Transcriptional profiles in Strongyloides stercoralis males reveal deviations from the Caenorhabditis sex determination model

Abstract The human and canine parasitic nematode Strongyloides stercoralis utilizes an XX/XO sex determination system, with parasitic females reproducing by mitotic parthenogenesis and free-living males and females reproducing sexually. However, the genes controlling S. stercoralis sex determination...

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Main Authors: Damia Gonzalez Akimori, Emily J. Dalessandro, Thomas J. Nolan, Christopher R. Stieha, James B. Lok, Jonathan D. C. Stoltzfus
Format: Article
Language:English
Published: Nature Publishing Group 2021-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-87478-3
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spelling doaj-4af44b54378442aea9e52bf6c26c76ad2021-04-18T11:39:21ZengNature Publishing GroupScientific Reports2045-23222021-04-0111111610.1038/s41598-021-87478-3Transcriptional profiles in Strongyloides stercoralis males reveal deviations from the Caenorhabditis sex determination modelDamia Gonzalez Akimori0Emily J. Dalessandro1Thomas J. Nolan2Christopher R. Stieha3James B. Lok4Jonathan D. C. Stoltzfus5Department of Biology, Millersville University of PennsylvaniaDepartment of Biology, Millersville University of PennsylvaniaDepartment of Pathobiology, School of Veterinary Medicine, University of PennsylvaniaDepartment of Biology, Millersville University of PennsylvaniaDepartment of Pathobiology, School of Veterinary Medicine, University of PennsylvaniaDepartment of Biology, Millersville University of PennsylvaniaAbstract The human and canine parasitic nematode Strongyloides stercoralis utilizes an XX/XO sex determination system, with parasitic females reproducing by mitotic parthenogenesis and free-living males and females reproducing sexually. However, the genes controlling S. stercoralis sex determination and male development are unknown. We observed precocious development of rhabditiform males in permissive hosts treated with corticosteroids, suggesting that steroid hormones can regulate male development. To examine differences in transcript abundance between free-living adult males and other developmental stages, we utilized RNA-Seq. We found two clusters of S. stercoralis-specific genes encoding predicted transmembrane proteins that are only expressed in free-living males. We additionally identified homologs of several genes important for sex determination in Caenorhabditis species, including mab-3, tra-1, fem-2, and sex-1, which may have similar functions. However, we identified three paralogs of gld-1; Ss-qki-1 transcripts were highly abundant in adult males, while Ss-qki-2 and Ss-qki-3 transcripts were highly abundant in adult females. We also identified paralogs of pumilio domain-containing proteins with sex-specific transcripts. Intriguingly, her-1 appears to have been lost in several parasite lineages, and we were unable to identify homologs of tra-2 outside of Caenorhabditis species. Together, our data suggest that different mechanisms control male development in S. stercoralis and Caenorhabditis species.https://doi.org/10.1038/s41598-021-87478-3
collection DOAJ
language English
format Article
sources DOAJ
author Damia Gonzalez Akimori
Emily J. Dalessandro
Thomas J. Nolan
Christopher R. Stieha
James B. Lok
Jonathan D. C. Stoltzfus
spellingShingle Damia Gonzalez Akimori
Emily J. Dalessandro
Thomas J. Nolan
Christopher R. Stieha
James B. Lok
Jonathan D. C. Stoltzfus
Transcriptional profiles in Strongyloides stercoralis males reveal deviations from the Caenorhabditis sex determination model
Scientific Reports
author_facet Damia Gonzalez Akimori
Emily J. Dalessandro
Thomas J. Nolan
Christopher R. Stieha
James B. Lok
Jonathan D. C. Stoltzfus
author_sort Damia Gonzalez Akimori
title Transcriptional profiles in Strongyloides stercoralis males reveal deviations from the Caenorhabditis sex determination model
title_short Transcriptional profiles in Strongyloides stercoralis males reveal deviations from the Caenorhabditis sex determination model
title_full Transcriptional profiles in Strongyloides stercoralis males reveal deviations from the Caenorhabditis sex determination model
title_fullStr Transcriptional profiles in Strongyloides stercoralis males reveal deviations from the Caenorhabditis sex determination model
title_full_unstemmed Transcriptional profiles in Strongyloides stercoralis males reveal deviations from the Caenorhabditis sex determination model
title_sort transcriptional profiles in strongyloides stercoralis males reveal deviations from the caenorhabditis sex determination model
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-04-01
description Abstract The human and canine parasitic nematode Strongyloides stercoralis utilizes an XX/XO sex determination system, with parasitic females reproducing by mitotic parthenogenesis and free-living males and females reproducing sexually. However, the genes controlling S. stercoralis sex determination and male development are unknown. We observed precocious development of rhabditiform males in permissive hosts treated with corticosteroids, suggesting that steroid hormones can regulate male development. To examine differences in transcript abundance between free-living adult males and other developmental stages, we utilized RNA-Seq. We found two clusters of S. stercoralis-specific genes encoding predicted transmembrane proteins that are only expressed in free-living males. We additionally identified homologs of several genes important for sex determination in Caenorhabditis species, including mab-3, tra-1, fem-2, and sex-1, which may have similar functions. However, we identified three paralogs of gld-1; Ss-qki-1 transcripts were highly abundant in adult males, while Ss-qki-2 and Ss-qki-3 transcripts were highly abundant in adult females. We also identified paralogs of pumilio domain-containing proteins with sex-specific transcripts. Intriguingly, her-1 appears to have been lost in several parasite lineages, and we were unable to identify homologs of tra-2 outside of Caenorhabditis species. Together, our data suggest that different mechanisms control male development in S. stercoralis and Caenorhabditis species.
url https://doi.org/10.1038/s41598-021-87478-3
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