Diverse Host-Seeking Behaviors of Skin-Penetrating Nematodes
Publication Date
August 14, 2014
Journal
PLOS Pathogens
Authors
Michelle L. Castelletto, Spencer S. Gang, Ryo P. Okubo, Anastassia A. Tselikova, et al
Volume
10
Issue
8
Pages
e1004305
DOI
https://dx.plos.org/10.1371/journal.ppat.1004305
Publisher URL
http://journals.plos.org/plospathogens/article?id=10.1371%2Fjournal.ppat.1004305
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/25121736
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4133384
Europe PMC
http://europepmc.org/abstract/MED/25121736
Web of Science
000341576300028
Scopus
84953344390
Mendeley
http://www.mendeley.com/research/diverse-hostseeking-behaviors-skinpenetrating-nematodes
Events
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Mendeley | Further Information

{"title"=>"Diverse Host-Seeking Behaviors of Skin-Penetrating Nematodes", "type"=>"journal", "authors"=>[{"first_name"=>"Michelle L.", "last_name"=>"Castelletto", "scopus_author_id"=>"8386315400"}, {"first_name"=>"Spencer S.", "last_name"=>"Gang", "scopus_author_id"=>"56749754700"}, {"first_name"=>"Ryo P.", "last_name"=>"Okubo", "scopus_author_id"=>"57039762400"}, {"first_name"=>"Anastassia A.", "last_name"=>"Tselikova", "scopus_author_id"=>"57039976100"}, {"first_name"=>"Thomas J.", "last_name"=>"Nolan", "scopus_author_id"=>"7102073678"}, {"first_name"=>"Edward G.", "last_name"=>"Platzer", "scopus_author_id"=>"7005031457"}, {"first_name"=>"James B.", "last_name"=>"Lok", "scopus_author_id"=>"7006705986"}, {"first_name"=>"Elissa A.", "last_name"=>"Hallem", "scopus_author_id"=>"7801398082"}], "year"=>2014, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537374", "scopus"=>"2-s2.0-84953344390", "pui"=>"607916831", "doi"=>"10.1371/journal.ppat.1004305", "isbn"=>"1553-7366", "sgr"=>"84953344390", "pmid"=>"25121736"}, "id"=>"4007f635-093f-3b79-af94-fa296b5807ef", "abstract"=>"Skin-penetrating parasitic nematodes infect approximately one billion people worldwide and are responsible for some of the most common neglected tropical diseases. The infective larvae of skin-penetrating nematodes are thought to search for hosts using sensory cues, yet their host-seeking behavior is poorly understood. We conducted an in-depth analysis of host seeking in the skin-penetrating human parasite Strongyloides stercoralis, and compared its behavior to that of other parasitic nematodes. We found that Str. stercoralis is highly mobile relative to other parasitic nematodes and uses a cruising strategy for finding hosts. Str. stercoralis shows robust attraction to a diverse array of human skin and sweat odorants, most of which are known mosquito attractants. Olfactory preferences of Str. stercoralis vary across life stages, suggesting a mechanism by which host seeking is limited to infective larvae. A comparison of odor-driven behavior in Str. stercoralis and six other nematode species revealed that parasite olfactory preferences reflect host specificity rather than phylogeny, suggesting an important role for olfaction in host selection. Our results may enable the development of new strategies for combating harmful nematode infections.", "link"=>"http://www.mendeley.com/research/diverse-hostseeking-behaviors-skinpenetrating-nematodes", "reader_count"=>28, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_subject_area"=>{"Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>22, "Medicine and Dentistry"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>22}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Environmental Science"=>{"Environmental Science"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Poland"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1635828"], "description"=>"<p><b>A</b>. Phylogeny of selected nematode species. Phylogenetic analysis is from Dillman <i>et al.</i>, 2012 <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004305#ppat.1004305-Dillman1\" target=\"_blank\">[22]</a>. Species used in the present study are highlighted. Red = skin-penetrating mammalian-parasitic nematode; gold = passively ingested mammalian-parasitic nematode; blue = entomopathogenic nematode; green = free-living nematode. For each of the selected species, icons depict one of their common hosts (human, rat, beetle, or cow). Phylogenetic relationships are based on ML and Bayesian analyses of nearly complete SSU sequences. Values above each branch represent Bayesian posterior probabilities; ML bootstrap indices appear below each branch. Values lower than 75 are not reported. <i>Priapulus caudatus</i> and <i>Chordodes morgani</i> were defined as outgroups. Detailed methods for phylogenetic tree construction are provided in Dillman <i>et al.</i>, 2012 <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004305#ppat.1004305-Dillman1\" target=\"_blank\">[22]</a>. <b>B–C</b>. Life cycles of skin-penetrating nematodes. <b>B</b>. Hookworms must infect a new host every generation. IJs infect hosts by skin-penetration. Nematodes develop to adulthood, reproduce, and lay eggs inside the host. Eggs are excreted in host feces and develop into IJs, which find and infect new hosts. <b>C</b>. <i>Str. stercoralis</i> and <i>Str. ratti</i> can develop through a single generation outside the host. Some larvae excreted in host feces develop into IJs; others develop into free-living adults that mate and reproduce outside the host. All progeny of free-living adults develop into IJs, which find and infect new hosts. L1–L4 are larval stages; IJ = infective juvenile. <b>D</b>. Ecology of selected nematode species.</p>", "links"=>[], "tags"=>["nematode", "infective larvae", "parasite Strongyloides stercoralis", "host"], "article_id"=>1139200, "categories"=>["Biological Sciences"], "users"=>["Michelle L. Castelletto", "Spencer S. Gang", "Ryo P. Okubo", "Anastassia A. Tselikova", "Thomas J. Nolan", "Edward G. Platzer", "James B. Lok", "Elissa A. Hallem"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004305.g001", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_relationships_and_life_cycles_of_parasitic_nematodes_/1139200", "title"=>"Phylogenetic relationships and life cycles of parasitic nematodes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-14 09:29:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1635831"], "description"=>"<p><b>A–B</b>. Responses of either <i>Str. stercoralis</i> (<b>A</b>) or <i>Str. ratti</i> (<b>B</b>) IJs, free-living adults, and free-living larvae to host odorants and fecal odor. *, <i>P</i><0.05; ***, <i>P</i><0.001, two-way ANOVA with Tukey's post-test. n = 4–12 trials for <i>Str. stercoralis</i> and n = 6–26 trials for <i>Str. ratti</i> for each condition. Error bars indicate SEM.</p>", "links"=>[], "tags"=>["nematode", "infective larvae", "parasite Strongyloides stercoralis", "host"], "article_id"=>1139203, "categories"=>["Biological Sciences"], "users"=>["Michelle L. Castelletto", "Spencer S. Gang", "Ryo P. Okubo", "Anastassia A. Tselikova", "Thomas J. Nolan", "Edward G. Platzer", "James B. Lok", "Elissa A. Hallem"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004305.g004", "stats"=>{"downloads"=>5, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Olfactory_responses_of_Strongyloides_species_vary_across_life_stages_/1139203", "title"=>"Olfactory responses of <i>Strongyloides</i> species vary across life stages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-14 09:29:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1635832", "https://ndownloader.figshare.com/files/1635833", "https://ndownloader.figshare.com/files/1635834", "https://ndownloader.figshare.com/files/1635835", "https://ndownloader.figshare.com/files/1635836", "https://ndownloader.figshare.com/files/1635837", "https://ndownloader.figshare.com/files/1635838", "https://ndownloader.figshare.com/files/1635839", "https://ndownloader.figshare.com/files/1635840", "https://ndownloader.figshare.com/files/1635841", "https://ndownloader.figshare.com/files/1635842", "https://ndownloader.figshare.com/files/1635843", "https://ndownloader.figshare.com/files/1635844", "https://ndownloader.figshare.com/files/1635845", "https://ndownloader.figshare.com/files/1635846", "https://ndownloader.figshare.com/files/1635847"], "description"=>"<div><p>Skin-penetrating parasitic nematodes infect approximately one billion people worldwide and are responsible for some of the most common neglected tropical diseases. The infective larvae of skin-penetrating nematodes are thought to search for hosts using sensory cues, yet their host-seeking behavior is poorly understood. We conducted an in-depth analysis of host seeking in the skin-penetrating human parasite <i>Strongyloides stercoralis</i>, and compared its behavior to that of other parasitic nematodes. We found that <i>Str. stercoralis</i> is highly mobile relative to other parasitic nematodes and uses a cruising strategy for finding hosts. <i>Str. stercoralis</i> shows robust attraction to a diverse array of human skin and sweat odorants, most of which are known mosquito attractants. Olfactory preferences of <i>Str. stercoralis</i> vary across life stages, suggesting a mechanism by which host seeking is limited to infective larvae. A comparison of odor-driven behavior in <i>Str. stercoralis</i> and six other nematode species revealed that parasite olfactory preferences reflect host specificity rather than phylogeny, suggesting an important role for olfaction in host selection. Our results may enable the development of new strategies for combating harmful nematode infections.</p></div>", "links"=>[], "tags"=>["nematode", "infective larvae", "parasite Strongyloides stercoralis", "host"], "article_id"=>1139204, "categories"=>["Biological Sciences"], "users"=>["Michelle L. Castelletto", "Spencer S. Gang", "Ryo P. Okubo", "Anastassia A. Tselikova", "Thomas J. Nolan", "Edward G. Platzer", "James B. Lok", "Elissa A. Hallem"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004305.s001", "https://dx.doi.org/10.1371/journal.ppat.1004305.s002", "https://dx.doi.org/10.1371/journal.ppat.1004305.s003", "https://dx.doi.org/10.1371/journal.ppat.1004305.s004", "https://dx.doi.org/10.1371/journal.ppat.1004305.s005", "https://dx.doi.org/10.1371/journal.ppat.1004305.s006", "https://dx.doi.org/10.1371/journal.ppat.1004305.s007", "https://dx.doi.org/10.1371/journal.ppat.1004305.s008", "https://dx.doi.org/10.1371/journal.ppat.1004305.s009", "https://dx.doi.org/10.1371/journal.ppat.1004305.s010", "https://dx.doi.org/10.1371/journal.ppat.1004305.s011", "https://dx.doi.org/10.1371/journal.ppat.1004305.s012", "https://dx.doi.org/10.1371/journal.ppat.1004305.s013", "https://dx.doi.org/10.1371/journal.ppat.1004305.s014", "https://dx.doi.org/10.1371/journal.ppat.1004305.s015", "https://dx.doi.org/10.1371/journal.ppat.1004305.s016"], "stats"=>{"downloads"=>9, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Diverse_Host_Seeking_Behaviors_of_Skin_Penetrating_Nematodes_/1139204", "title"=>"Diverse Host-Seeking Behaviors of Skin-Penetrating Nematodes", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-08-14 09:29:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1635829"], "description"=>"<p><b>A</b>. IJ motility in the absence of chemosensory stimulation. Motility varies across species (<i>P</i><0.0001, one-way ANOVA), with <i>Str. stercoralis</i> being the most active (<i>P</i><0.01, one-way ANOVA with Tukey-Kramer post-test). n = 6–9 trials for each species. For this graph and subsequent graphs with multiple species, red = skin-penetrating; gold = passively ingested; blue = entomopathogenic. Of the three entomopathogenic species, <i>Ste. carpocapsae</i> is considered an ambusher, <i>Ste. glaseri</i> is considered an active cruiser, and <i>He. bacteriophora</i> is considered a less active cruiser <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004305#ppat.1004305-Downes1\" target=\"_blank\">[15]</a>. Statistical analysis is shown in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004305#ppat.1004305.s007\" target=\"_blank\">Table S1</a>. <b>B</b>. Unstimulated vs. heat-stimulated mean speeds of mammalian-parasitic IJs. Heat-stimulated IJs were exposed to an acute 37°C stimulus and tracked at 37°C. ***, <i>P</i><0.001; *, <i>P</i><0.01, unpaired t test or Mann-Whitney test. n = 5–10 trials for each species. <b>C–D</b>. Heat stimulates local search behavior. <b>C</b>. Representative tracks for <i>Str. stercoralis</i> and <i>Str. ratti</i> from 20 s recordings at room temperature versus 37 s recordings at room temperature versus 37°C. <b>D</b>. Movement patterns at room temperature versus 37°C. Distance ratios were calculated as the total track length divided by the maximum displacement attained during the 20 s recording period. A distance ratio of 1 indicates travel in a straight line s recording period. A distance ratio of 1 indicates travel in a straight line; a distance ratio of >1 indicates a curved trajectory. ***, <i>P</i><0.001; **, <i>P</i><0.01, Mann-Whitney test. n = 5–10 trials. <b>E</b>. Nictation frequencies of IJs. Nictation was defined as standing or waving behavior of at least 5 s in duration over the course of a 2 min period. Nictation frequencies varied among species (<i>P</i><0.0001, chi-square test). <i>N. brasiliensis</i> showed a nictation frequency comparable to <i>Ste. carpocapsae</i> (<i>P</i>>0.05, chi-square test with Bonferroni correction) and greater than <i>Str. stercoralis</i> or <i>Str. ratti</i> (<i>P</i><0.01, chi-square test with Bonferroni correction). Statistical analysis is shown in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004305#ppat.1004305.s010\" target=\"_blank\">Table S4</a>. n = 20–28 IJs for each species. For all graphs, error bars indicate SEM.</p>", "links"=>[], "tags"=>["nematode", "infective larvae", "parasite Strongyloides stercoralis", "host"], "article_id"=>1139201, "categories"=>["Biological Sciences"], "users"=>["Michelle L. Castelletto", "Spencer S. Gang", "Ryo P. Okubo", "Anastassia A. Tselikova", "Thomas J. Nolan", "Edward G. Platzer", "James B. Lok", "Elissa A. Hallem"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004305.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Foraging_behaviors_of_skin_penetrating_nematodes_/1139201", "title"=>"Foraging behaviors of skin-penetrating nematodes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-14 09:29:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1635830"], "description"=>"<p><b>A</b>. <i>Str. stercoralis</i> is attracted to a number of human-emitted odorants. Red = attractants for <i>Str. stercoralis</i> that also attract anthropophilic mosquitoes <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004305#ppat.1004305-Qiu1\" target=\"_blank\">[31]</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004305#ppat.1004305-Mukabana1\" target=\"_blank\">[52]</a>–<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004305#ppat.1004305-Millar1\" target=\"_blank\">[58]</a>. n = 6–23 trials per odorant. <i>Str. stercoralis</i> did not respond to the chemotaxis controls (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004305#ppat.1004305.s003\" target=\"_blank\">Figure S3</a>). *, <i>P</i><0.05; ***, <i>P</i><0.001 relative to control, t-test (CO<sub>2</sub> vs. air and L-lactic acid vs. H<sub>2</sub>O) or one-way ANOVA with Bonferroni post-test (all other odorants vs. paraffin oil). <b>B</b>. Olfactory responses across species. Response magnitudes are color-coded according to the scale shown to the right of the heat map, and odorants are ordered based on hierarchical cluster analysis. n = 6–14 trials for each odorant-species combination. Each species exhibited a unique odor response profile (<i>P</i><0.0001, two-way ANOVA with Tukey's post-test). Data for responses of EPNs and <i>C. elegans</i> to 10% CO<sub>2</sub> are from Dillman <i>et al.</i>, 2012 <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004305#ppat.1004305-Dillman1\" target=\"_blank\">[22]</a>. Red = skin-penetrating; gold = passively ingested; blue = insect-parasitic; green = free-living. <b>C</b>. Responses of <i>Ha. contortus</i> to grass odor. Responses to the odors of two different grass samples were examined. n = 8–17 trials for each sample. <b>D</b>. Olfactory preferences reflect host specificity rather than phylogeny. The behavioral dendrogram was constructed based on the odor response profiles of each species. Hierarchical cluster analysis was performed using UPGMA (Unweighted Pair Group Method with Arithmetic Mean). Euclidean distance was used as a similarity measure. Hosts (humans, ruminants, rodents, or insects) for each species are indicated. Coph. Corr. = 0.96. For all graphs, error bars indicate SEM.</p>", "links"=>[], "tags"=>["nematode", "infective larvae", "parasite Strongyloides stercoralis", "host"], "article_id"=>1139202, "categories"=>["Biological Sciences"], "users"=>["Michelle L. Castelletto", "Spencer S. Gang", "Ryo P. Okubo", "Anastassia A. Tselikova", "Thomas J. Nolan", "Edward G. Platzer", "James B. Lok", "Elissa A. Hallem"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004305.g003", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Olfactory_responses_of_mammalian_parasitic_nematodes_/1139202", "title"=>"Olfactory responses of mammalian-parasitic nematodes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-14 09:29:29"}

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Relative Metric

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