Identification of a new Sarcocystis sp. in marsh deer (Blastocerus dichotomus) from wetlands of Argentina
Author
Berra, Yanina
C´atedra de Salud Pública, Facultad de Ciencias Veterinarias, Universidad de Buenos Aires, Chorroarin 280, (C 1217 DSM), Ciudad Aut´onoma de Buenos Aires, & Consejo Nacional de Investigaciones Científicas y T´ecnicas (CONICET). Godoy Cruz 2290, (C 1425 FQB), Ciudad Aut´onoma de Buenos Aires, Argentina
Author
Gast
Author
Mor, on
Author
e
Laboratorio de Inmunoparasitología (LAINPA), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, Calle 60 y 118, (B 1904), La Plata, Buenos Aires, & Consejo Nacional de Investigaciones Científicas y T´ecnicas (CONICET). Godoy Cruz 2290, (C 1425 FQB), Ciudad Aut´onoma de Buenos Aires, Argentina
Author
Helman, Elisa
Laboratorio de Inmunoparasitología (LAINPA), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, Calle 60 y 118, (B 1904), La Plata, Buenos Aires, & Consejo Nacional de Investigaciones Científicas y T´ecnicas (CONICET). Godoy Cruz 2290, (C 1425 FQB), Ciudad Aut´onoma de Buenos Aires, Argentina
Author
Argibay, Hernan D.
Instituto de Saúde Coletiva, Universidade Federal da Bahia, Salvador, Bahia, 40110 - 040, Brazil
Author
Orozco, M. Marcela
Consejo Nacional de Investigaciones Científicas y T´ecnicas (CONICET). Godoy Cruz 2290, (C 1425 FQB), Ciudad Aut´onoma de Buenos Aires, Argentina & Instituto de Ecología, Gen´etica y Evoluci´on de Buenos Aires (IEGEBA-CONICET), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires. Av. Int. & C´atedra de Salud Pública, Facultad de Ciencias Veterinarias, Universidad de Buenos Aires, Chorroarin 280, (C 1217 DSM), Ciudad Aut´onoma de Buenos Aires,
text
International Journal for Parasitology: Parasites and Wildlife
2023
2023-04-30
20
39
45
http://dx.doi.org/10.1016/j.ijppaw.2022.12.007
journal article
307101
10.1016/j.ijppaw.2022.12.007
854c3e57-5ca7-4cee-ba86-619b254c0a82
2213-2244
PMC9849927
36688075
13287653
Sarcocystis blastoceris
n. sp.
Named after the record in marsh deer muscles (
Blastocerus dichotomus
).
Sarcocysts morphology: thin-walled (≤1 μm) without visible protrusions at optical microscopy. Measured up to 650 μm long and 70 μm wide. Cyst wall ultrastructure by TEM formed by a layer of ground substance and the outer unit membrane which form small invaginations into the ground substance giving an undulating appearance, from which arise bent ribbon-like protrusions folded over the cyst surface. Smooth ground substance layer measured 0.4 μm thick.
Fig. 3. Neighbor-Joining consensus phylogenetic tree
. Phylogenetic tree based on an alignment of 41
Sarcocystis
spp.
18S rRNA sequences performed with GENEIOUS software (Version R9), using a Tamura-Nei genetic distance model. The three sequences from marsh deer obtained in the present study are in bold. Branch consensus support is expressed as % from 1000 bootstraps. Sequence M97703 from
T. gondii
used as outgroup.
Fig. 4. Neighbor-Joining consensus phylogenetic tree
. Phylogenetic tree based on an alignment of 40
Sarcocystis
spp.
COI
sequences performed with GENEIOUS software (Version R9), using a Tamura-Nei genetic distance model and no outgroup. The three sequences from marsh deer (one from each animal) are in bold. Branch consensus support is expressed as % from 1000 bootstraps. Sequence JX473257 from
T. gondii
used as outgroup.
Intermediate hosts: Marsh deer (
Blastocerus dichotomus
).
Distribution:
Argentina
and probably South America following distribution of intermediate host.
Definitive host: based on the phylogenetic results and predator-prey geographical distribution, highly probable to be wild native canids (i.e.
Chrysocyon brachyurus
,
Lycalopex gymnocercus
,
Cerdocyon thous
) and domestic dogs.
Molecular characteristics: sequences registered in GenBank from
18S rRNA
gene fragment (Accession numbers ON911503-ON911505) and cytochrome oxidase subunit I gene (COI) fragment (Accession numbers ON932790-ON932794).
4. Discussion
The current study presents a morphological and molecular characterization of an undescribed
Sarcocystis
sp.
found in muscles from marsh deer from
Argentina
. A moderate frequency was observed by optical microscopy, observing sarcocysts in muscles from 6/14 animals. Some of the samples were in advanced autolysis. Therefore, the true prevalence of
Sarcocystis
spp.
in marsh deer may be even higher than reported here due to cyst disruption prior to or during homogenization (More´et al., 2011, 2013).
Sarcocystis
sp.
infected animals were observed in both sampled regions, being 5/
10 in
Ibera´and 1/
4 in
Delta. In
Brazil
, a frequency of
Sarcocystis
spp.
infection of 3/31 was observed in musculoskeletal system of marsh deer, also by optical microscopy (Navas-Suarez´et al., 2018). This lower proportion observed in
Brazil
could be due to a lower interspecific contact or deer predation. However, to confirm such a hypothesis, more representative samplings are required.
All the sarcocysts observed were microscopic and thin-walled. At optical microscopy, no evident protrusions were observed, similar to features from other
Sarcocystis
spp.
detected in cervids in
Argentina
(
Chang Reissig et al., 2016
,
2020
). The cyst wall ultrastructure from four cysts obtained from two marsh deer from Ibera´Wetlands showing ribbon-like protrusions resembled other species in cervids muscles like
S. cervicanis
S. grueneri
,
S. linearis
,
S. morae
,
S. taeniata
and
S. wapiti
(
Gjerde, 2014a
;
Dubey et al., 2016
;
Gjerde et al., 2017a
, b; Cerqueira-C´ezar et al., 2018; Delgado de Las Cuevas et al., 2019; Rudaityte-Luko ˙ˇsiene˙et al., 2021). A similar image was obtained previously from cysts in pudu muscles from
Argentina
(
Chang Reissig et al., 2020
). Altogether, the morphological information suggested that marsh deer are frequently infected with a single species, similar to other
Sarcocystis
spp.
affecting cervids worldwide and the
Sarcocystis
sp.
identified in pudu muscles in
Argentina
.
The molecular results reinforce the hypothesis of a single species present in marsh deer from
Argentina
. However, sequence identities (especially the ones from the
COI
gene) were below 90% with other
Sarcocystis
spp.
reported sequences. Other cervid species showed a greater diversity of
Sarcocysti
s spp. in muscles (
Gjerde, 2014a
;
Dubey et al., 2016
;
Gjerde et al., 2017a
, b; Rudaityte-Luko ˙ˇsiene˙et al., 2020a; Rudaityte-Luko ˙ˇsiene˙et al., 2020b; Rudaityte-Luko ˙ˇsiene˙et al., 2021), possibly a restricted predator-prey relationship is occurring with the marsh deer in South America, resulting in a reduced species variety. On the other hand, from 12 individual cysts or cyst portions, only eight resulted positive by
18S rRNA
PCR, and from only three samples, a sequence shorter than expected was obtained. Some of the samples were in an advanced autolysis process, which may have resulted in DNA degradation. Regarding the
ITS1
fragment, a low level of amplification was also observed, and no consensus sequence was achieved. Similar difficulties in amplifying and sequencing the
18S rRNA
and
ITS1
fragments from
S. wapiti
from North American
C. elaphus
have been mentioned by Cerqueira-C´ezar et al. (2018). Probably, the priming regions from
S. wapiti
and the species detected in marsh deer are not conserved, as previously assumed from most
Sarcocystis
spp.
(
Dahlgren et al., 2008
; More´et al., 2013). Additionally, an intraspecific sequence variation (both
18S rRNA
and
ITS1
) could also result in unintelligible sequences when the PCR products are sequenced directly. Despite the morphological similarity, the
18S rRNA
gene sequences obtained from
Sarcocystis
sp.
in marsh deer showed a low homology (93.7–96.7%) with sequences from
S. cervicanis
in red deer in
Spain
(Gjerde et al., 2017b)
S. grueneri
from reindeer in
Norway
(Dahlgren and Gjerde, 2007),
S. linearis
in roe deer from
Spain
and
Lithuania
(Rudaityt´e- Lukoˇsiene ˙ et al., 2020b),
S. morae
in fallow deer in
Lithuania
(Rudaityt´e- Lukoˇsiene ˙ et al., 2020a);
Sarcocystis
sp.
from pudu from
Argentina
(
Chang Reissig et al., 2020
),
S. taeniata
in sika deer in
Lithuania
(
Prakas et al., 2016
),
S. tarandivulpes
from reindeer from
Iceland
(Dahlgren et al., 2007) and
S. wapiti
from elk (Cerqueira-C´ezar et al., 2018). The differences at this target suggested that the
Sarcocystis
sp.
in marsh deer could be a different species. In addition, the sequences from the present study were phylogenetically positioned in the same branch with only a
S. grueneri
sequence. Several other sequences from
S. cervicanis
,
S. cruzi
,
S. hjorti
,
S. iberica
,
S. linearis
,
S. morae
,
S. rangi
,
Sarcocystis
sp.
from huemul and pudu in
Argentina
,
S. taeniata
S. tenella
,
S. venatoria
and
S. wapiti
were distant related, however, according to the positioning it is possible that all these species shared a common ancestor. Since most of these species use canids as definitive hosts, the
Sarcocystis
sp.
in marsh deer may use canids too.
Aiming further characterization, different PCR (using two reverse primers) to obtain
COI
gene fragments were performed as previously reported for species using cervids as intermediate hosts (
Gjerde, 2013
;
Gjerde et al., 2017a
). Both combinations resulted in proper amplicons for sequencing, and good quality sequences were obtained from all three cysts previously analyzed by
18S rRNA
. These results reinforce the idea of priming failure or intraspecific sequence variation of
18S rRNA
and
ITS1
fragments. All the
COI
sequences obtained in the present study showed a high homology among them and a low homology with others reported in the GenBank, being up to 89.7% with several
S. grueneri
sequences, with the highest score with the sequence KC209624 from
Rangifer tarandus
from
Norway
(
Gjerde, 2013
).
As far as we know, there are no reports of
COI
sequences from
S. wapiti
(Cerqueira-C´ezar et al., 2018), so proper comparisons are not possible. Despite morphological similarities, the high sequence divergence at
18S rRNA
and
COI
allowed the assumption that
Sarcocystis
sp.
from marsh deer is a different species from
S. wapiti
and other
Sarcocystis
spp.
producing cysts in cervids muscles. Thus, we propose the name
Sarcocystis blastoceris
n. sp.
for the species producing sarcocysts in marsh deer. In the phylogenetic tree, all
S. blastoceris COI
sequences are positioned along with sequences from
S. grueneri
from
Norway
(
Gjerde, 2013
) and with a sister clade containing sequences from
S. cervicanis
,
S. linearis
,
S. morae
,
Sarcocystis
sp.
from pudu in
Argentina
and
S. taeniata
. Several of these species are known to use canids as definitive hosts and suggest a potential common ancestor for these species (
Dubey et al., 2016
; Tuska-Szalay et al., 2021). Additionally, these native cervids are part of an alimentary chain being consumed (as prey or carrion) by domestic dogs (
Canis familiaris
) and different native canid species like maned wolf (
Chrysocyon brachyurus
), pampas fox (
Lycalopex gymnocercus
) and crab-eating fox (
Cerdocyon thous
) (
Canevari et al., 2007
).
In summary, the sarcocyst morphology, the positioning on the phylogenetic trees, and that marsh deer are frequently predated by dogs and foxes, allowed the assumption that
S. blastoceris
could have canids as definitive hosts.
Further studies should be conducted to properly identify naturally infected definitive hosts for
S. blastoceris
and its potential role on marsh deer health status.