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Gastropod parasitic nematodes (Phasmarhabditis sp.) are attracted to hyaluronic acid in snail mucus by cGMP signalling

Published online by Cambridge University Press:  15 November 2018

P. Andrus ,
O. Ingle ,
T. Coleman  and
R. Rae Open the ORCID record for R. Rae [Opens in a new window]
P. Andrus
Affiliation:
Liverpool John Moores University, School of Natural Sciences and Psychology, Byrom Street, Liverpool L33AF, UK
O. Ingle
Affiliation:
Liverpool John Moores University, School of Natural Sciences and Psychology, Byrom Street, Liverpool L33AF, UK
T. Coleman
Affiliation:
Liverpool John Moores University, School of Natural Sciences and Psychology, Byrom Street, Liverpool L33AF, UK
R. Rae*
Affiliation:
Liverpool John Moores University, School of Natural Sciences and Psychology, Byrom Street, Liverpool L33AF, UK
*
Author for correspondence: R. Rae, E-mail: [email protected]
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Abstract

Phasmarhabditis hermaphrodita is a parasitic nematode of terrestrial gastropods that has been formulated into a biological control agent for farmers and gardeners to kill slugs and snails. In order to locate slugs it is attracted to mucus, faeces and volatile cues; however, there is no information about whether these nematodes are attracted to snail cues. It is also unknown how wild isolates of P. hermaphrodita or different Phasmarhabditis species behave when exposed to gastropod cues. Therefore, we investigated whether P. hermaphrodita (commercial and wild isolated strains), P. neopapillosa and P. californica were attracted to mucus from several common snail species (Cepaea nemoralis, Cepaea hortensis, Arianta arbustorum and Cornu aspersum). We also examined whether snails (C. aspersum) collected from different locations around the UK differed in their attractiveness to wild isolates of P. hermaphrodita. Furthermore, we also investigated what properties of snail mucus the nematodes were attracted to, including hyaluronic acid and metal salts (FeSO4, ZnSO4, CuSO4 and MgSO4). We found that the commercial strain of P. hermaphrodita responded poorly to snail mucus compared to wild isolated strains, and C. aspersum collected from different parts of the UK differed in their attractiveness to the nematodes. We found that Phasmarhabditis nematodes were weakly attracted to all metals tested but were strongly attracted to hyaluronic acid. In a final experiment we also showed that pharmacological manipulation of cyclic guanosine monophosphate (cGMP) increased chemoattraction to snail mucus, suggesting that the protein kinase EGL-4 may be responsible for Phasmarhabditis sp. chemoattraction.

Keywords

chemotaxisEGL-4gastropodshyaluronic acidnematodesparasites
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e9
Copyright
Copyright © Cambridge University Press 2018 

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References

Andersen, EC et al. (2014) A variant in the neuropeptide receptor npr-1 is a major determinant of Caenorhabditis elegans growth and physiology. PLoS Genetics 10(3), e1004316.Google Scholar
Andrus, P and Rae, R (2018a) Development of Phasmarhabditis hermaphrodita (and members of the Phasmarhabditis genus) as new genetic model nematodes to study the genetic basis of parasitism. Journal of Helminthology, doi: 10.1017/S0022149X18000305.Google Scholar
Andrus, P and Rae, R (2018b) Natural variation in chemoattraction of Phasmarhabditis hermaphrodita, Phasmarhabditis neopapillosa and Phasmarhabditis californica exposed to slug mucus. Nematology (in press).Google Scholar
Bargmann, CI (2006) Chemosensation in C. elegans. In Wormbook (ed.), The C. elegans Research Community. Wormbook, doi: 10.1895/wormbook.1.123.1.Google Scholar
Bargmann, CI, Hartwieg, E and Horvitz, HR (1993) Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74, 515–527.Google Scholar
Beeson, JG et al. (2000) Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nature Medicine 6, 86–90.Google Scholar
Ben-Shahar, Y et al. (2002) Influence of gene action across different time scales on behaviour. Science 296, 741–744.Google Scholar
Branden, C and Tooze, J (1999) Introduction to Protein Structure. New York, NY: Garland Science.Google Scholar
Burton, RF (1965) Relationships between cation contents of slime and blood in the snail Helix pomatia L. Comparative Biochemistry and Physiology 15, 339–345.Google Scholar
Carnaghi, M et al. (2017) Nematode associates and susceptibility of a protected slug (Geomalacus maculosus) to four biocontrol nematode species. Biocontrol, Science and Technology 27, 294–299.Google Scholar
Cassada, RC and Russell, RL (1975) The dauer larva, a post-embryonic variant of the nematode Caenorhabditis elegans. Developmental Biology 46, 326–342.Google Scholar
Castelletto, ML et al. (2014) Diverse host-seeking behaviours of skin-penetrating nematodes. PLoS Pathogens 10(8), e1004305.Google Scholar
Coupland, JB (1995) Susceptibility of helicid snails to isolates of the nematode Phasmarhabitis hermaphrodita from southern France. Journal of Invertebrate Pathology 66, 207–208.Google Scholar
Dieterich, C et al. (2008) The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nature Genetics 40, 1193–1198.Google Scholar
Dillman, AR et al. (2012) Olfaction shapes host–parasite interactions in parasitic nematodes. Proceedings of the National Academy of Sciences of the United States of America 109, E2324–2333.Google Scholar
Duveau, F and Félix, MA (2012) Role of pleiotropy in the evolution of a cryptic developmental variation in Caenorhabditis elegans. PLoS Biology 10(1), e1001230.Google Scholar
Glen, DM et al. (1996) Exploring and exploiting the potential of the rhabditid nematode Phasmarhabditis hermaphrodita as a biocontrol agent for slugs. In Slugs and Snails: Agricultural, Veterinary and Environmental Perspectives. British Crop Protection Council (BCPC) Symposium Proceedings No. 66, pp. 271–280.Google Scholar
Haas, W and Ostrowskide de Núñez, M (1988) Chemical signals of fish skin for the attachment response of Acanthostomum brauni cercariae. Parasitological Research 74, 552–557.Google Scholar
Hapca, S et al. (2007a) Movement of Phasmarhabditis hermaphrodita nematode in heterogeneous structure. Nematology 95, 731–738.Google Scholar
Hapca, S et al. (2007b) Movement of the parasitic nematode Phasmarhabditis hermaphrodita in the presence of the slug Deroceras reticulatum. Biological Control 41, 223–229.Google Scholar
Hong, RL and Sommer, RJ (2006) Chemoattraction in Pristionchus nematodes and implications for insect recognition. Current Biology 16, 2359–2365.Google Scholar
Hong, RL, Witte, H and Sommer, RJ (2008) Natural variation in Pristionchus pacificus insect pheromone attraction involves the protein kinase EGL-4. Proceedings of the National Academy of Sciences of the United States of America 105, 7779–7784.Google Scholar
Hooper, DJ et al. (1999) Some observations on the morphology and protein profiles of the slug-parasitic nematodes Phasmarhabditis hermaphrodita and P. neopapillosa (Nematoda: Rhabditidae). Nematology 1, 173–182.Google Scholar
Kim, YS et al. (1996) A new glycosaminoglycan from the giant African snail Achatina fulica. Journal of Biological Chemistry 271, 11750–11755.Google Scholar
Kroetz, SM et al. (2012) The cGMP signalling pathway affects feeding behaviour in the necromenic nematode Pristionchus pacificus. PLoS One 7(4), e34464.Google Scholar
Kubota, Y et al. (1985) Purification and characterization of an antibacterial factor from snail mucus. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology 82, 345–348.Google Scholar
Lee, DL (2002) Behaviour. In DL, Lee (ed.), The Biology of Nematodes. London: Taylor and Francis, pp. 369–388.Google Scholar
L'Etoile, ND et al. (2002) The cyclic GMP-dependent protein kinase EGL-4 regulates olfactory adaptation in C. elegans. Neuron 36, 1079–1089.Google Scholar
McGrath, PT et al. (2009) Quantitative mapping of a digenic behavioural trait implicates globin variation in C. elegans sensory behaviors. Neuron 61, 692–699.Google Scholar
Nermut, J, Puza, V and Mracek, Z (2012) The response of Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae) and Steinernema feltiae (Nematoda: Steinernematidae) to different host-associated cues. Biological Control 61, 201–206.Google Scholar
Ng, T et al. (2013) Snails and their trails: the multiple functions of trail-following in gastropods. Biological Reviews 88, 683–700.Google Scholar
Osborne, KA et al. (1997) Natural behaviour polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277, 834–836.Google Scholar
Rae, R (2017a) Phasmarhabditis hermaphrodita – a new model to study the genetic evolution of parasitism. Nematology 19, 375–387.Google Scholar
Rae, R (2017b) The gastropod shell has been co-opted to kill parasitic nematodes. Scientific Reports 7, 4545.Google Scholar
Rae, R (2018) Shell encapsulation of parasitic nematodes by Arianta arbustorum (Linnaeus, 1758) in the laboratory and in field collections. Journal of Molluscan Studies 84, 92–95.Google Scholar
Rae, RG, Robertson, JF and Wilson, MJ (2006) The chemotactic response of Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae) to cues of Deroceras reticulatum (Mollusca: Gastropoda). Nematology 8, 197–200.Google Scholar
Rae, R et al. (2007) Biological control of terrestrial molluscs using Phasmarhabditis hermaphrodita – progress and prospects. Pest Management Science 63, 1153–1164.Google Scholar
Rae, RG, Robertson, JF and Wilson, MJ (2009) Chemoattraction and host preference of the gastropod parasitic nematode Phasmarhabditis hermaphrodita. Journal of Parasitology 95, 517–526.Google Scholar
Rae, RG, Tourna, M and Wilson, MJ (2010) The slug parasitic nematode Phasmarhabditis hermaphrodita associates with complex and variable assemblages that do not affect its virulence. Journal of Invertebrate Pathology 104, 222–226.Google Scholar
Rengarajan, S and Hallem, EA (2016) Olfactory circuits and behaviors of nematodes. Current Opinion in Neurobiology 41, 136–148.Google Scholar
Ruiz, F et al. (2017) Experience-dependent olfactory behaviors of the parasitic nematode Heligmosomoides polygyrus. PLoS Pathogens 13, e1006709.Google Scholar
Sallam, AAA, El-Massry, SA and Nasr, IN (2009) Chemical analysis of mucus from certain land snails under Egyptian conditions. Archives of Phytopathology and Plant Protection 42, 874–881.Google Scholar
Small, RW and Bradford, C (2008) Behavioural responses of Phasmarhabditis hermaphrodita (Nematoda: Rhabditida) to mucus from potential hosts. Nematology 10, 591–598.Google Scholar
Smith, AM et al. (2009) Robust cross-links in molluscan adhesive gels: testing for contributions from hydrophobic and electrostatic interactions. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 152, 110–117.Google Scholar
South, A (1992) Terrestrial Slugs: Biology, Ecology and Control. London: Springer.Google Scholar
Sterken, MG et al. (2015) The laboratory domestication of Caenorhabditis elegans. Trends in Genetics 31, 224–231.Google Scholar
Tan, L and Grewal, PS (2001) Infection behaviour of the rhabditid nematode Phasmarhabditis hermaphrodita to the grey garden slug Deroceras reticulatum. Journal of Parasitology 87, 1349–1354.Google Scholar
Tandingan De Ley, I et al. (2016) Description of Phasmarhabditis californica n. sp. and first report of P. papillosa (Nematoda: Rhabditidae) from invasive slugs in the USA. Nematology 18, 175–193.Google Scholar
Werneke, SW et al. (2007) The role of metals in molluscan adhesive gels. Journal of Experimental Biology 210, 2137–2145.Google Scholar
Williams, AJ and Rae, R (2015) Susceptibility of the giant African snail (Achatina fulica) exposed to the gastropod parasitic nematode Phasmarhabditis hermaphrodita. Nematology 127, 122–126.Google Scholar
Williams, AJ and Rae, R (2016) Cepaea nemoralis (Linnaeus, 1758) uses its shell as a defense mechanism to trap and kill parasitic nematodes. Journal of Molluscan Studies 82, 1–2.Google Scholar
Wilson, MJ and Rae, R (2015) Phasmarhabditis hermaphrodita as a control agent for slugs. In Campos-Herrera, R (ed.), Nematode Pathogenesis of Insects and Other Pests – Ecology and Applied Technologies for Sustainable Plant and Crop Protection. Cham, Switzerland: Springer International Publishing, pp. 509–521.Google Scholar
Wilson, MJ, Glen, DM and George, SK (1993) The rhabditid nematode Phasmarhabditis hermaphrodita as a potential biological control agent for slugs. Biocontrol Science and Technology 3, 503–511.Google Scholar
Wilson, MJ et al. (1995a) Selection of a bacterium for the mass production of Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae) as a biocontrol agent for slugs. Fundamental and Applied Nematology 18, 419–425.Google Scholar
Wilson, MJ et al. (1995b) Monoxenic culture of the slug parasite Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae) with different bacteria in liquid and solid phase. Fundamental and Applied Nematology 18, 159–166.Google Scholar
Wilson, MJ et al. (2000) Effects of Phasmarhabditis hermaphrodita on non-target molluscs. Pest Management Science 56, 711–716.Google Scholar