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Polyphyletic origin, intracellular invasion, and meiotic genes in the putatively asexual agamococcidians (Apicomplexa incertae sedis)

Polyphyletic origin, intracellular invasion, and meiotic genes in the putatively asexual agamococcidians (Apicomplexa incertae sedis)
Polyphyletic origin, intracellular invasion, and meiotic genes in the putatively asexual agamococcidians (Apicomplexa incertae sedis)
Agamococcidians are enigmatic and poorly studied parasites of marine invertebrates with unexplored diversity and unclear relationships to other sporozoans such as the human pathogens Plasmodium and Toxoplasma. It is believed that agamococcidians are not capable of sexual reproduction, which is essential for life cycle completion in all well studied parasitic apicomplexans. Here, we describe three new species of agamococcidians belonging to the genus Rhytidocystis. We examined their cell morphology and ultrastructure, resolved their phylogenetic position by using near-complete rRNA operon sequences, and searched for genes associated with meiosis and oocyst wall formation in two rhytidocystid transcriptomes. Phylogenetic analyses consistently recovered rhytidocystids as basal coccidiomorphs and away from the corallicolids, demonstrating that the order Agamococcidiorida Levine, 1979 is polyphyletic. Light and transmission electron microscopy revealed that the development of rhytidocystids begins inside the gut epithelial cells, a characteristic which links them specifically with other coccidiomorphs to the exclusion of gregarines and suggests that intracellular invasion evolved early in the coccidiomorphs. We propose a new superorder Eococcidia for early coccidiomorphs. Transcriptomic analysis demonstrated that both the meiotic machinery and oocyst wall proteins are preserved in rhytidocystids. The conservation of meiotic genes and ultrastructural similarity of rhytidocystid trophozoites to macrogamonts of true coccidians point to an undescribed, cryptic sexual process in the group.
2045-2322
Miroliubova, Tatiana S.
6223e19a-ece4-4821-ad41-4c07f5962650
Simdyanov, Timur G.
6ecfaba3-1c94-4602-a933-1805ea4b5e9d
Mikhailov, Kirill
98f78548-d981-496a-b066-025565f69363
Aleoshin, Vladimir V.
96f45de0-b518-46fc-882f-c3f15ddb629a
Janouskovec, Jan
fbaa4a5d-872e-465b-b2c3-bb35df455cc6
Belova, Polina A.
93332084-3c9c-4453-824e-c41964cea870
Paskerova, Gita G.
60109f96-ba02-4b3d-baa0-200246bc9201
Miroliubova, Tatiana S.
6223e19a-ece4-4821-ad41-4c07f5962650
Simdyanov, Timur G.
6ecfaba3-1c94-4602-a933-1805ea4b5e9d
Mikhailov, Kirill
98f78548-d981-496a-b066-025565f69363
Aleoshin, Vladimir V.
96f45de0-b518-46fc-882f-c3f15ddb629a
Janouskovec, Jan
fbaa4a5d-872e-465b-b2c3-bb35df455cc6
Belova, Polina A.
93332084-3c9c-4453-824e-c41964cea870
Paskerova, Gita G.
60109f96-ba02-4b3d-baa0-200246bc9201

Miroliubova, Tatiana S., Simdyanov, Timur G., Mikhailov, Kirill, Aleoshin, Vladimir V., Janouskovec, Jan, Belova, Polina A. and Paskerova, Gita G. (2020) Polyphyletic origin, intracellular invasion, and meiotic genes in the putatively asexual agamococcidians (Apicomplexa incertae sedis). Scientific Reports, 10. (doi:10.1038/S41598-020-72287-X).

Record type: Article

Abstract

Agamococcidians are enigmatic and poorly studied parasites of marine invertebrates with unexplored diversity and unclear relationships to other sporozoans such as the human pathogens Plasmodium and Toxoplasma. It is believed that agamococcidians are not capable of sexual reproduction, which is essential for life cycle completion in all well studied parasitic apicomplexans. Here, we describe three new species of agamococcidians belonging to the genus Rhytidocystis. We examined their cell morphology and ultrastructure, resolved their phylogenetic position by using near-complete rRNA operon sequences, and searched for genes associated with meiosis and oocyst wall formation in two rhytidocystid transcriptomes. Phylogenetic analyses consistently recovered rhytidocystids as basal coccidiomorphs and away from the corallicolids, demonstrating that the order Agamococcidiorida Levine, 1979 is polyphyletic. Light and transmission electron microscopy revealed that the development of rhytidocystids begins inside the gut epithelial cells, a characteristic which links them specifically with other coccidiomorphs to the exclusion of gregarines and suggests that intracellular invasion evolved early in the coccidiomorphs. We propose a new superorder Eococcidia for early coccidiomorphs. Transcriptomic analysis demonstrated that both the meiotic machinery and oocyst wall proteins are preserved in rhytidocystids. The conservation of meiotic genes and ultrastructural similarity of rhytidocystid trophozoites to macrogamonts of true coccidians point to an undescribed, cryptic sexual process in the group.

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More information

Accepted/In Press date: 28 August 2020
Published date: 28 September 2020
Additional Information: © The Author(s) 2020

Identifiers

Local EPrints ID: 467586
URI: http://eprints.soton.ac.uk/id/eprint/467586
ISSN: 2045-2322
PURE UUID: 6f2c8539-3b19-4e13-a526-4a93aca7fd64
ORCID for Jan Janouskovec: ORCID iD orcid.org/0000-0001-6547-749X

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Date deposited: 14 Jul 2022 17:11
Last modified: 17 Mar 2024 04:11

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Contributors

Author: Tatiana S. Miroliubova
Author: Timur G. Simdyanov
Author: Kirill Mikhailov
Author: Vladimir V. Aleoshin
Author: Jan Janouskovec ORCID iD
Author: Polina A. Belova
Author: Gita G. Paskerova

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