006
6. Hepatozoon sp. (A2)	99.13%	99.13%	98.70%	99.13%	99.30%

Hepatozoon	Developmental stages	N	C (µm)	PL (µm)	PW (µm)	PA (µm²)	NL (µm)	NW (µm)	NA (µm²)
H. caimani Genotype C3 (Figure 2)	IGV	15		9.82 ± 2.01	5.45 ± 0.56	47.08 ± 2.53	3.74 ± 0.55	5.41± 0.38	11.02 ± 0.85
	GV	15		13.85 ± 0.99	5.10 ± 0.79	61.95 ± 3.99	5.35 ± 0.21	4.14 ± 0.61	12.67 ± 0.97
	MG	25		14.75 ± 1.85	5.71 ± 1.33	59.64 ± 2.14	4.18 ± 0.74	3.79 ± 1.00	16.01 ± 1.00
	GS	2		17.51± 0.58	6.43 ± 0.44	94.11 ± 1.80	5.85 ± 1.01	5.04 ± 0.92	18.07 ± 1.32
H. caimani	FG	25		24.71 ± 1.06	3.42 ± 0.96	59.40 ± 6.01	6.41 ± 0.42	3.09 ± 0.61	12.07 ± 1.33
Genotype C1	IGV	30		13.95 ± 1.21	4.77 ± 1.00	62.53 ± 8.05	5.45 ± 0.98	3.93 ± 0.76	12.75 ± 2.03
(Figure 3)	IGG	15		13.87 ± 1.21	5.02 ± 0.99	64.78 ± 0.86	6.78 ± 1.72	4.87 ± 1.01	16.78 ± 3.05
	LIG	50		13.59 ± 1.43	3.54 ± 0.86	55.64 ± 13.36	5.98 ± 1.26	3.20 ± 0.48	13.30 ± 2.99
	MG1	50		15.57 ± 1.72	5.84 ± 0.98	77.93 ± 5.01	4.67 ± 0.87	4.05 ± 1.23	14.54 ± 2.00
	Mi	15	3.82 ± 0.41	9.26 ± 0.85	9.90 ± 1.30	73.58 ± 19.55
	Miz	10		4.80 ± 0.94	1.20 ± 0.22	5.36 ± 1.02	0.82 ± 0.68	1.06 ± 0.41	1.67 ± 0.55
Hepatozoon sp.	FG	15		25.28 ± 0.70	2.73 ± 0.56	61.38 ± 5.10	8.77 ± 0.65	2.73 ± 0.56	14.60 ± 1.75
Genotype A1	IG	20		14.70 ± 2.01	5.12 ± 3.0	70.88 ± 2.74	4.44 ± 0.71	4.77 ± 0.97	16.08 ± 2.54
(Figure 4)	MG	40		13.47 ± 0.46	4.55 ± 0.40	55.75 ± 3.91	6.75 ± 0.62	2.79 ± 0.36	15.43 ± 1.78
	Mi	16	1.75 ± 0.31	10.81 ± 2.00	9.69 ± 1.68	76.93 ± 9.41
	Ma (R109)	2	N - 4.45	14.05 - 13.32	16.20 - 19.16	142.60 – 169.12
	Maz	5		7.56 ± 0.40	1.82 ± 0.25	11.03 ± 1.55	2.60 ± 0.38	1.68 ± 0.25	3.67 ± 0.59
	Ma (R115)	1		29.39	22.35	366.06
	Maz	7		9.27 ± 0.65	3.39 ± 0.20	18.90 ± 3.20	3.80 ± 0.63	2.15 ± 0.19	9.22 ± 1.31
Hepatozoon sp.	FG	25		12.83 ± 1.51	4.35 ± 0.33	51.66 ± 0.62	6.37 ± 0.92	3.33 ± 0.54	12.01 ± 1.85
Genotype A2	T	25		10.19 ± 0.83	3.88 ± 1.02	42.81 ± 3.78	5.93 ± 1.24	2.86 ± 0.91	12.04 ± 0.79
(Figure 5)	IG	50		12.83 ± 1.51	4.35 ± 0.33	51.66 ± 4.02	6.37 ± 0.92	3.35 ± 0.54	14.97 ± 2.00
	MG	50		12.84 ± 0.34	4.88 ± 0.17	61.12 ± 2.09	6.46 ± 0.62	4.24 ± 0.43	15.04 ± 1.22

[1] *e-mail: letspungari@hotmail.com; leticia.p.ungari@gmail.com

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Há somente uma espécie de Hepatozoon infectando caimans brasileiros? Taxonomia integrativa desvendando essa diversidade parasitária

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