Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T09:20:40.610Z Has data issue: false hasContentIssue false
  • English
  • Français

Dive into the sea: first molecular phylogenetic evidence of host expansion from terrestrial/freshwater to marine organisms in Mermithidae (Nematoda: Mermithida)

Published online by Cambridge University Press:  06 May 2022

K. Kakui Open the ORCID record for K. Kakui [Opens in a new window]  and
D. Shimada Open the ORCID record for D. Shimada [Opens in a new window]
K. Kakui*
Affiliation:
Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan
D. Shimada
Affiliation:
Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan
*
Author for correspondence: K. Kakui, E-mail: kakui@eis.hokudai.ac.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

We report the first mermithid nematode found to be parasitic in a marine tanaidacean crustacean. Ten host tanaidaceans were collected from a depth of 52 m in Otsuchi Bay, Iwate, Japan, north-western Pacific, and identified as a species in the tanaidid genus Zeuxo Templeton, 1840. Nematodes occurred in the host's body cavity; in one case, at least two individuals inhabited a single host. We provide a brief description and illustrations of the morphology of the nematode. In a phylogenetic reconstruction based on the 18S ribosomal RNA gene, the nematode nested in a clade otherwise containing mermithids from terrestrial or freshwater hosts, showing an expansion in host utilization in Mermithidae Braun, 1883 from terrestrial/freshwater hosts to a marine organism.

Keywords

Endoparasiteintermediate hostphylogenyroundworm
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e33
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Current address: Center for Molecular Biodiversity Research, National Museum of Nature and Science, Tsukuba 305-0005, Japan.

References

Anderson, G (2020) Tanaidacea—forty years of scholarship, version 3.0. Available at https://aquila.usm.edu/tanaids30/5/ (accessed 22 February 2022).Google Scholar
Bamber, RN (2005) The tanaidaceans (Arthropoda: Crustacea: Peracarida: Tanaidacea) of Esperance, western Australia, Australia. pp. 613–727 in Wells, FE, Walker, DI and Kendrick, GA (Eds) The marine flora and fauna of Esperance, Western Australia. Perth, Western Australian Museum.Google Scholar
Bamber, RN and Boxshall, GA (2006) A new genus and species of the Langitanainae (Crustacea: Peracarida: Tanaidacea: Tanaidae) bearing a new genus and species of nicothoid parasite (Crustacea: Copepoda: Siphonostomatoida: Nicothoidae) from the New Caledonia slope. Species Diversity 11, 137–148.CrossRefGoogle Scholar
Belaich, MN, Buldain, D, Ghiringhelli, PD, Hyman, B, Micieli, MV and Achinelly, MF (2015) Nucleotide sequence differentiation of Argentine isolates of the mosquito parasitic nematode Strelkovimermis spiculatus (Nematoda: Mermithidae). Journal of Vector Ecology 40, 415–418.CrossRefGoogle Scholar
Chim, CK and Tong, SJW (2019) Xenosinelobus balanocolus, a new tanaidid genus and species (Crustacea: Peracarida: Tanaidacea) from barnacles on intertidal rocky shores and seawalls in the Singapore Strait. Zootaxa 4629, 413–427.CrossRefGoogle ScholarPubMed
Crainey, JL, Wilson, MD and Post, RJ (2009) An 18S ribosomal DNA barcode for the study of Isomermis lairdi, a parasite of the blackfly Simulium damnosum s.l. Medical and Veterinary Entomology 23, 238–244.CrossRefGoogle Scholar
Dusto, JA (2020) First record and description of a mermithid nematode infecting a marine decapod crustacean. MSc thesis, University of California San Diego. Available at https://escholarship.org/uc/item/4fm8v8cd (accessed 22 February 2022).Google Scholar
Gardiner, LF (1975) The systematics, postmarsupial development, and ecology of the deep-sea family Neotanaidae (Crustacea: Tanaidacea). Washington, Smithsonian Institution Press.CrossRefGoogle Scholar
Gillespie, JJ, Johnston, JS, Cannone, JJ and Gutell, RR (2006) Characteristics of the nuclear (18S, 5.8S, 28S and 5S) and mitochondrial (12S and 16S) rRNA genes of Apis mellifera (Insecta: Hymenoptera): structure, organization, and retrotransposable elements. Insect Molecular Biology 15, 657–686.CrossRefGoogle ScholarPubMed
Gruber, AR, Lorenz, R, Bernhart, SH, Neuböck, R and Hofacker, IL (2008) The Vienna RNA websuite. Nucleic Acids Research 36, W70–W74.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Holovachov, O and Boström, S (2013) Många nya arter av nematoder hittas i bottenslammet. Fauna och Flora 108, 28–34.Google Scholar
Holterman, M, van der Wurff, A, van den Elsen, S, van Megen, H, Bongers, T, Holovachov, O, Bakker, J and Helder, J (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution 23, 1792–1800.CrossRefGoogle ScholarPubMed
Hyman, BC, Tang, S, Wu, Z, Platzer, EG and Pacheco, R (2005) Haplotype hypervariation and rampant gene rearrangement shape mermithid nematode mitochondrial genome organization. Journal of Nematology 37, 373.Google Scholar
INSD (2022). International Nucleotide Sequence Database Collaboration. Available at https://www.insdc.org/ (accessed 22 February 2022).Google Scholar
Iryu, T, Tanaka, R and Yoshiga, T (2020) Mermithid nematodes isolated from the shield bug Parastrachia japonensis. Nematological Research 50, 1–7.CrossRefGoogle Scholar
Jakiel, A, Palero, F and Błażewicz, M (2019) Deep ocean seascape and Pseudotanaidae (Crustacea: Tanaidacea) diversity at the Clarion-Clipperton Fracture Zone. Scientific Reports 9, 17305.CrossRefGoogle ScholarPubMed
Kakui, K, Katoh, T, Hiruta, SF, Kobayashi, N and Kajihara, H (2011) Molecular systematics of Tanaidacea (Crustacea: Peracarida) based on 18S sequence data, with an amendment of suborder/superfamily-level classification. Zoological Science 28, 749–757.CrossRefGoogle ScholarPubMed
Kalyaanamoorthy, S, Minh, BQ, Wong, TKF, von Haeseler, A and Jermiin, LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587–589.CrossRefGoogle ScholarPubMed
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.CrossRefGoogle ScholarPubMed
Kobylinski, KC, Sylla, M, Black W, IV and Foy, BD (2012) Mermithid nematodes found in adult Anopheles from southeastern Senegal. Parasites & Vectors 5, 131.CrossRefGoogle ScholarPubMed
Kubo, R, Ugajin, A and Ono, M (2016) Molecular phylogenetic analysis of mermithid nematodes (Mermithida: Mermithidae) discovered from Japanese bumblebee (Hymenoptera: Bombinae) and behavioral observation of an infected bumblebee. Applied Entomology and Zoology 51, 549–554.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Larsen, K, Guţu, M and Sieg, J (2015) Order Tanaidacea Dana, 1849. pp. 249–329 in von Vaupel Klein, J, Charmantier-Daures, M and Schram, F (Eds) The Crustacea. Revised and updated, as well as extended from the traité de zoologie, Vol. 5. Leiden, Brill.Google Scholar
Lorenz, R, Bernhart, SH, Zu Siederdissen, CH, Tafer, H, Flamm, C, Stadler, PF and Hofacker, IL (2011) ViennaRNA package 2.0. Algorithms for Molecular Biology 6, 1–14.CrossRefGoogle ScholarPubMed
Maggenti, A (1981) General nematology (Springer series in microbiology). New York, Springer-Verlag.CrossRefGoogle Scholar
Martell, DJ and McClelland, G (1995) Transmission of Pseudoterranova decipiens (Nematoda: Ascaridoidea) via benthic macrofauna to sympatric flatfishes (Hippoglossoides platessoides, Pleuronectes ferrugineus, P. americanus) on Sable Island Bank, Canada. Marine Biology 122, 129–135.CrossRefGoogle Scholar
Mazza, G, Paoli, F, Strangi, A, et al. (2017) Hexamermis popilliae n. sp. (Nematoda: Mermithidae) parasitizing the Japanese beetle Popillia japonica Newman (Coleoptera: Scarabaeidae) in Italy. Systematic Parasitology 94, 915–926.CrossRefGoogle Scholar
Meldal, BHM, Debenham, NJ, de Ley, P, et al. (2007) An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Molecular Phylogenetics and Evolution 42, 622–636.CrossRefGoogle ScholarPubMed
Minh, BQ, Schmidt, HA, Chernomor, O, Schrempf, D, Woodhams, MD, von Haeseler, A and Lanfear, R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530–1534.CrossRefGoogle ScholarPubMed
Nemys (2022) Nemys: World Database of Nematodes. Available at https://nemys.ugent.be (accessed 24 February 2022).Google Scholar
Olia, M, Ahmad, W, Araki, M, Minaka, N, Oba, H and Okada, H (2008) Actus salvadoricus Baqri and Jairajpuri (Mononchida: Mylonchulidae) from Japan with comment on the phylogenetic position of the genus Actus based on 18S rDNA sequences. Japanese Journal of Nematology 38, 57–69.CrossRefGoogle Scholar
Pérez-Pacheco, R, Platzer, EG, Woodward, D and Hyman, BC (2015) Bioassays for comparative infectivity of mermithid nematodes (Romanomermis iyengari, Romanomermis culicivorax and Strelkovimermis spiculatus) for culicine mosquito larvae. Biological Control 80, 113–118.CrossRefGoogle Scholar
Poinar, GO Jr and Mullens, BA (1987) Heleidomermis magnapapula n. sp. (Mermithidae: Nematoda) parasitizing Culicoides variipennis (Ceratopogonidae: Diptera) in California. Revue de Nématologie 10, 387–391.Google Scholar
Poinar, GO Jr, Porter, SD, Tang, S and Hyman, BC (2007) Allomermis solenopsi n. sp. (Nematoda: Mermithidae) parasitising the fire ant Solenopsis invicta Buren (Hymenoptera: Formicidae) in Argentina. Systematic Parasitology 68, 115–128.CrossRefGoogle Scholar
Presswell, B, Evans, S, Poulin, R and Jorge, F (2015) Morphological and molecular characterization of Mermis nigrescens Dujardin, 1842 (Nematoda: Mermithidae) parasitizing the introduced European earwig (Dermaptera: Forficulidae) in New Zealand. Journal of Helminthology 89, 267–276.CrossRefGoogle ScholarPubMed
Rambaut, A (2022) FigTree v1.4.4. Available at http://tree.bio.ed.ac.uk/software/figtree/ (accessed 22 February 2022).Google Scholar
Ross, JL, Ivanova, ES, Spiridonov, SE, Waeyenberge, L, Moens, M, Nicol, GW and Wilson, MJ (2010) Molecular phylogeny of slug-parasitic nematodes inferred from 18S rRNA gene sequences. Molecular Phylogenetics and Evolution 55, 738–743.CrossRefGoogle ScholarPubMed
Sieg, J (1980) Taxonomische Monographie der Tanaidae Dana 1849 (Crustacea: Tanaidacea). Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 537, 1–267.Google Scholar
Stubbins, FL, Agudelo, P, Reay-Jones, FPF and Greene, JK (2016) Agamermis (Nematoda: Mermithidae) infection in South Carolina agricultural pests. Journal of Nematology 48, 290–296.CrossRefGoogle ScholarPubMed
Tchesunov, AV and Hope, WD (1997) Thalassomermis megamphis n. gen., n. sp. (Mermithidae: Nemata) from the bathyal South Atlantic Ocean. Journal of Nematology 29, 451–464.Google Scholar
Tchesunov, AV and Rozenberg, AA (2011) Data on the life cycle of parasitic benthimermithid nematodes with the description of a new species discovered in marine aquaria. Russian Journal of Nematology 19, 139–150.Google Scholar
Tchesunov, AV and Spiridorov, SE (1993) Nematimermis enoplivora gen. n., sp. n. (Nematoda: Mermithoidea) from marine free-living nematodes Enoplus spp. Journal of Russian Nematology 1, 7–16.Google Scholar
Tobias, ZJC, Jorge, F and Poulin, R (2017) Life at the beach: comparative phylogeography of a sandhopper and its nematode parasite reveals extreme lack of parasite mtDNA variation. Biological Journal of the Linnean Society 122, 113–132.CrossRefGoogle Scholar
Umbers, KDL, Byatt, LJ, Hill, NJ, Bartolini, RJ, Hose, GC, Herberstein, ME and Power, ML (2015) Prevalence and molecular identification of nematode and dipteran parasites in an Australian alpine grasshopper (Kosciuscola tristis). PLoS One 10, e0121685.CrossRefGoogle Scholar
Vandergast, AG and Roderick, GK (2003) Mermithid parasitism of Hawaiian Tetragnatha spiders in a fragmented landscape. Journal of Invertebrate Pathology 84, 128–136.CrossRefGoogle Scholar
Van Megen, H, van den Elsen, S, Holterman, M, Karssen, G, Mooyman, P, Bongers, T, Holovachov, O, Bakker, J and Helder, J (2009) A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11, 927–950.CrossRefGoogle Scholar
Wang, J-Y, Xu, F, Liu, X-S and Wang, G-X (2007) Molecular phylogeny of entomopathogenic nematodes (Mermithidae) inferred from DNA sequences of 18S rDNA, 28S rDNA, and COI genes. Acta Zoologica Sinica 53, 835–844 (in Chinese, English abstract).Google Scholar
Warren, MB, Dutton, HR, Whelan, NV, Yanong, RPE and Bullard, SA (2019) First record of a species of Mermithidae Braun, 1883 infecting a decapod, Palaemon paludosus (Palaemonidae). Journal of Parasitology 105, 237–247.Google Scholar
Watanabe, S, Tsunashima, A, Itoyama, K and Shinya, R (2021) Survey of mermithid nematodes (Mermithida: Mermithidae) infecting fruit-piercing stink bugs (Hemiptera: Pentatomidae) in Japan. Applied Entomology and Zoology 56, 27–39.CrossRefGoogle Scholar
Westerman, R, Neves, BM, Ahmed, M and Holovachov, O (2021) Aborjinia corallicola sp. n., a new nematode species (Nematoda: Marimermithidae) associated with the bamboo coral Acanella arbuscula (Johnson). Systematic Parasitology 98, 559–579.CrossRefGoogle Scholar
Winterton, SL, Hardy, NB and Wiegmann, BM (2010) On wings of lace: phylogeny and Bayesian divergence time estimates of Neuropterida (Insecta) based on morphological and molecular data. Systematic Entomology 35, 349–378.CrossRefGoogle Scholar
Yeates, GW and Buckley, TR (2009) First records of mermithid nematodes (Nematoda: Mermithidae) parasitising stick insects (Insecta: Phasmatodea). New Zealand Journal of Zoology 36, 35–39.CrossRefGoogle Scholar
Yoshino, H and Waki, T (2021) First report on Mermithidae (Mermithida) infection in Ligidium sp. (Isopoda, Ligiidae). Parasitology International 82, 102304.CrossRefGoogle Scholar
Supplementary material: File

Kakui and Shimada supplementary material

Kakui and Shimada supplementary material

Download Kakui and Shimada supplementary material(File)
File 45.5 KB