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Chemotactic and temperature-dependent responses of the Strongyloidoidea superfamily of nematodes

Published online by Cambridge University Press:  05 October 2021

Alex Dulovic*
Affiliation:
Max Planck Institute for Developmental Biology, Tübingen, Baden Württemberg, Germany NMI Natural and Medical Sciences Institute at the University of Tübingen, Tübingen, Baden Württemberg, Germany
Mat Norman
Affiliation:
Max Planck Institute for Developmental Biology, Tübingen, Baden Württemberg, Germany UBC Faculty of Medicine, Vancouver, British Columbia, Canada
Dorothee Harbecke
Affiliation:
Max Planck Institute for Developmental Biology, Tübingen, Baden Württemberg, Germany
Adrian Streit
Affiliation:
Max Planck Institute for Developmental Biology, Tübingen, Baden Württemberg, Germany
*
Author for correspondence: Alex Dulovic, E-mail: alex.dulovic@nmi.de

Abstract

Host-seeking behaviour and how a parasite identifies the correct host to infect remains a poorly understood area of parasitology. What is currently known is that host sensation and seeking behaviour is formed from a complex mixture of chemo-, thermo- and mechanosensory behaviours, of which chemosensation is the best studied. Previous studies of olfaction in parasitic nematodes suggested that this behaviour appears to be more closely related to target host and infection mode than phylogeny. However, there has not yet been a study comparing the chemotactic and temperature-dependent behaviours of very closely related parasitic and non-parasitic nematodes. To this end, we examined the temperature-dependent and chemotactic responses of the Strongyloidoidea superfamily of nematodes. We found differences in temperature response between the different species and within infective larvae. Chemotactic responses were highly divergent, with different attraction profiles between all species studied. When examining direct stimulation with fur, we found that it was insufficient to cause an attractive response. Overall, our results support the notion that olfactory sensation is more closely related to lifestyle and host range than phylogeny, and that multiple cues are required to initiate host-seeking behaviour.

Type
Research Article
Copyright
Copyright © Max-Planck Institute for Developmental Biology at Tübingen, 2021. Published by Cambridge University Press

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References

Ara, K, Hama, M, Akiba, S, Koike, K, Okisaka, K, Hagura, T, Kamiya, T and Tomita, F (2006) Foot odor due to microbial metabolism and its control. Canadian Journal of Microbiology 52, 357364.CrossRefGoogle ScholarPubMed
Bargmann, CI (2006) Chemosensation in C. elegans. WormBook, 129. doi: 10.1895/wormbook.1.123.1Google ScholarPubMed
Beknazarova, M, Whiley, H and Ross, K (2016) Strongyloidiasis: a disease of socioeconomic disadvantage. International Journal of Environmental Research and Public Health 13, 517. doi: 10.3390/ijerph13050517CrossRefGoogle ScholarPubMed
Bernier, UR, Kline, DL, Barnard, DR, Schreck, CE and Yost, RA (2000) Analysis of human skin emanations by gas chromatography/mass spectrometry. 2. Identification of volatile compounds that are candidate attractants for the yellow fever mosquito (Aedes aegypti). Analytical Chemistry 72, 747756.CrossRefGoogle ScholarPubMed
Bryant, AS, Ruiz, F, Gang, SS, Castelletto, ML, Lopez, JB and Hallem, EA (2018). A critical role for thermosensation in host seeking by skin-penetrating Nematodes. Current Biology 28, 23382347.e2336.CrossRefGoogle ScholarPubMed
Castelletto, ML, Gang, SS, Okubo, RP, Tselikova, AA, Nolan, TJ, Platzer, EG, Lok, JB and Hallem, EA (2014) Diverse host-seeking behaviors of skin-penetrating Nematodes. PLoS Pathogens 10, e1004305.CrossRefGoogle ScholarPubMed
Dillman, AR, Guillermin, ML, Lee, JH, Kim, B, Sternberg, PW and Hallem, EA (2012) Olfaction shapes host-parasite interactions in parasitic nematodes. Proceedings of the National Academy of Sciences of the USA 109, E2324E2333.CrossRefGoogle ScholarPubMed
Dulovic, A, Puller, V and Streit, A (2016). Optimizing culture conditions for free-living stages of the nematode parasite Strongyloides ratti. Experimental Parasitology, 168, 2530.CrossRefGoogle ScholarPubMed
Dulovic, A, Renahan, T, Röseler, W, Rödelsperger, C, Rose, AM and Streit, A (2020) Rhabditophanes diutinus a parthenogenetic clade IV nematode with dauer larvae. PLoS Pathogens 16, e1009113.CrossRefGoogle ScholarPubMed
Eberhardt, AG, Mayer, WE and Streit, A (2007) The free-living generation of the nematode Strongyloides papillosus undergoes sexual reproduction. International Journal for Parasitology 37, 9891000.CrossRefGoogle ScholarPubMed
Eberhardt, AG, Mayer, WE, Bonfoh, B and Streit, A (2008) The Strongyloides (Nematoda) of sheep and the predominant Strongyloides of cattle form at least two different, genetically isolated populations. Veterinary Parasitology 157, 8999.CrossRefGoogle ScholarPubMed
Gallagher, M, Wysocki, CJ, Leyden, JJ, Spielman, AI, Sun, X and Preti, G (2008) Analyses of volatile organic compounds from human skin. British Journal of Dermatology 159, 780791.CrossRefGoogle ScholarPubMed
Gemmill, AW, Viney, ME and Read, AF (2000) The evolutionary ecology of host-specificity: experimental studies with Strongyloides ratti. Parasitology 120, 429437.CrossRefGoogle ScholarPubMed
Grant, WN, Stasiuk, S, Newton-Howes, J, Ralston, M, Bisset, SA, Heath, DD and Shoemaker, CB (2006) Parastrongyloides trichosuri, a nematode parasite of mammals that is uniquely suited to genetic analysis. International Journal for Parasitology 36, 453466.CrossRefGoogle ScholarPubMed
Hallem, EA and Sternberg, PW (2008) Acute carbon dioxide avoidance in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the USA 105, 80388043.CrossRefGoogle ScholarPubMed
Hallem, EA, Rengarajan, M, Ciche, TA and Sternberg, PW (2007) Nematodes, bacteria, and flies: a tripartite model for nematode parasitism. Current Biology 17, 898904.CrossRefGoogle Scholar
Hart, AC and Chao, MY (2010) From odors to behaviours in Caenorhabditis elegans. In Menini, A (ed.), The Neurobiology of Olfaction. Boca Raton, FL: CRC Press/Taylor & Francis.Google Scholar
Hong, RL (2015) Pristionchus pacificus olfaction. In Sommer, RJ (ed.), Pristionchus pacificus – A Nematode Model for Comparative and Evolutionary Biology, Vol. 11. Brill, pp. 331352.Google Scholar
Hotez, PJ, Brindley, PJ, Bethony, JM, King, CH, Pearce, EJ and Jacobson, J (2008) Helminth infections: the great neglected tropical diseases. The Journal of Clinical Investigation 118, 13111321.CrossRefGoogle ScholarPubMed
Hunt, VL, Tsai, IJ, Coghlan, A, Reid, AJ, Holroyd, N, Foth, BJ, Tracey, A, Cotton, JA, Stanley, EJ, Beasley, H, Bennett, HM, Brooks, K, Harsha, B, Kajitani, R, Kulkarni, A, Harbecke, D, Nagayasu, E, Nichol, S, Ogura, Y, Quail, MA, Randle, N, Xia, D, Brattig, NW, Soblik, H, Ribeiro, DM, Sanchez-Flores, A, Hayashi, T, Itoh, T, Denver, DR, Grant, W, Stoltzfus, JD, Lok, JB, Murayama, H, Wastling, J, Streit, A, Kikuchi, T, Viney, M and Berriman, M (2016) The genomic basis of parasitism in the Strongyloides clade of nematodes. Nature Genetics 48, 299307.CrossRefGoogle ScholarPubMed
Jaleta, TG, Zhou, S, Bemm, FM, Schär, F, Khieu, V, Muth, S, Odermatt, P, Lok, JB and Streit, A (2017) Different but overlapping populations of Strongyloides stercoralis in dogs and humans – dogs as a possible source for zoonotic strongyloidiasis. PLoS Neglected Tropical Diseases 11, e0005752.CrossRefGoogle ScholarPubMed
Kulkarni, A, Dyka, A, Nemetschke, L, Grant, WN and Streit, A (2013) Parastrongyloides trichosuri suggests that XX/XO sex determination is ancestral in Strongyloididae (Nematoda). Parasitology 140, 18221830.CrossRefGoogle ScholarPubMed
Nutman, TB (2017) Human infection with Strongyloides stercoralis and other related Strongyloides species. Parasitology 144, 263273.CrossRefGoogle ScholarPubMed
Safer, D, Brenes, M, Dunipace, S and Schad, G (2007) Urocanic acid is a major chemoattractant for the skin-penetrating parasitic nematode Strongyloides stercoralis. Proceedings of the National Academy of Sciences 104, 16271630.CrossRefGoogle Scholar
Schär, F, Trostdorf, U, Giardina, F, Khieu, V, Muth, S, Marti, H, Vounatsou, P and Odermatt, P (2013) Strongyloides stercoralis: global distribution and risk factors. PLoS Neglected Tropical Diseases 7, e2288.CrossRefGoogle ScholarPubMed
Stiernagle, T. (2006). Maintenance of C. elegans. WormBook, ed. The C. elegans Research Community, Wormbook, doi/10.1895/wormbook.1.101.1. Available at http://www.wormbook.org.Google Scholar
Streit, A (2014) How to become a parasite without sex chromosomes: a hypothesis for the evolution of Strongyloides spp. and related nematodes. Parasitology 141, 12441254.CrossRefGoogle ScholarPubMed
Streit, A (2016) Genetics: modes of reproduction and genetic analysis. Parasitology 144 (Special Issue 3: Strongyloides), 111. doi: 10.1017/s0031182016000342Google ScholarPubMed
Streit, A, Wang, J, Kang, Y and Davis, RE (2016) Gene silencing and sex determination by programmed DNA elimination in parasitic nematodes. Current Opinion in Microbiology 32, 120127.CrossRefGoogle ScholarPubMed
Sultana, Y, Jeoffreys, N, Watts, MR, Gilbert, GL and Lee, R (2013) Real-time polymerase chain reaction for detection of Strongyloides stercoralis in stool. American Journal of Tropical Medicine and Hygiene 88, 10481051.CrossRefGoogle ScholarPubMed
Tsubokawa, D, Hatta, T, Kikuchi, T, Maeda, H, Mikami, F, Alim, MA, Maruyama, H and Tsuji, N (2017) Venestatin, a Ca(++)-binding protein from the parasitic nematode Strongyloides venezuelensis, is involved in the larval migration process. International Journal for Parasitology 47, 501509.CrossRefGoogle Scholar
Viney, M (2017) How can we understand the genomic basis of nematode parasitism? Trends in Parasitology 33, 444452.CrossRefGoogle ScholarPubMed
Viney, ME and Lok, JB (2007) Strongyloides spp. WormBook, ed. The C. elegans Research Community, Wormbook, doi/10.1895/wormbook.1.141.1. Available at http://www.wormbook.org.CrossRefGoogle Scholar
Viney, ME and Lok, JB (2015) The biology of Strongyloides spp. WormBook, 117. doi: 10.1895/wormbook.1.141.2CrossRefGoogle ScholarPubMed
Zhou, S, Harbecke, D and Streit, A (2019) From the faeces to the genome: a guideline for the isolation and preservation of Strongyloides stercoralis in the field for genetic and genomic analysis of individual worms. Parasites & Vectors 12, 496.CrossRefGoogle Scholar
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