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A new microsporidium Percutemincola moriokae gen. nov., sp. nov. from Oscheius tipulae: A novel model of microsporidia–nematode associations

Published online by Cambridge University Press:  17 April 2018

Kenji Nishikori Open the ORCID record for Kenji Nishikori [Opens in a new window] ,
Davin H. E. Setiamarga ,
Takahiro Tanji ,
Eisuke Kuroda ,
Hirohisa Shiraishi  and
Ayako Ohashi-Kobayashi
Kenji Nishikori*
Affiliation:
Department of Immunobiology, School of Pharmacy, Iwate Medical University, Nishitokuta 2-1-1, Yahaba, Shiwa, Iwate, Japan
Davin H. E. Setiamarga
Affiliation:
Department of Applied Chemistry and Biochemistry, National Institute of Technology, Wakayama College, Noda, Noshima 77, Gobo City, Wakayama, Japan The University Museum, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo, Japan
Takahiro Tanji
Affiliation:
Department of Immunobiology, School of Pharmacy, Iwate Medical University, Nishitokuta 2-1-1, Yahaba, Shiwa, Iwate, Japan
Eisuke Kuroda
Affiliation:
Department of Immunobiology, School of Pharmacy, Iwate Medical University, Nishitokuta 2-1-1, Yahaba, Shiwa, Iwate, Japan
Hirohisa Shiraishi
Affiliation:
Department of Immunobiology, School of Pharmacy, Iwate Medical University, Nishitokuta 2-1-1, Yahaba, Shiwa, Iwate, Japan
Ayako Ohashi-Kobayashi
Affiliation:
Department of Immunobiology, School of Pharmacy, Iwate Medical University, Nishitokuta 2-1-1, Yahaba, Shiwa, Iwate, Japan
*
Author for correspondence: Kenji Nishikori, E-mail: knishiko@iwate-med.ac.jp
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Abstract

Here, we describe a new microsporidium Percutemincola moriokae gen. nov., sp. nov., which was discovered in the intestinal and hypodermal cells of a wild strain of the nematode Oscheius tipulae that inhabits in the soil of Morioka, Iwate Prefecture, Japan. The spores of Pe. moriokae had an average size of 1.0 × 3.8 µm and 1.3 × 3.2 µm in the intestine and hypodermis, respectively, and electron microscopy revealed that they exhibited distinguishing features with morphological diversity in the hypodermis. Isolated spores were able to infect a reference strain of O. tipulae (CEW1) through horizontal transmission but not the nematode Caenorhabditis elegans. Upon infection, the spores were first observed in the hypodermis and then in the intestine the following day, suggesting a unique infectious route among nematode-infective microsporidia. Molecular phylogenetic analysis grouped this new species with the recently identified nematode-infective parasites Enteropsectra and Pancytospora forming a monophyletic sister clade to Orthosomella in clade IV, which also includes human pathogens such as Enterocytozoon and Vittaforma. We believe that this newly discovered species and its host could have application as a new model in microsporidia–nematode association studies.

Keywords

Eukaryotic parasitesintracellular associationmicrosporidiosisnovel genusnovel speciesparasites of nematodes
Type
Research Article
Information
Parasitology , Volume 145 , Issue 14 , December 2018 , pp. 1853 - 1864
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Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

*

Present address: Department of Infection Microbiology, Research Institute for Microbial Diseases, Osaka University, Osaka, Japan.

References

Ardila-Garcia, AM and Fast, NM (2012) Microsporidian infection in a free-living marine nematode. Eukaryotic Cell 11, 1544–1551.Google Scholar
Ardila-Garcia, AM, et al. (2013) Microsporidian diversity in soil, sand, and compost of the pacific northwest. Journal of Eukaryotic Microbiology 60, 601–608.Google Scholar
Baïlle, D, Barrière, A and Félix, MA (2008) Oscheius tipulae, a widespread hermaphroditic soil nematode, displays a higher genetic diversity and geographical structure than Caenorhabditis elegans. Molecular Ecology 17, 1523–1534.Google Scholar
Bakowski, MA, et al. (2014) Ubiquitin-mediated response to microsporidia and virus infection in C. elegans. PLoS Pathology 10, e1004200.Google Scholar
Balla, KM, et al. (2015) A wild C. elegans strain has enhanced epithelial immunity to a natural microsporidian parasite. PLoS Pathology 11, e1004583.Google Scholar
Barrière, A and Félix, MA (2014) Isolation of C. elegans and related nematodes. In The C. elegans Research Community, WormBook (eds). WormBook. doi/10.1895/wormbook.1.115.2, http://www.wormbook.org.Google Scholar
Brenner, S (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71–94.Google Scholar
Cali, A (1991) General microsporidian features and recent findings on AIDS isolates. The Journal of Protozoology 38, 625–630.Google Scholar
Capella-Gutiérrez, S, Marcet-Houben, M and Gabaldón, T (2012) Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biology 10, 47.Google Scholar
Chan, CM, et al. (2003) Microsporidial keratoconjunctivitis in healthy individuals: a case series. Ophthalmology 110, 1420–1425.Google Scholar
Cho, SW, et al. (2013) Heritable gene knockout in Caenorhabditis elegans by direct injection of Cas9–sgRNA ribonucleoproteins. Genetics 195, 1177–1180.Google Scholar
Chu, JS, et al. (2014) High-throughput capturing and characterization of mutations in essential genes of Caenorhabditis elegans. BMC Genomics 5, 361.Google Scholar
Didier, ES and Weiss, LM (2011) Microsporidiosis: not just in AIDS patients. Current Opinion in Infectious Diseases 24, 490–495.Google Scholar
Eden, PA, et al. (1991) Phylogenetic analysis of Aquaspirillum magnetotacticum using polymerase chain reaction-amplified 16S rRNA-specific DNA. International Journal of Systematic and Evolutionary Microbiology 41, 324–325.Google Scholar
Fay, SD (2013) Classical genetic methods. In The C. elegans Research Community, WormBook (eds). WormBook. doi: 10.1895/wormbook.1.165.1, http://www.wormbook.org.Google Scholar
Félix, MA (2006) Oscheius tipulae. In The C. elegans Research Community, WormBook (eds). WormBook. doi: 10.1895/wormbook.1.119.1, http://www.wormbook.org.Google Scholar
Franzen, C and Müller, A (1999) Molecular techniques for detection, species differentiation, and phylogenetic analysis of microsporidia. Clinical Microbiology Reviews 12, 243–285.Google Scholar
Haag, KL, et al. (2014) Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites. Proceedings of the National Academy of Sciences of the United States of America 111, 15480–15485.Google Scholar
Han, B and Weiss, LM (2017) Microsporidia: obligate intracellular pathogens within the fungal kingdom. In Heitman, J, Howlett, B, Crous, P, Stukenbrock, E, James, T, Gow, N (eds), The Fungal Kingdom. Washington, DC: ASM Press, pp 97–113. doi: 10.1128/microbiolspec. FUNK-0018-2016.Google Scholar
Harris, JK, Kellye, ST and Pace, NR (2004) New perspective on uncultured bacterial phylogenetic division OP11. Applied and Environmental Microbiology 70, 845–849.Google Scholar
James, TY, et al. (2013) Shared signatures of parasitism and phylogenomics unite Cryptomycota and Microsporidia. Current Biology 23, 1548–1553.Google Scholar
Kawai, H, et al. (2009) Normal formation of a subset of intestinal granules in Caenorhabditis elegans requires ATP-binding cassette transporters HAF-4 and HAF-9, which are highly homologous to human lysosomal peptide transporter TAP-like. Molecular Biology of the Cell 20, 2979–2990.Google Scholar
Kumar, S, Stecher, G and Tamura, T (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Luallen, RJ, et al. (2016) Discovery of a natural microsporidian pathogen with a broad tissue tropism in Caenorhabditis elegans. PLoS Pathology 12, e1005724.Google Scholar
McGhee, JD (2007) The C. elegans intestine. In The C. elegans Research Community, WormBook (eds). WormBook. doi: 10.1895/wormbook.1.133.1, http://www.wormbook.org.Google Scholar
Sahl, JW, et al. (2008) Subsurface microbial diversity in deep-granitic-fracture water in Colorado. Applied and Environmental Microbiology 74, 143–152.Google Scholar
Sapir, A, et al. (2014) Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea. Frontiers in Microbiology 5, 43.Google Scholar
Sarin, S, et al. (2008) Caenorhabditis elegans mutant allele identification by whole-genome sequencing. Nature Methods 5, 865–867.Google Scholar
Silvestro, D and Michalak, I (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution 12, 335–337.Google Scholar
Sokolova, YY and Fuxa, JR (2008) Biology and life-cycle of the microsporidium Kneallhazia solenopsae Knell Allan Hazard 1977 gen. n., comb. n., from the fire ant Solenopsis invicta. Parasitology 135, 903–929.Google Scholar
Sokolova, YY, Lange, CE and Fuxa, JR (2007) Establishment of Liebermannia dichroplusae n. comb. on the basis of molecular characterization of Perezia dichroplusae Lange, 1987 (Microsporidia). Journal of Eukaryotic Microbiology 54, 223–230.Google Scholar
Sokolova, YY, et al. (2009) Morphology and taxonomy of the microsporidium Liebermannia covasacrae n. sp. From the grasshopper Covasacris pallidinota (Orthoptera, Acrididae). Journal of Invertebrate Pathology 101, 34–42.Google Scholar
Stamatakis, A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (oxford, England) 22, 2688–2690.Google Scholar
Stentiford, GD, et al. (2013) Microsporidia: diverse, dynamic, and emergent pathogens in aquatic systems. Trends in Parasitology 29, 567–578.Google Scholar
Szumowski, SC, et al. (2014) The small GTPase RAB-11 directs polarized exocytosis of the intracellular pathogen N. parisii for fecal-oral transmission from C. elegans. Proceedings of the National Academy of Sciences of the United States of America 111, 8215–8220.Google Scholar
Tanji, T, et al. (2016) Characterization of HAF-4- and HAF-9-localizing organelles as distinct organelles in Caenorhabditis elegans intestinal cells. BMC Cell Biology 17, 4.Google Scholar
Troemel, ER, et al. (2008) Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biology 6, e309.Google Scholar
Vávra, J and Lukeš, J (2013) Microsporidia and ‘The art of living together’. In Rollinson, D (ed). Advances in Parasitology, vol. 82. Amsterdam: Academic Press, Elsevier B.V, pp. 253–320.Google Scholar
Vávra, J, et al. (1998) Microsporidia of the genus Trachipleistophora−Causative agents of human microsporidiosis: description of Trachipleistophora anthropophthera n. sp. (Protozoa: Microsporidia). Journal of Eukaryotic Microbiology 45, 273–283.Google Scholar
Vávra, J, et al. (2006) Vairimorpha disparis n. comb. (Microsporidia: Burenellidae): a redescription and taxonomic revision of Thelohania disparis Timofejeva 1956, a microsporidian parasite of the gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae). Journal of Eukaryotic Microbiology 53, 292–304.Google Scholar
Vossbrinck, CR and Debrunner-Vossbrinck, BA (2005) Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitologica 52, 131–142.Google Scholar
Weber, R, Deplazes, P and Mathis, A (2011) Microsporidia. In Versalovic, J, Carroll, KC, Funke, G, Jorgensen, JH, Landry, ML and Warnock, DW (eds). Manual of Clinical Microbiology, 10th edn. Washington, DC: ASM Press, pp. 2190–2199.Google Scholar
Zhang, G, et al. (2016) A large collection of novel nematode-infecting microsporidia and their diverse interactions with Caenorhabditis elegans and other elated nematodes. PLoS Pathology 12, e1006093.Google Scholar
Zhu, X, et al. (1993) Nucleotide sequence of the small ribosomal RNA of Encephailtozoon cuniculi. Nucleic Acids Research 21, 1315.Google Scholar
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