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      The impact of maturity on the ability of Eimeria acervulina and Eimeria meleagrimitis oocysts to sporulate Translated title: L’impact de la maturité sur la capacité à sporuler des oocystes d’ Eimeria acervulina et d’ Eimeria meleagrimitis

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          Abstract

          The sporulation of oocysts of Eimeria that infect poultry is known to be under the influence of environmental conditions, including temperature, oxygen supply, and moisture. However, even when these conditions are optimal, the level of sporulation can remain low. The effect of oocyst maturity on their ability to sporulate was investigated for two species of Eimeria: E. acervulina of chickens, and E. meleagrimitis of turkeys. After oral infection of birds, oocysts were collected at their production site in the intestine at different times around the prepatent period. The percentage of sporulation was determined by observation of 100 oocysts for each sample. With E. acervulina, it was observed that sporulation depended on the time of collection of the oocysts in the intestine, and that it increased with aging oocysts (from 5% to 40% globally in 8 h). With E. meleagrimitis, sporulation remained low with oocysts collected in the duodenum (below 20%), but oocysts collected in the midgut and in the lower intestine sporulated more efficiently (around 80%) than oocysts collected in the duodenum at the same time. One explanation for these results is the assumption that oocysts may be produced before fertilization, and that microgametes have not yet fertilized the newly produced oocysts. As time goes on, more oocysts would be fertilized, locally in the duodenum for E. acervulina, and descending along the gut for E. meleagrimitis. This hypothesis needs to be investigated further, but it could lead to new approaches to control these parasites by targeting the microgametes.

          Translated abstract

          La sporulation des oocystes chez les Eimeria qui infectent la volaille est connue pour être influencée par les conditions environnementales (température, apport d’oxygène et humidité). Cependant, même lorsque ces conditions sont optimales, le niveau de sporulation peut rester faible. L’effet de la maturité des oocystes sur leur capacité à sporuler a été étudié pour deux espèces d’ Eimeria : E. acervulina du poulet et E. meleagrimitis de la dinde. Après infection orale des oiseaux, les oocystes ont été collectés sur leur site de production dans l’intestin à différents moments autour de la période prépatente. Le pourcentage de sporulation a été déterminé en observant 100 oocystes pour chaque échantillon. Avec E. acervulina, il a été observé que le pourcentage de sporulation dépendait du moment de la collecte des oocystes dans l’intestin, et qu’il augmentait avec des oocystes vieillissants (globalement de 5 % à 40 % en 8 heures). Avec E. meleagrimitis, le pourcentage de sporulation restait faible avec les oocystes collectés dans le duodénum (inférieur à 20 %), mais les oocystes collectés dans l’intestin moyen et dans l’intestin inférieur ont sporulé plus efficacement (environ 80 %) que les oocystes recueillis dans le duodénum en même temps. Une explication de ces résultats repose sur l’hypothèse que les oocystes peuvent être produits avant la fécondation et que les microgamètes n’ont pas encore fécondé les oocystes nouvellement produits. Avec le temps, davantage d’oocystes seraient fécondés, localement dans le duodénum pour E. acervulina, et descendant le long de l’intestin pour E. meleagrimitis. Cette hypothèse doit être approfondie, mais elle peut conduire à de nouvelles approches pour contrôler ces parasites en ciblant les microgamètes.

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          Most cited references18

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          Prevalence and distribution of Eimeria species in broiler chicken farms of different capacities

          We conducted a survey in broiler farms from Romania to establish prevalence and distribution of Eimeria species using single PCR assay. We found Eimeria spp. in 21 (91%) out of 23 flocks, and in 11 (92%) out of 12 farms. Four species of Eimeria were identified: E. acervulina (21/23; 91%), E. tenella (14/23; 61%), E. maxima (5/23; 22%) and E. praecox (3/23; 13%). Infection with a single species (E. acervulina) was detected in 6 (26%) infected flocks originated from large farms. Mixed infections were found in 15 (65%) flocks and the most prevalent combination was E. acervulina + E. tenella (8/23; 35%). Four flocks (17%) harboured mixed infection with E. acervulina + E. tenella + E. maxima. E. acervulina was significantly more prevalent in flocks that received ionophores as anticoccidial feed additives.
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            The development of the macrogamete and oocyst wall in Eimeria maxima: immuno-light and electron microscopy.

            We have identified, and followed the development of three macrogamete organelles involved in the formation of the oocyst wall of Eimeria maxima. The first were small lucent vacuoles that cross-reacted with antibodies to the apple domains of the Toxoplasma gondii microneme protein 4. They appeared early in development and were secreted during macrogamete maturation to form an outer veil and were termed veil forming bodies. The second were the wall forming bodies type 1, large, electron dense vacuoles that stained positively only with antibodies raised to an enriched preparation of the native forms of 56 (gam56), 82 (gam82) and 230 kDa (gam230) gametocyte antigens (termed anti-APGA). The third were the wall forming bodies type 2, which appeared before the wall forming bodies type 1 but remain enclosed within the rough endoplasmic reticulum and stained positively with antibodies raised to recombinant versions of gam56 (anti-gam56), gam82 (anti-gam82) and gam230 (anti-gam230) plus anti-APGA. At the initiation of oocyst wall formation, the anti-T. gondii microneme protein 4 positive outer veil detached from the surface. The outer layer of the oocyst wall was formed by the release of the contents of wall forming bodies type 1 at the surface to form an electron dense, anti-APGA positive layer. The wall forming bodies type 2 appeared, subsequently, to give rise to the electron lucent inner layer. Thus, oocyst wall formation in E. maxima represents a sequential release of the contents of the veil forming bodies, wall forming bodies types 1 and 2 and this may be controlled at the level of the rough endoplasmic reticulum/Golgi body.
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              Sex and Eimeria: a molecular perspective.

              Eimeria is a common genus of apicomplexan parasites that infect diverse vertebrates, most notably poultry, causing serious disease and economic loss. Like all apicomplexans, eimerians have a complex life cycle characterized by asexual divisions that amplify the parasite population in preparation for sexual reproduction. This can be divided into three events: gametocytogenesis, producing gametocytes from merozoites; gametogenesis, producing microgametes and macrogametes from gametocytes; and fertilization of macrogametes by microgametes, producing diploid zygotes with ensuing meiosis completing the sexual phase. Sexual development in Eimeria depends on the differential expression of stage-specific genes, rather than presence or absence of sex chromosomes. Thus, it involves the generation of specific structures and, implicitly, storage of proteins and regulation of protein expression in macrogametes, in preparation for fertilization. In Eimeria, the formation of a unique, resilient structure, the oocyst wall, is essential for completion of the sexual phase and parasite transmission. In this review, we piece together the molecular events that underpin sexual reproduction in Eimeria and use additional details from analogous events in Plasmodium to fill current knowledge gaps. The mechanisms governing sexual stage formation and subsequent fertilization may represent targets for counteracting parasite transmission.
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                Author and article information

                Journal
                parasite
                https://www.parasite-journal.org
                Parasite
                Parasite
                EDP Sciences
                1776-1042
                02 April 2021
                2021
                02 April 2021
                02 April 2021
                : 28
                : ( publisher-idID: parasite/2021/01 )
                : 32
                Affiliations
                [1 ] Avian and Rabbit Virology, Immunology, Parasitology Unit, ANSES, Laboratory of Ploufragan-Plouzané-Niort, , PO Box 53, 22440 Ploufragan, France,
                Author notes
                [* ]Corresponding author: Jean-michel.reperant@ 123456anses.fr
                Author information
                https://orcid.org/0000-0003-2485-1603
                Article
                parasite200179
                10.1051/parasite/2021031
                de4c1ed3-b24c-4c25-8bc5-1952b19f8e78
                © J.-M. Répérant et al., published by EDP Sciences, 2021

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 03 November 2020
                : 14 March 2021
                Page count
                Figures: 4, Tables: 1, Equations: 0, References: 17, Pages: 7
                Categories
                Research Article
                Custom metadata
                Parasite 28, 32 (2021)
                2021
                2021
                2021
                yes

                Parasitology,Life sciences
                Turkey,Chicken,Oocysts,Sporulation,Coccidia,Eimeria
                Parasitology, Life sciences
                Turkey, Chicken, Oocysts, Sporulation, Coccidia, Eimeria

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