Novel insight into the genetic diversity of strongylid nematodes infecting South-East and East Asian primates

. 2024 Apr ; 151 (5) : 514-522. [epub] 20240417

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38629119

Grantová podpora
15H04283 Japan Society for the Promotion of Science
16H06181 Japan Society for the Promotion of Science
20H03333 Japan Society for the Promotion of Science
24770232 Japan Society for the Promotion of Science
446 Japan Society for the Promotion of Science
22-16475S Grantová Agentura České Republiky

With many non-human primates (NHPs) showing continued population decline, there is an ongoing need to better understand their ecology and conservation threats. One such threat is the risk of disease, with various bacterial, viral and parasitic infections previously reported to have damaging consequences for NHP hosts. Strongylid nematodes are one of the most commonly reported parasitic infections in NHPs. Current knowledge of NHP strongylid infections is restricted by their typical occurrence as mixed infections of multiple genera, which are indistinguishable through traditional microscopic approaches. Here, modern metagenomics approaches were applied for insight into the genetic diversity of strongylid infections in South-East and East Asian NHPs. We hypothesized that strongylid nematodes occur in mixed communities of multiple taxa, dominated by Oesophagostomum, matching previous findings using single-specimen genetics. Utilizing the Illumina MiSeq platform, ITS-2 strongylid metabarcoding was applied to 90 samples from various wild NHPs occurring in Malaysian Borneo and Japan. A clear dominance of Oesophagostomum aculeatum was found, with almost all sequences assigned to this species. This study suggests that strongylid communities of Asian NHPs may be less species-rich than those in African NHPs, where multi-genera communities are reported. Such knowledge contributes baseline data, assisting with ongoing monitoring of health threats to NHPs.

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Ambardar S, Gupta R, Trakroo D, Lal R and Vakhlu J (2016) High throughput sequencing: an overview of sequencing chemistry. Indian J. Microbiol 56, 394–404. PubMed PMC

Anisimova M, Gil M, Dufayard JF, Dessimoz C and Gascuel O (2011) Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Systematic Biology 60, 685–699. PubMed PMC

Arizono N, Yamada M, Tegoshi T and Onishi K (2012) Molecular identification of oesophagostomum and trichuris eggs isolated from wild Japanese macaques. The Korean Journal of Parasitology 50, 253–257. PubMed PMC

Bates D, Mächler M, Bolker BM and Walker SC (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.

Bicca-Marques JC, Rabelo RM, de Almeida MAB and Sales LP (2022) The risks of yellow fever to Asian primates. International Journal of Primatology 43, 74–91.

Blouin MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527–531. PubMed

Brooks DR (1979) Testing the context and extent of host–parasite coevolution. Systematic Biology 28, 299–307.

Callahan B, McMurdie P, Rosen M, Han A, Johnson A and Holmes S (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581–583. PubMed PMC

Callinan APL and Westcott JM (1986) Vertical distribution of trichostrongylid larvae on herbage and in soil. International Journal for Parasitology 16, 241–244. PubMed

Cantacessi C, Campbell BE and Gasser RB (2012) Key strongylid nematodes of animals – impact of next-generation transcriptomics on systems biology and biotechnology. Biotechnology Advances 30, 469–488. PubMed

Chapman CA, Gillespie TR and Goldberg TL (2005) Primates and the ecology of their infectious diseases: how will anthropogenic change affect host–parasite interactions? Evolutionary Anthropology: Issues, News, and Reviews 14, 134–144.

Conole JC, Chilton NB, Järvis T and Gasser RB (1999) Intraspecific and interspecific variation in the second internal transcribed spacer sequence for Metastrongylus (Nematoda: Metastrongyloidea) detected by high resolution PCR-linked restriction fragment length polymorphism. International Journal for Parasitology 29, 1935–1940. PubMed

Cooper N, Griffin R, Franz M, Omotayo M and Nunn CL (2012) Phylogenetic host specificity and understanding parasite sharing in primates. Ecology Letters 15, 1370–1377. PubMed

Cozzolino R, Cordischi C, Aureli F and Scucchi S (1992) Environmental temperature and reproductive seasonality in Japanese macaques (Macaca fuscata). Primates 33, 329–336.

Dallas TA, Han BA, Nunn CL, Park AW, Stephens PR and Drake JM (2019) Host traits associated with species roles in parasite sharing networks. Oikos 128, 23–32.

de Boeck P, Bakker M, Zwitser R, Nivard M, Hofman A, Tuerlinckx F and Partchev I (2011) The estimation of item response models with the lmer function from the lme4 package in R. Journal of Statistical Software 39, 1–28.

Deplazes P, Eckert J, Mathis A, von Samson-Himmelstjerna G and Zahner H (2016) Parasitology in Veterinary Medicine. Wageningen, Netherlands: Wageningen Academic Publisher.

De Vienne DM, Giraud T and Shykoff JA (2007) When can host shifts produce congruent host and parasite phylogenies? A simulation approach. Journal of Evolutionary Biology 20, 1428–1438. PubMed

Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Di Fiore A, Anne-Isola Nekaris K, Nijman V, Heymann EW, Lambert JE, Rovero F, Barelli C, Setchell JM, Gillespie TR, Mittermeier RA, Arregoitia LV, de Guinea M, Gouveia S, Dobrovolski R, Shanee S, Shanee N, Boyle SA, Fuentes A, MacKinnon KC, Amato KR, Meyer ALS, Wich S, Sussman RW, Pan R, Kone I and Li B (2017) Impending extinction crisis of the world's primates: why primates matter. Science Advances 3, 26. PubMed PMC

Fernández D, Kerhoas D, Dempsey A, Billany J, McCabe G and Argirova E (2022) The current status of the world's primates: mapping threats to understand priorities for primate conservation. International Journal of Primatology 43, 15–39. PubMed PMC

Fernando SU, Udagama PV and Fernando SP (2022) Effect of urbanization on zoonotic gastrointestinal parasite prevalence in endemic toque macaque (Macaca sinica) from different climatic zones in Sri Lanka. International Journal for Parasitology: Parasites and Wildlife 17, 100–109. PubMed PMC

Fonti N, Parisi F, Mancianti F, Freer G and Poli A (2023) Cancerogenic parasites in veterinary medicine: a narrative literature review. Infectious Agents and Cancer 2023 18:1 18, 1–27. PubMed PMC

Fooden J (1982) Ecogeographic segregation of macaque species. Primates 23, 574–579.

Frias L and MacIntosh AJJ (2020) Global diversity and distribution of soil-transmitted helminths in monkeys. In Jones-Engel L and Knauf S (eds), Neglected Diseases in Monkeys. Cham, Switzerland: Springer Nature, pp. 291–322. doi: 10.1007/978-3-030-52283-4_13 DOI

Frias L, Stark DJ, Lynn MS, Nathan SK, Goossens B, Okamoto M and MacIntosh AJJ (2018) Lurking in the dark: cryptic strongyloides in a Bornean slow loris. International Journal for Parasitology: Parasites and Wildlife 7, 141–146. PubMed PMC

Frias L, Stark DJ, Salgado Lynn M, Nathan S, Goossens B, Okamoto M and MacIntosh AJJ (2019) Molecular characterization of nodule worm in a community of Bornean primates. Ecology and Evolution 9, 3937–3945. PubMed PMC

Frias L, Hasegawa H, Chua TH, Sipangkui S, Stark DJ, Salgado-Lynn M, Goossens B, Keuk K, Okamoto M and MacIntosh AJJ (2021) Parasite community structure in sympatric Bornean primates. International Journal for Parasitology 51, 925–933. PubMed

Ghai RR, Chapman CA, Omeja PA, Davies TJ and Goldberg TL (2014) Nodule worm infection in humans and wild primates in Uganda: cryptic species in a newly identified region of human transmission. PLOS Neglected Tropical Diseases 8, e2641. PubMed PMC

Gillespie TR, Nunn CL and Leendertz FH (2008) Integrative approaches to the study of primate infectious disease: implications for biodiversity conservation and global health. American Journal of Physical Anthropology 137, 53–69. PubMed

Gotoh S (2000) Regional differences in the infection of wild Japanese macaques by gastrointestinal Helminth parasites. Primates 41, 291–298. PubMed

Halvarsson P and Tydén E (2023) The complete ITS2 barcoding region for Strongylus vulgaris and Strongylus edentatus. Veterinary Research Communications 47, 1767–1771. PubMed PMC

Hartig F (2020) DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package.

Hatcher MJ, Dick JTA and Dunn AM (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Frontiers in Ecology and the Environment 10, 186–194.

Hayaishi S and Kawamoto Y (2006) Low genetic diversity and biased distribution of mitochondrial DNA haplotypes in the Japanese macaque (Macaca fuscata yakui) on Yakushima Island. Primates 47, 158–164. PubMed

Hoang DT, Chernomor O, Von Haeseler A, Minh BQ and Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35, 518–522. PubMed PMC

Hudson PJ and Dobson AP (1995) Macroparasites: observed patterns in naturally fluctuating animal populations. Ecology of Infectious Diseases in Natural Populations 5, 144–176.

Ilík V, Kreisinger J, Modrý D, Schwarz EM, Tagg N, Mbohli D, Nkombou IC, Petrželková KJ and Pafčo B (2023) High diversity and sharing of strongylid nematodes in humans and great apes co-habiting an unprotected area in Cameroon. PLOS Neglected Tropical Diseases 17, e0011499. PubMed PMC

Irwin DM, Kocher TD and Wilson AC (1991) Evolution of the cytochrome b gene of mammals. Journal of Molecular Evolution 32, 128–144. PubMed

Ito T, Hayakawa T, Suzuki–Hashido N, Hamada Y, Kurihara Y, Hanya G, Kaneko A, Natsume T, Aisu S, Honda T, Yachimori S, Anezaki T, Omi T, Hayama SI, Tanaka M, Wakamori H, Imai H and Kawamoto Y (2021) Phylogeographic history of Japanese macaques. Journal of Biogeography 48, 1420–1431.

Jex AR, Lim YAL, Bethony JM, Hotez PJ, Young ND and Gasser RB (2011) Soil-transmitted helminths of humans in Southeast Asia—towards integrated control. Advances in Parasitology 74, 231–265. PubMed

Jiang H, Lei R, Ding SW and Zhu S (2014) Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 15, 182. PubMed PMC

Kalousová B, Piel AK, Pomajbíková K, Modrý D, Stewart FA and Petrželková KJ (2014) Gastrointestinal parasites of Savanna Chimpanzees (Pan troglodytes schweinfurthii) in Ugalla, Tanzania. International Journal of Primatology 35, 463–475.

Kalyaanamoorthy S, Minh BQ, Wong TKF, Von Haeseler A and Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 2017 14:6 14, 587–589. PubMed PMC

Kawamoto Y, Shotake T, Nozawa K, Kawamoto S, Tomari IK, Kawai S, Shirai K, Morimitsu Y, Takagi N, Akaza H, Fujii H, Hagihara K, Aizawa K, Akachi S, Oi T and Hayaishi S (2007) Postglacial population expansion of Japanese macaques (Macaca fuscata) inferred from mitochondrial DNA phylogeography. Primates 48, 27–40. PubMed

Kircher M and Kelso J (2010) High-throughput DNA sequencing – concepts and limitations. BioEssays 32, 524–536. PubMed

Knapp-Lawitzke F, Küchenmeister F, Küchenmeister K, von Samson-Himmelstjerna G and Demeler J (2014) Assessment of the impact of plant species composition and drought stress on survival of strongylid third-stage larvae in a greenhouse experiment. Parasitology Research 113, 4123–4131. PubMed

Krief S, Jamart A, Mahé S, Leendertz FH, Mätz-Rensing K, Crespeau F, Bain O and Guillot J (2008) Clinical and pathologic manifestation of oesophagostomosis in African great apes: does self-medication in wild apes influence disease progression? Journal of Medical Primatology 37, 188–195. PubMed

Kumar S, Sundararaj P, Kumara HN, Pal A, Santhosh K and Vinoth S (2018) Prevalence of gastrointestinal parasites in bonnet macaque and possible consequences of their unmanaged relocations. PLOS ONE 13, e0207495. PubMed PMC

Kurniawati D, Kurniawati DA, Suwanti LT, Lastuti NDR, Kusdarto S, Suprihati E, Mufasirin M and Pratiwi A (2020) Zoonotic potential of gastrointestinal parasite in long-tailed Macaque Macaca fascicularis at Baluran National Park, Situbondo, East Java, Indonesia. Aceh Journal of Animal Science 5, 47–56.

Letunic I and Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research 49, W293–W296. PubMed PMC

Lim-Leroy A and Chua TH (2020) Prevalence and risk factors of geohelminthiasis among the rural village children in Kota Marudu, Sabah, Malaysia. PLOS ONE 15, e0239680. PubMed PMC

Marmi J, Bertranpetit J, Terradas J, Takenaka O and Domingo-Roura X (2004) Radiation and phylogeography in the Japanese macaque, Macaca fuscata. Molecular Phylogenetics and Evolution 30, 676–685. PubMed

Mason B, Petrzelkova KJ, Kreisinger J, Bohm T, Cervena B, Fairet E, Fuh T, Gomez A, Knauf S, Maloueki U, Modry D, Shirley MH, Tagg N, Wangue N and Pafco B (2022) Gastrointestinal symbiont diversity in wild gorilla: a comparison of bacterial and strongylid communities across multiple localities. Molecular Ecology 31, 4127–4145. PubMed

Mclean ER, Kinsella JM, Chiyo P, Obanda V, Moss C and Archie EA (2012) Genetic identification of five strongyle nematode parasites in wild African elephants (Loxodonta africana). Journal of Wildlife Diseases 48, 707–716. PubMed

Medkour H, Castaneda S, Amona I, Fenollar F, André C, Belais R, Mungongo P, Muyembé-Tamfum JJ, Levasseur A, Raoult D, Davoust B and Mediannikov O (2021) Potential zoonotic pathogens hosted by endangered bonobos. Scientific Reports 2021 11:1 11, 1–16. PubMed PMC

Mittermeier RA, Valladares-Pádua C, Rylands AB, Eudey AA, Butynski TM, Ganzhorn JU, Kormos R, Aguiar JM and Walker S (2006) Primates in peril: the world's 25 most endangered primates, 2004–2006. Primate Conservation 2006, 1–28.

Muhangi D, Gardiner CH, Ojok L, Cranfield MR, Gilardi KVK, Mudakikwa AB and Lowenstine LJ (2021) Pathological lesions of the digestive tract in free-ranging mountain gorillas (Gorilla beringei beringei). American Journal of Primatology 83, e23290. PubMed

Mul IF, Paembonan W, Singleton I, Wich SA and Van Bolhuis HG (2007) Intestinal parasites of free-ranging, semicaptive, and captive Pongo abelii in Sumatra, Indonesia. International Journal of Primatology 28, 407–420.

Nunn C, Altizer S, Jones K and Sechrest W (2003) Comparative tests of parasite species richness in primates. American Naturalist 162, 597–614. PubMed

Obanda V, Maingi N, Muchemi G, Ng'Ang’A CJ, Angelone S and Archie EA (2019) Infection dynamics of gastrointestinal helminths in sympatric non-human primates, livestock and wild ruminants in Kenya. PLOS ONE 14, e0217929. PubMed PMC

Oksanen JF, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin P, O'Hara RB, Simpson GL, Solymos P, Stevens H, Szoecs H and Wagner H (2019) Vegan: Community Ecology Package. R package version 2.5–5.

Pafčo B, Čížková D, Kreisinger J, Hasegawa H, Vallo P, Shutt K, Todd A, Petrželková KJ and Modrý D (2018) Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Scientific Reports 8, 5933. doi: 10.1038/s41598-018-24126-3 PubMed DOI PMC

Pafčo B, Kreisinger J, Čížková D, Pšenková-Profousová I, Shutt-Phillips K, Todd A, Fuh T, Petrželková KJ and Modrý D (2019) Genetic diversity of primate strongylid nematodes: do sympatric nonhuman primates and humans share their strongylid worms? Molecular Ecology 28, 4786–4797. PubMed

Phosuk I, Intapan PM, Sanpool O, Janwan P, Thanchomnang T, Sawanyawisuth K, Morakote N and Maleewong W (2013) Molecular evidence of Trichostrongylus colubriformis and Trichostrongylus axei infections in humans from Thailand and Lao PDR. The American Journal of Tropical Medicine and Hygiene 89, 376–379. PubMed PMC

Pit D, Polderman A, Baeta S, Schulz-Key H and Soboslay P (2001) Parasite-specific antibody and cellular immune responses in humans infected with Necator americanus and Oesophagostomum bifurcum. Parasitology Research 87, 722–729. PubMed

Poissant J, Gavriliuc S, Bellaw J, Redman EM, Avramenko RW, Robinson D, Workentine ML, Shury TK, Jenkins EJ, McLoughlin PD, Nielsen MK and Gilleard JS (2021) A repeatable and quantitative DNA metabarcoding assay to characterize mixed strongyle infections in horses. International Journal for Parasitology 51, 183–192. PubMed

Sharifdini M, Derakhshani S, Alizadeh SA, Ghanbarzadeh L, Mirjalali H, Mobedi I and Saraei M (2017) Molecular identification and phylogenetic analysis of human Trichostrongylus species from an endemic area of Iran. Acta Tropica 176, 293–299. PubMed

Silangwa SM and Todd AC (1964) Vertical migration of trichostrongylid larvae on grasses. The Journal of Parasitology 50, 278–285. PubMed

Sirima C, Bizet C, Hamou H, Červená B, Lemarcis T, Esteban A, Peeters M, Mpoudi Ngole E, Mombo IM, Liégeois F, Petrželková KJ, Boussinesq M and Locatelli S (2021) Soil-transmitted helminth infections in free-ranging non-human primates from Cameroon and Gabon. Parasites and Vectors 14, 1–18. PubMed PMC

Thierry B (2007) Unity in diversity: lessons from macaque societies. Evolutionary Anthropology: Issues, News, and Reviews 16, 224–238.

Trifinopoulos J, Nguyen LT, von Haeseler A and Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44, W232–W235. PubMed PMC

Tsuji Y, Kazahari N, Kitahara M and Takatsuki S (2008) A more detailed seasonal division of the energy balance and the protein balance of Japanese macaques (Macaca fuscata) on Kinkazan Island, northern Japan. Primates 49, 157–160. PubMed

von Bubnoff A (2008) Next-generation sequencing: the race is on. Cell 132, 721–723. PubMed

Walker JG and Morgan ER (2014) Generalists at the interface: nematode transmission between wild and domestic ungulates. International Journal for Parasitology: Parasites and Wildlife 3, 242–250. PubMed PMC

Wang Q, Garrity GM, Tiedje JM and Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 5261–5267. PubMed PMC

Yalcindag E, Stuart P, Hasegawa H, Streit A, Doležalová J, Morrogh-Bernard H, Cheyne SM, Nurcahyo W and Foitová I (2021) Genetic characterization of nodular worm infections in Asian Apes. Scientific Reports 2021 11:1 11, 1–11. PubMed PMC

Zajac AM (2006) Gastrointestinal nematodes of small ruminants: life cycle, anthelmintics, and diagnosis. Veterinary Clinics of North America – Food Animal Practice 22, 529–541. PubMed

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