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Evidence from the resurrected family Polyrhabdinidae Kamm, 1922 (Apicomplexa: Gregarinomorpha) supports the epimerite, an attachment organelle, as a major eugregarine innovation

Evidence from the resurrected family Polyrhabdinidae Kamm, 1922 (Apicomplexa: Gregarinomorpha) supports the epimerite, an attachment organelle, as a major eugregarine innovation
Evidence from the resurrected family Polyrhabdinidae Kamm, 1922 (Apicomplexa: Gregarinomorpha) supports the epimerite, an attachment organelle, as a major eugregarine innovation
Background
Gregarines are a major group of apicomplexan parasites of invertebrates. The gregarine classification is largely incomplete because it relies primarily on light microscopy, while electron microscopy and molecular data in the group are fragmentary and often do not overlap. A key characteristic in gregarine taxonomy is the structure and function of their attachment organelles (AOs). AOs have been commonly classified as “mucrons” or “epimerites” based on their association with other cellular traits such as septation. An alternative proposal focused on the AOs structure, functional role, and developmental fate has recently restricted the terms “mucron” to archigregarines and “epimerite” to eugregarines.

Methods
Light microscopy and scanning and transmission electron microscopy, molecular phylogenetic analyses of ribosomal RNA genes.

Results
We obtained the first data on fine morphology of aseptate eugregarines Polyrhabdina pygospionis and Polyrhabdina cf. spionis, the type species. We demonstrate that their AOs differ from the mucron in archigregarines and represent an epimerite structurally resembling that in other eugregarines examined using electron microscopy. We then used the concatenated ribosomal operon DNA sequences (SSU, 5.8S, and LSU rDNA) of P. pygospionis to explore the phylogeny of eugregarines with a resolution superior to SSU rDNA alone. The obtained phylogenies show that the Polyrhabdina clade represents an independent, deep-branching family in the Ancoroidea clade within eugregarines. Combined, these results lend strong support to the hypothesis that the epimerite is a synapomorphic innovation of eugregarines. Based on these findings, we resurrect the family Polyrhabdinidae Kamm, 1922 and erect and diagnose the family Trollidiidae fam. n. within the superfamily Ancoroidea Simdyanov et al., 2017. Additionally, we re-describe the characteristics of P. pygospionis, emend the diagnoses of the genus Polyrhabdina, the family Polyrhabdinidae, and the superfamily Ancoroidea.
2167-8359
Paskerova, Gita G.
60109f96-ba02-4b3d-baa0-200246bc9201
Miroliubova, Tatiana S.
6223e19a-ece4-4821-ad41-4c07f5962650
Valigurova, Andrea
6016e7b8-4f73-440a-8ee1-a4b05e0a26f3
Janouskovec, Jan
fbaa4a5d-872e-465b-b2c3-bb35df455cc6
Kovacikova, Magdalena
01c4c337-890d-485f-8430-04ae6f4f9890
Diakin, Andrei
770cd810-cda3-4427-89ad-7f5d94d969d3
Sokolova, Yuliya Ya
c382476d-7e74-4dfd-a689-b84b4b7d16f5
V. Mikhailov, Kirill
90508a75-5057-4d61-957f-2a6d4d4e8c4c
V. Aleoshin, Vladimir
6dcb2d2e-99ed-47c1-bb77-a499d62a62d3
Simdyanov, Timur G.
6ecfaba3-1c94-4602-a933-1805ea4b5e9d
Paskerova, Gita G.
60109f96-ba02-4b3d-baa0-200246bc9201
Miroliubova, Tatiana S.
6223e19a-ece4-4821-ad41-4c07f5962650
Valigurova, Andrea
6016e7b8-4f73-440a-8ee1-a4b05e0a26f3
Janouskovec, Jan
fbaa4a5d-872e-465b-b2c3-bb35df455cc6
Kovacikova, Magdalena
01c4c337-890d-485f-8430-04ae6f4f9890
Diakin, Andrei
770cd810-cda3-4427-89ad-7f5d94d969d3
Sokolova, Yuliya Ya
c382476d-7e74-4dfd-a689-b84b4b7d16f5
V. Mikhailov, Kirill
90508a75-5057-4d61-957f-2a6d4d4e8c4c
V. Aleoshin, Vladimir
6dcb2d2e-99ed-47c1-bb77-a499d62a62d3
Simdyanov, Timur G.
6ecfaba3-1c94-4602-a933-1805ea4b5e9d

Paskerova, Gita G., Miroliubova, Tatiana S., Valigurova, Andrea, Janouskovec, Jan, Kovacikova, Magdalena, Diakin, Andrei, Sokolova, Yuliya Ya, V. Mikhailov, Kirill, V. Aleoshin, Vladimir and Simdyanov, Timur G. (2021) Evidence from the resurrected family Polyrhabdinidae Kamm, 1922 (Apicomplexa: Gregarinomorpha) supports the epimerite, an attachment organelle, as a major eugregarine innovation. PeerJ. (doi:10.7717/PEERJ.11912).

Record type: Article

Abstract

Background
Gregarines are a major group of apicomplexan parasites of invertebrates. The gregarine classification is largely incomplete because it relies primarily on light microscopy, while electron microscopy and molecular data in the group are fragmentary and often do not overlap. A key characteristic in gregarine taxonomy is the structure and function of their attachment organelles (AOs). AOs have been commonly classified as “mucrons” or “epimerites” based on their association with other cellular traits such as septation. An alternative proposal focused on the AOs structure, functional role, and developmental fate has recently restricted the terms “mucron” to archigregarines and “epimerite” to eugregarines.

Methods
Light microscopy and scanning and transmission electron microscopy, molecular phylogenetic analyses of ribosomal RNA genes.

Results
We obtained the first data on fine morphology of aseptate eugregarines Polyrhabdina pygospionis and Polyrhabdina cf. spionis, the type species. We demonstrate that their AOs differ from the mucron in archigregarines and represent an epimerite structurally resembling that in other eugregarines examined using electron microscopy. We then used the concatenated ribosomal operon DNA sequences (SSU, 5.8S, and LSU rDNA) of P. pygospionis to explore the phylogeny of eugregarines with a resolution superior to SSU rDNA alone. The obtained phylogenies show that the Polyrhabdina clade represents an independent, deep-branching family in the Ancoroidea clade within eugregarines. Combined, these results lend strong support to the hypothesis that the epimerite is a synapomorphic innovation of eugregarines. Based on these findings, we resurrect the family Polyrhabdinidae Kamm, 1922 and erect and diagnose the family Trollidiidae fam. n. within the superfamily Ancoroidea Simdyanov et al., 2017. Additionally, we re-describe the characteristics of P. pygospionis, emend the diagnoses of the genus Polyrhabdina, the family Polyrhabdinidae, and the superfamily Ancoroidea.

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More information

e-pub ahead of print date: 16 September 2021

Identifiers

Local EPrints ID: 471359
URI: http://eprints.soton.ac.uk/id/eprint/471359
ISSN: 2167-8359
PURE UUID: e23fabbe-8b87-4864-b235-2709c03ea846
ORCID for Jan Janouskovec: ORCID iD orcid.org/0000-0001-6547-749X

Catalogue record

Date deposited: 03 Nov 2022 18:06
Last modified: 17 Mar 2024 04:11

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Contributors

Author: Gita G. Paskerova
Author: Tatiana S. Miroliubova
Author: Andrea Valigurova
Author: Jan Janouskovec ORCID iD
Author: Magdalena Kovacikova
Author: Andrei Diakin
Author: Yuliya Ya Sokolova
Author: Kirill V. Mikhailov
Author: Vladimir V. Aleoshin
Author: Timur G. Simdyanov

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