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

Damia Gonzalez Akimori,Christopher R Stieha,Jonathan D C Stoltzfus,Thomas J Nolan,Emily J Dalessandro,James B Lok

doi:10.1038/s41598-021-87478-3

Damia Gonzalez Akimori, Christopher R Stieha + Show 4 more

Open Access

https://doi.org/10.1038/s41598-021-87478-3

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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.

Highlights

The human and canine parasitic nematode Strongyloides stercoralis utilizes an XX/XO sex determination system, with parasitic females reproducing by mitotic parthenogenesis and freeliving males and females reproducing sexually
These males are morphologically similar to those described by K reis[7]. We hypothesize that these rhabditiform males are precociously developing free-living males—an observation consistent with the male sex of the post-parasitic generation of S. stercoralis being determined by the inheritance of a single X chromosome, such that genetically male post-parasitic larvae invariably develop towards a rhabditiform free-living larva whether they are in the environment or in the h ost[6]
Our studies in S. stercoralis have revived the idea that post-parasitic males can precociously develop inside the host; whether these rhabditiform males are capable of tissue penetration warrants further study

Summary

Introduction

The human and canine parasitic nematode Strongyloides stercoralis utilizes an XX/XO sex determination system, with parasitic females reproducing by mitotic parthenogenesis and freeliving males and females reproducing sexually. The post-parasitic generation, which can include both males and females[7,8], develops either homogonically to infectious larvae or heterogonically to free-living adults[3]. Post-parasitic males invariably develop into free-living rhabditiform (short pharynx with two bulbs) larvae. The switch controlling homogonic versus heterogonic development for S. stercoralis post-parasitic female larvae is triggered early in the first larval stage (L1)[11]. Factors controlling this switch include temperature[12] and strain genetics[13], and these signals are mediated, in part, by dafachronic acids[14]. Greater than 95% of post-parasitic larvae in the S. stercoralis strain used in this study develop via the heterogonic route when cultured at 22 °C

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