Dynamically expressed genes provide candidate viability biomarkers in a model coccidian.

Eimeria parasites cause enteric disease in livestock and the closely related Cyclospora cayetanensis causes human disease. Oocysts of these coccidian parasites undergo maturation (sporulation) before becoming infectious. Here, we assessed transcription in maturing oocysts of Eimeria acervulina, a wi...

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Autores principales:	Matthew S Tucker, Celia N O'Brien, Mark C Jenkins, Benjamin M Rosenthal
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/85104a4715374b07889833c1f5b5002c
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spelling	oai:doaj.org-article:85104a4715374b07889833c1f5b5002c2021-12-02T20:17:23ZDynamically expressed genes provide candidate viability biomarkers in a model coccidian.1932-620310.1371/journal.pone.0258157https://doaj.org/article/85104a4715374b07889833c1f5b5002c2021-01-01T00:00:00Zhttps://doi.org/10.1371/journal.pone.0258157https://doaj.org/toc/1932-6203Eimeria parasites cause enteric disease in livestock and the closely related Cyclospora cayetanensis causes human disease. Oocysts of these coccidian parasites undergo maturation (sporulation) before becoming infectious. Here, we assessed transcription in maturing oocysts of Eimeria acervulina, a widespread chicken parasite, predicted gene functions, and determined which of these genes also occur in C. cayetanensis. RNA-Sequencing yielded ~2 billion paired-end reads, 92% of which mapped to the E. acervulina genome. The ~6,900 annotated genes underwent temporally-coordinated patterns of gene expression. Fifty-three genes each contributed >1,000 transcripts per million (TPM) throughout the study interval, including cation-transporting ATPases, an oocyst wall protein, a palmitoyltransferase, membrane proteins, and hypothetical proteins. These genes were enriched for 285 gene ontology (GO) terms and 13 genes were ascribed to 17 KEGG pathways, defining housekeeping processes and functions important throughout sporulation. Expression differed in mature and immature oocysts for 40% (2,928) of all genes; of these, nearly two-thirds (1,843) increased their expression over time. Eight genes expressed most in immature oocysts, encoding proteins promoting oocyst maturation and development, were assigned to 37 GO terms and 5 KEGG pathways. Fifty-six genes underwent significant upregulation in mature oocysts, each contributing at least 1,000 TPM. Of these, 40 were annotated by 215 GO assignments and 9 were associated with 18 KEGG pathways, encoding products involved in respiration, carbon fixation, energy utilization, invasion, motility, and stress and detoxification responses. Sporulation orchestrates coordinated changes in the expression of many genes, most especially those governing metabolic activity. Establishing the long-term fate of these transcripts in sporulated oocysts and in senescent and deceased oocysts will further elucidate the biology of coccidian development, and may provide tools to assay infectiousness of parasite cohorts. Moreover, because many of these genes have homologues in C. cayetanensis, they may prove useful as biomarkers for risk.Matthew S TuckerCelia N O'BrienMark C JenkinsBenjamin M RosenthalPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 16, Iss 10, p e0258157 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Matthew S Tucker Celia N O'Brien Mark C Jenkins Benjamin M Rosenthal Dynamically expressed genes provide candidate viability biomarkers in a model coccidian.
description	Eimeria parasites cause enteric disease in livestock and the closely related Cyclospora cayetanensis causes human disease. Oocysts of these coccidian parasites undergo maturation (sporulation) before becoming infectious. Here, we assessed transcription in maturing oocysts of Eimeria acervulina, a widespread chicken parasite, predicted gene functions, and determined which of these genes also occur in C. cayetanensis. RNA-Sequencing yielded ~2 billion paired-end reads, 92% of which mapped to the E. acervulina genome. The ~6,900 annotated genes underwent temporally-coordinated patterns of gene expression. Fifty-three genes each contributed >1,000 transcripts per million (TPM) throughout the study interval, including cation-transporting ATPases, an oocyst wall protein, a palmitoyltransferase, membrane proteins, and hypothetical proteins. These genes were enriched for 285 gene ontology (GO) terms and 13 genes were ascribed to 17 KEGG pathways, defining housekeeping processes and functions important throughout sporulation. Expression differed in mature and immature oocysts for 40% (2,928) of all genes; of these, nearly two-thirds (1,843) increased their expression over time. Eight genes expressed most in immature oocysts, encoding proteins promoting oocyst maturation and development, were assigned to 37 GO terms and 5 KEGG pathways. Fifty-six genes underwent significant upregulation in mature oocysts, each contributing at least 1,000 TPM. Of these, 40 were annotated by 215 GO assignments and 9 were associated with 18 KEGG pathways, encoding products involved in respiration, carbon fixation, energy utilization, invasion, motility, and stress and detoxification responses. Sporulation orchestrates coordinated changes in the expression of many genes, most especially those governing metabolic activity. Establishing the long-term fate of these transcripts in sporulated oocysts and in senescent and deceased oocysts will further elucidate the biology of coccidian development, and may provide tools to assay infectiousness of parasite cohorts. Moreover, because many of these genes have homologues in C. cayetanensis, they may prove useful as biomarkers for risk.
format	article
author	Matthew S Tucker Celia N O'Brien Mark C Jenkins Benjamin M Rosenthal
author_facet	Matthew S Tucker Celia N O'Brien Mark C Jenkins Benjamin M Rosenthal
author_sort	Matthew S Tucker
title	Dynamically expressed genes provide candidate viability biomarkers in a model coccidian.
title_short	Dynamically expressed genes provide candidate viability biomarkers in a model coccidian.
title_full	Dynamically expressed genes provide candidate viability biomarkers in a model coccidian.
title_fullStr	Dynamically expressed genes provide candidate viability biomarkers in a model coccidian.
title_full_unstemmed	Dynamically expressed genes provide candidate viability biomarkers in a model coccidian.
title_sort	dynamically expressed genes provide candidate viability biomarkers in a model coccidian.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/85104a4715374b07889833c1f5b5002c
work_keys_str_mv	AT matthewstucker dynamicallyexpressedgenesprovidecandidateviabilitybiomarkersinamodelcoccidian AT celianobrien dynamicallyexpressedgenesprovidecandidateviabilitybiomarkersinamodelcoccidian AT markcjenkins dynamicallyexpressedgenesprovidecandidateviabilitybiomarkersinamodelcoccidian AT benjaminmrosenthal dynamicallyexpressedgenesprovidecandidateviabilitybiomarkersinamodelcoccidian
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Dynamically expressed genes provide candidate viability biomarkers in a model coccidian.

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