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Introduction to Strongyloides stercoralis Anatomy

Michelle L. Castelletto

Michelle L. Castelletto

Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los AngelesLos Angeles,
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Castelletto, Michelle L.
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Damia Akimori

Damia Akimori

  • Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los AngelesLos Angeles,
  • Molecular Biology Interdepartmental Ph.D. Program, University of California, Los AngelesLos Angeles,
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Akimori, Damia
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Ruhi Patel

Ruhi Patel

Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los AngelesLos Angeles,
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Patel, Ruhi
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Nathan E. Schroeder

Nathan E. Schroeder

Department of Crop Sciences, University of Illinois at Urbana-ChampaignUrbana,
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Schroeder, Nathan E.
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Elissa A. Hallem

Elissa A. Hallem

  • Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los AngelesLos Angeles,
  • Molecular Biology Institute, University of California, Los AngelesLos Angeles,
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Hallem, Elissa A.
  
09 giu 2024
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Categoria dell'articolo: Research Paper
Pubblicato online: 09 giu 2024
Ricevuto: 14 nov 2023
DOI: https://doi.org/10.2478/jofnem-2024-0019
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© 2024 Michelle L. Castelletto et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

Figure 1:

The life cycle of Strongyloides stercoralis. S. stercoralis post-parasitic larvae are a mix of males and females. An S. stercoralis post-parasitic first-stage larva (L1) can follow one of three developmental routes: homogonic (direct) development (female only), heterogonic (indirect) development (male or female), or autoinfective development (female only). A larva entering the heterogonic pathway develops into a free-living male or female adult. All progeny of the free-living adults become infective third-stage larvae (iL3s), which must infect a host to continue the life cycle. A larva entering the homogonic pathway develops directly into an iL3. Once inside a host, iL3s develop into parasitic adults. Finally, a larva that follows the autoinfective route develops into an autoinfective larva (aL3) and ultimately a parasitic adult inside the same host. All developmental pathways involve four larval stages (L1-L4); only the first and third larval stages are depicted. Image is adapted from Castelletto et al., 2021 with permission (Castelletto and Hallem, 2021).
The life cycle of Strongyloides stercoralis. S. stercoralis post-parasitic larvae are a mix of males and females. An S. stercoralis post-parasitic first-stage larva (L1) can follow one of three developmental routes: homogonic (direct) development (female only), heterogonic (indirect) development (male or female), or autoinfective development (female only). A larva entering the heterogonic pathway develops into a free-living male or female adult. All progeny of the free-living adults become infective third-stage larvae (iL3s), which must infect a host to continue the life cycle. A larva entering the homogonic pathway develops directly into an iL3. Once inside a host, iL3s develop into parasitic adults. Finally, a larva that follows the autoinfective route develops into an autoinfective larva (aL3) and ultimately a parasitic adult inside the same host. All developmental pathways involve four larval stages (L1-L4); only the first and third larval stages are depicted. Image is adapted from Castelletto et al., 2021 with permission (Castelletto and Hallem, 2021).

Figure 2:

The adult stages of S. stercoralis. Schematics of an S. stercoralis (A) parasitic adult female; (B) free-living adult female; and (C) free-living adult male. Colored structures depict the pharynx (green), intestine (pink), and gonad (blue). Schematics are based on line drawings by Little, 1966 (Little, 1966a).
The adult stages of S. stercoralis. Schematics of an S. stercoralis (A) parasitic adult female; (B) free-living adult female; and (C) free-living adult male. Colored structures depict the pharynx (green), intestine (pink), and gonad (blue). Schematics are based on line drawings by Little, 1966 (Little, 1966a).

Figure 3:

An S. stercoralis parasitic adult female. DIC image of an S. stercoralis young adult parasitic female. Scale bar is 100 µm. Image source: D. Akimori. DIC image was created using the Stitching plugin for ImageJ (Preibisch et al., 2009; Schindelin et al., 2012).
An S. stercoralis parasitic adult female. DIC image of an S. stercoralis young adult parasitic female. Scale bar is 100 µm. Image source: D. Akimori. DIC image was created using the Stitching plugin for ImageJ (Preibisch et al., 2009; Schindelin et al., 2012).

Figure 4:

S. stercoralis free-living adults. (A) DIC image of an S. stercoralis free-living adult female; (B) DIC image of an S. stercoralis free-living adult male. Scale bars are 100 µm. Image source: D. Akimori. DIC images were created using the Stitching plugin for ImageJ (Preibisch et al., 2009; Schindelin et al., 2012).
S. stercoralis free-living adults. (A) DIC image of an S. stercoralis free-living adult female; (B) DIC image of an S. stercoralis free-living adult male. Scale bars are 100 µm. Image source: D. Akimori. DIC images were created using the Stitching plugin for ImageJ (Preibisch et al., 2009; Schindelin et al., 2012).

Figure 5:

Line drawings of the rhabditiform larval stages of S. stercoralis undergoing free-living (heterogonic) development. Reproduced with permission from Buonfrate et al., 2023 (Buonfrate et al., 2023).
Line drawings of the rhabditiform larval stages of S. stercoralis undergoing free-living (heterogonic) development. Reproduced with permission from Buonfrate et al., 2023 (Buonfrate et al., 2023).

Figure 6:

S. stercoralis free-living larvae. (A) DIC image of a male L4 larva. Box indicates the region enlarged in B. Arrow indicates the developing male copulatory structures. (B) Enlarged image of the tail of the male larva shown in A. Arrow indicates the developing male copulatory structures. (C) DIC image of a female L3 larva. Box indicates the region enlarged in D. Arrow indicates the developing vulva. (D) Enlarged image of the mid-body of the female larva shown in C. Arrow indicates the developing vulva. (E) DIC image of a female L4 larva. Box indicates the region enlarged in F. (F) Enlarged image of the mid-body of the L4 larva shown in E. Arrow indicates the distinctive invagination of the vulva that occurs at the L4 stage. For all images, scale bar is 50 µm. Image source: M. Castelletto.
S. stercoralis free-living larvae. (A) DIC image of a male L4 larva. Box indicates the region enlarged in B. Arrow indicates the developing male copulatory structures. (B) Enlarged image of the tail of the male larva shown in A. Arrow indicates the developing male copulatory structures. (C) DIC image of a female L3 larva. Box indicates the region enlarged in D. Arrow indicates the developing vulva. (D) Enlarged image of the mid-body of the female larva shown in C. Arrow indicates the developing vulva. (E) DIC image of a female L4 larva. Box indicates the region enlarged in F. (F) Enlarged image of the mid-body of the L4 larva shown in E. Arrow indicates the distinctive invagination of the vulva that occurs at the L4 stage. For all images, scale bar is 50 µm. Image source: M. Castelletto.

Figure 7:

An S. stercoralis infective larva. (A) DIC image of an S. stercoralis iL3. Box shows the region enlarged in B. Scale bar is 20 µm. (B) Enlarged image of the iL3 tail, with its distinctive tetrafurcated tip. Scale bar is 10 µm. (C) DIC image of an activated S. stercoralis iL3 isolated from a gerbil intestine. Scale bar is 20 µm. Image source: M. Castelletto.
An S. stercoralis infective larva. (A) DIC image of an S. stercoralis iL3. Box shows the region enlarged in B. Scale bar is 20 µm. (B) Enlarged image of the iL3 tail, with its distinctive tetrafurcated tip. Scale bar is 10 µm. (C) DIC image of an activated S. stercoralis iL3 isolated from a gerbil intestine. Scale bar is 20 µm. Image source: M. Castelletto.

Figure 8:

Comparison of an S. stercoralis autoinfective larva and an S. stercoralis iL3. (A) Line drawing of an autoinfective larva (aL3). (B) Line drawing of an iL3. An, anus; Es/In, esophageal-intestinal junction (also called the pharyngeal-intestinal junction); Nr, nerve ring. Adapted with permission from Buonfrate et al., 2023 (Buonfrate et al., 2023).
Comparison of an S. stercoralis autoinfective larva and an S. stercoralis iL3. (A) Line drawing of an autoinfective larva (aL3). (B) Line drawing of an iL3. An, anus; Es/In, esophageal-intestinal junction (also called the pharyngeal-intestinal junction); Nr, nerve ring. Adapted with permission from Buonfrate et al., 2023 (Buonfrate et al., 2023).

Figure 9:

Cuticle of an S. venezuelensis parasitic female. (A) TEM image of the cuticle of an S. venezuelensis parasitic female. sc, surface coat; e, epicuticle layer; oc, outer cortical layer; ic, inner cortical layer; em, external medial layer; im, internal medial layer; f, fibrous layer; b, basal layer. (B) Freeze-fracture image of the body wall of an S. venezuelensis parasitic female. s, surface coat; c, cuticle; h, hypodermis; m, muscle. The arrow indicates intramembranous particles. Images in A and B are reproduced from Martinez and de Sousa, 1995 with permission (Martinez and de Souza, 1995).
Cuticle of an S. venezuelensis parasitic female. (A) TEM image of the cuticle of an S. venezuelensis parasitic female. sc, surface coat; e, epicuticle layer; oc, outer cortical layer; ic, inner cortical layer; em, external medial layer; im, internal medial layer; f, fibrous layer; b, basal layer. (B) Freeze-fracture image of the body wall of an S. venezuelensis parasitic female. s, surface coat; c, cuticle; h, hypodermis; m, muscle. The arrow indicates intramembranous particles. Images in A and B are reproduced from Martinez and de Sousa, 1995 with permission (Martinez and de Souza, 1995).

Figure 10:

Cuticle of an S. stercoralis iL3. (A) TEM image of the cuticle of an S. stercoralis iL3. C, cuticle; H, hypodermis; M, muscle. Pseudo-coloring indicates muscle cells in green with pink outline and hypodermal layer in beige. (B) SEM image of the cuticle of an S. stercoralis iL3. TA, transverse annulations; LS, longitudinal striations; LG, longitudinal grooves. Scale bar is 2 µm. (C) TEM cross section of an S. stercoralis iL3. LG, longitudinal grooves. Pseudo-coloring indicates a subset of the muscle cells. (D) SEM image of the tail of an S. stercoralis iL3. NT, notched tail. The tail appears notched but is tetrafurcated (Nichols, 1956; Little, 1966a; Schad, 1989). Scale bar is 2 µm. Images are reproduced from Riyong et al., 2020 with permission (Riyong et al., 2020), with pseudo-color added in A and C.
Cuticle of an S. stercoralis iL3. (A) TEM image of the cuticle of an S. stercoralis iL3. C, cuticle; H, hypodermis; M, muscle. Pseudo-coloring indicates muscle cells in green with pink outline and hypodermal layer in beige. (B) SEM image of the cuticle of an S. stercoralis iL3. TA, transverse annulations; LS, longitudinal striations; LG, longitudinal grooves. Scale bar is 2 µm. (C) TEM cross section of an S. stercoralis iL3. LG, longitudinal grooves. Pseudo-coloring indicates a subset of the muscle cells. (D) SEM image of the tail of an S. stercoralis iL3. NT, notched tail. The tail appears notched but is tetrafurcated (Nichols, 1956; Little, 1966a; Schad, 1989). Scale bar is 2 µm. Images are reproduced from Riyong et al., 2020 with permission (Riyong et al., 2020), with pseudo-color added in A and C.

Figure 11:

S. stercoralis amphid sensillum. (A) TEM image of one of the paired amphid sensilla of an S. stercoralis iL3. The amphid neurons (center) are connected to each other and to the sheath cell via tight junctions. Surrounding the amphid neurons are processes from the lamellar neuron, which was originally called the lamellar cell or ALD neuron (Ashton et al., 1995) but has since been identified as the AFD neuron (Bryant et al., 2022). (B) Diagram of the amphidial bundle, showing the lamellar processes of the AFD neuron surrounding the other amphidial neuron processes (left, front). Images are reproduced from Ashton et al., 1995 with permission (Ashton et al., 1995).
S. stercoralis amphid sensillum. (A) TEM image of one of the paired amphid sensilla of an S. stercoralis iL3. The amphid neurons (center) are connected to each other and to the sheath cell via tight junctions. Surrounding the amphid neurons are processes from the lamellar neuron, which was originally called the lamellar cell or ALD neuron (Ashton et al., 1995) but has since been identified as the AFD neuron (Bryant et al., 2022). (B) Diagram of the amphidial bundle, showing the lamellar processes of the AFD neuron surrounding the other amphidial neuron processes (left, front). Images are reproduced from Ashton et al., 1995 with permission (Ashton et al., 1995).

Figure 12:

Excretory cell of S. stercoralis. (A) An S. stercoralis male L4 larva. The excretory cell is pseudo-colored. Scale bar is 50 µm. (B) Enlarged image of the head of the larva shown in A, with the excretory cell pseudo-colored. Image source: M. Castelletto.
Excretory cell of S. stercoralis. (A) An S. stercoralis male L4 larva. The excretory cell is pseudo-colored. Scale bar is 50 µm. (B) Enlarged image of the head of the larva shown in A, with the excretory cell pseudo-colored. Image source: M. Castelletto.

Figure 13:

Syncytial gonads of S. stercoralis free-living larvae. Images show the syncytial gonads of S. stercoralis free-living (A) female and (B) male L4 larvae. Regions of the syncytial gonad are outlined; arrows point to selected nuclei in the syncytial gonad. Scale bar is 20 µm. A and B are enlarged versions of the images shown in Figures 6E and 6A, respectively. Image source: M. Castelletto.
Syncytial gonads of S. stercoralis free-living larvae. Images show the syncytial gonads of S. stercoralis free-living (A) female and (B) male L4 larvae. Regions of the syncytial gonad are outlined; arrows point to selected nuclei in the syncytial gonad. Scale bar is 20 µm. A and B are enlarged versions of the images shown in Figures 6E and 6A, respectively. Image source: M. Castelletto.
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