Ultrastructural detection of intracellular bacterial symbionts in the wood-inhabiting nematode Bursaphelenchus mucronatus (Nematoda: Aphelenchoididae)
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Summary
Ultrastructural observations of the wood-inhabiting fungal- and plant-feeding nematode, Bursaphelenchus mucronatus, revealed intracellular bacteria in the male and female gonads. In males, bacteria were present inside the testis epithelial cells, spermatocytes, spermatids and immature spermatozoa. Spermatheca of females contained amoeboid pseudopod-bearing mature spermatozoa with bacteria closely associated with the sperm nucleus. Tissues of the females studied were free from bacteria. The gram-negative bacteria in their localisation, size, ultrastructure, and especially characteristic internal bundle of parallel filaments, were identified preliminary as related to the genus Cardinium (Bacteroidetes), which includes obligate endosymbionts of diverse arthropods and is known to be associated with several species of plant-parasitic nematodes.
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-
Atibalentja, N. & Noel, R.G. (2008). Bacterial endosymbionts of plant-parasitic nematodes. Symbiosis 46, 87-93.
-
Bigliardi, E., Sacchi, L., Genchi, M., Alma, A., Pajoro, M., Daffonchio, D., Marzorati, M. & Avanzati, A.M. (2006). Ultrastructure of a novel Cardinium sp. symbiont in Scaphoideus titanus (Hemiptera: Cicadellidae). Tissue and Cell 38, 257-261. DOI: 10.1016/j.tice.2006.06.001
-
Bright, M. & Bulgheresi, S. (2010). A complex journey: transmission of microbial symbionts. Nature reviews. Microbiology 8, 218-230. DOI: 10.1038/nrmicro2262
-
Brown, A.M.V. (2018). Endosymbionts of plant-parasitic nematodes. Annual Review of Phytopathology 56, 225-242. DOI: 10.1146/annurev-phyto-080417-045824
-
Coomans, A., Vandekerckhove, T.T.M. & Claeys, M. (2000). Transovarial transmission of symbionts in Xiphinema brevicollum (Nematoda: Longidoridae). Nematology 2, 443-449. DOI: 10.1163/156854100509303
-
Dallai, R., Mercati, D., Giusti, F., Gottardo, M. & Carapelli, A. (2011). A Cardinium-like symbiont in the proturan Acerella muscorum (Hexapoda). Tissue and Cell 43, 151-156. DOI: 10.1016/j.tice.2011.01.004
-
Denver, D.R., Brown, A.M.V., Howe, D.K., Peetz, A.B. & Zasada, I.A. (2016). Genome skimming: a rapid approach to gaining diverse biological insights into multicellular pathogens. PLOS Pathogens 12, e1005713. DOI: 10.1371/journal.ppat.1005713
-
Doremus, M.R., Kelly, S.E. & Hunter, M.S. (2019). Exposure to opposing temperature extremes causes comparable effects on Cardinium density but contrasting effects on Cardinium-induced cytoplasmic incompatibility. PLOS Pathogens 15, e1008022. DOI: 10.1371/journal.ppat.1008022
-
Endo, B.Y. (1979). The ultrastructure and distribution of an intracellular bacterium-like microorganism in tissues of larvae of the soybean cyst nematode, Heterodera glycines. Journal of Ultrastructure Research 67, 1-14. DOI: 10.1016/s0022-5320(79)80012-x
-
Guo, F., Castillo, P., Li, C., Qing, X. & Li, H. (2022). Description of Rotylenchus zhongshanensis sp. nov. (Tylenchomorpha: Hoplolaimidae) and discovery of its endosymbiont Cardinium. Journal of Helminthology 96, e48. DOI: 10.1017/S0022149X22000384
-
Kaur, R., Shropshire, J.D., Cross, K.L., Leigh, B., Mansueto, A.J., Stewart, V., Bordenstein, S.R. & Bordenstein, S.R. (2021). Living in the endosymbiotic world of Wolbachia: a centennial review. Cell Host & Microbe 29, 879-893. DOI: 10.1016/j.chom.2021.03.006
-
Kikuchi, Y. (2009). Endosymbiotic bacteria in insects: their diversity and culturability. Microbes and Environments 24, 195-204. DOI: 10.1264/jsme2.me09140s
-
Kim, B.-N., Kim, J.H., Ahn, J.-Y., Kim, S., Cho, B.-K., Kim, Y.-H. & Min, J. (2020). A short review of the pinewood nematode, Bursaphelenchus xylophilus. Toxicology and Environmental Health Sciences 12, 297-304. DOI: 10.1007/s13530-020-00068-0
-
Kitajima, E.W., Groot, T.V.M., Novelli, V.M., Freitas-Astúa, J., Alberti, G. & de Moraes, G.J. (2007). In situ observation of the Cardinium symbionts of Brevipalpus (Acari: Tenuipalpidae) by electron microscopy. Experimental and Applied Acarology 42, 263-271. DOI: 10.1007/s10493-007-9090-1
-
Manoj, R.R.S., Latrofa, M.S., Epis, S. & Otranto, D. (2021). Wolbachia: endosymbiont of onchocercid nematodes and their vectors. Parasites & Vectors 14, 245. DOI: 10.1186/s13071-021-04742-1
-
Marti, O., Rogers, C.E. & Styler, E.L. (1995). Report of an intracellular bacterial symbiont in Noctuidonema guyanense, an ectoparasitic nematode of Spodoptera frugiperda. Journal of Invertebrate Pathology 66, 94-96. DOI: 10.1006/jipa.1995.1068
-
Mota, M.M. & Vieira, P. (2008). Pine wilt disease: a worldwide threat to forest ecosystems. Dordrecht, The Netherlands, Springer. DOI: 10.1007/978-1-4020-8455-3
-
Musat, N., Giere, O., Gieseke, A., Thiermann, F., Amann, R. & Dubilier, N. (2007). Molecular and morphological characterization of the association between bacterial endosymbionts and the marine nematode Astomonema sp. from the Bahamas. Environmental Microbiology 9, 1345-1353. DOI: 10.1111/j.1462-2920.2006.01232.x
-
Nakamura, Y., Kawai, S., Yukuhiro, F., Ito, S., Gotoh, T., Kisimoto, R., Yanase, T., Matsumoto, Y., Kageyama, D. & Hiroaki, N. (2009). Prevalence of Cardinium bacteria in planthoppers and spider mites and taxonomic revision of “Candidatus Cardinium hertigii” based on detection of a new Cardinium group from biting midges. Applied and Environmental Microbiology 75, 6757-6763. DOI: 10.1128/AEM.01583-09
-
Noel, G.R. & Atibalentja, N. (2006). “Candidatus Paenicardinium endonii”, an endosymbiont of the plant-parasitic nematode Heterodera glycines (Nemata: Tylenchida), affiliated to the phylum Bacteroidetes. International Journal of Systematic and Evolutionary Microbiology 56, 1697-1702. DOI: 10.1099/ijs.0.64234-0
-
Palomares-Rius, J.E., Archidona-Yuste, A., Cantalapiedra-Navarrete, C., Prieto, P. & Castillo, P. (2016). Molecular diversity of bacterial endosymbionts associated with dagger nematodes of the genus Xiphinema (Nematoda: Longidoridae) reveals a high degree of phylogenetic congruence with their host. Molecular Ecology 25, 6225-6247. DOI: 10.1111/mec.13904
-
Palomares-Rius, J.E., Gutiérrez-Gutiérrez, C., Mota, M., Bert, M., Claeys, M., Yushin, V.V., Suzina, N.E., Ariskina, E.V., Evtushenko, L.I., Subbotin, S.A. et al. (2021). ‘Candidatus Xiphinematincola pachtaicus’ gen. nov., sp. nov., an endosymbiotic bacterium associated with nematode species of the genus Xiphinema (Nematoda, Longidoridae). International Journal of Systematic and Evolutionary Microbiology 71, 004888. DOI: 10.1099/ijsem.0.004888
-
Riegler, M. & O’Neill, S.L. (2006). The genus Wolbachia. In: Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.H. & Stackebrandt, E. (Eds). The prokaryotes. New York, NY, USA, Springer, pp. 547-561. DOI: 10.1007/0-387-30745-1_22
-
Sacchi, L., Genchi, M., Clementi, E., Bigliardi, E., Avanzati, A.M., Pajoro, M., Negri, I., Marzorati, M., Gonella, E., Alma, A. et al. (2008). Multiple symbiosis in the leafhopper Scaphoideus titanus (Hemiptera: Cicadellidae): details of transovarial transmission of Cardinium sp. and yeast-like endosymbionts. Tissue and Cell 40, 231-242. DOI: 10.1016/j.tice.2007.12.005
-
Sazama, E.J., Ouellette, S.P. & Wesner, J.S. (2019). Bacterial endosymbionts are common among, but not necessarily within, insect species. Environmental Entomology 48, 127-133. DOI: 10.1093/ee/nvy188
-
Shepherd, A.M. (1981). Interpretation of sperm development in nematodes. Nematologica 27, 122-125. DOI: 10.1163/187529281X00151
-
Shepherd, A.M., Clark, S.A. & Kempton, A. (1973). An intracellular micro-organism associated with tissues of Heterodera spp. Nematologica 19, 31-34. DOI: 10.1163/187529273X00060
-
Showmaker, K.C., Walden, K.K.O., Fields, C.J., Lambert, K.N. & Hudson, M.E. (2018). Genome sequence of the soybean cyst nematode (Heterodera glycines) endosymbiont “Candidatus Cardinium hertigii” strain cHgTN10. Genome Announcements 6, e00624-18. DOI: 10.1128/genomea.00624-18
-
Slos, D., Yushin, V.V., Claeys, M., Ivanova, E.S., Kosaka, H. & Bert, W. (2020). Structure, development, and evolutive patterns of spermatozoa in rhabditid nematodes (Nematoda: Rhabditida). Journal of Morphology 281, 1411-1435. DOI: 10.1002/jmor.21255
-
Taylor, M., Mediannikov, O., Raoult, D. & Greub, G. (2012). Endosymbiotic bacteria associated with nematodes, ticks and amoebae. FEMS Immunology & Medical Microbiology 64, 21-31. DOI: 10.1111/j.1574-695X.2011.00916.x
-
Taylor, M.J., Bandi, C. & Hoerauf, A. (2005). Wolbachia bacterial endosymbionts of filarial nematodes. Advances in Parasitology 60, 245-284. DOI: 10.1016/S0065-308X(05)60004-8
-
Tchesunov, A.V., Ingels, J. & Popova, E.V. (2012). Marine free-living nematodes associated with symbiotic bacteria in deep-sea canyons of north-east Atlantic Ocean. Journal of the Marine Biological Association of the United Kingdom 92, 1257-1271. DOI: 10.1017/s0025315411002116
-
Vandekerckhove, T.T.M., Willems, A., Gillis, M. & Coomans, A. (2000). Occurrence of novel verrucomicrobial species, endosymbiotic and associated with parthenogenesis in Xiphinema americanum-group species (Nematoda, Longidoridae). International Journal of Systematic and Evolutionary Microbiology 50, 2197-2205. DOI: 10.1099/00207713-50-6-2197
-
Walsh, J.A., Lee, D.L. & Shepherd, A.M. (1983a). The distribution and effect of intracellular rickettsia-like micro-organisms infecting adult males of the potato cyst-nematode Globodera rostochiensis. Nematologica 29, 227-239. DOI: 10.1163/187529283x00474
-
Walsh, J.A., Lee, D.L. & Shepherd, A.M. (1983b). The distribution and effect of intracellular rickettsia-like micro-organisms infecting second-stage juveniles of the potato cyst-nematode Globodera rostochiensis. Journal of Zoology 199, 395-419. DOI: 10.1111/j.1469-7998.1983.tb02104.x
-
Wang, M., Zhu, D., Dai, J., Zhong, Z., Zhang, Y. & Wang, J. (2018). Tissue localization and variation of major symbionts in Haemaphysalis longicornis, Rhipicephalus haemaphysaloides, and Dermacentor silvarum in China. Applied and Environmental Microbiology 84, e00029-18. DOI: 10.1128/aem.00029-18
-
Wasala, S.K., Brown, A.M.V., Kang, J., Howe, D.K., Peetz, A.B., Zasada, I.A. & Denver, D.R. (2019). Variable abundance and distribution of Wolbachia and Cardinium endosymbionts in plant-parasitic nematode field populations. Frontiers in Microbiology 10, 964. DOI: 10.3389/fmicb.2019.00964
-
Watanabe, K., Yukuhiro, F., Matsuura, Y., Fukatsu, T. & Noda, H. (2014). Intrasperm vertical symbiont transmission. Proceedings of the National Academy of Sciences of the United States of America 111, 7433-7437. DOI: 10.1073/pnas.1402476111
-
Weinert, L.A., Araujo-Jnr, E.V., Ahmed, M.Z. & Welch, J.J. (2015). The incidence of bacterial endosymbionts in terrestrial arthropods. Proceedings of the Royal Society B: Biological Sciences 282, 20150249. DOI: 10.1098/rspb.2015.0249
-
Werren, J.H., Baldo, L. & Clark, M.E. (2008). Wolbachia: master manipulators of invertebrate biology. Nature reviews. Microbiology 6, 741-751. DOI: 10.1038/nrmicro1969
-
White, J.A., Giorgini, M., Strand, M.R. & Pennacchio, F. (2013). Arthropod endosymbiosis and evolution. In: Minelli, A., Boxshall, G. & Fusco, G. (Eds). Arthropod biology and evolution. Berlin, Germany, Springer, pp. 441-477. https://link.springer.com/chapter/10.1007/978-3-642-36160-9_17
-
Yushin, V.V. & Ryss, A. (2011). Sperm development and structure in Bursaphelenchus mucronatus (Nematoda: Aphelenchoidea: Aphelenchoididae). Nematology 13, 395-407. DOI: 10.1163/138855410X526840
-
Yushin, V.V. & Ryss, A.Y. (2021). Ultrastructural observations of spermatogenesis in the fungivorous nematode Paraphelenchus myceliophthorus Goodey, 1958 (Rhabditida: Aphelenchoidea, Aphelenchidae). Nematology 23, 357-366. DOI: 10.1163/15685411-bja10046
-
Zchori-Fein, E. & Perlman, S.J. (2004). Distribution of the bacterial symbiont Cardinium in arthropods. Molecular Ecology 13, 2009-2016. DOI: 10.1111/j.1365-294X.2004.02203.x
-
Zchori-Fein, E., Gottlieb, Y., Kelly, S.E., Brown, J.K., Wilson, J.M., Karr, T.L. & Hunter, M.S. (2001). A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proceedings of the National Academy of Sciences of the United States of America 98, 12555-12560. DOI: 10.1073/pnas.221467498
-
Zchori-Fein, E., Perlman, S.J., Kelly, S.E., Katzir, N. & Hunter, M.S. (2004). Characterization of a ‘Bacteroidetes’ symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of ‘Candidatus Cardinium hertigii’. International Journal of Systematic and Evolutionary Microbiology 54, 961-968. DOI: 10.1099/ijs.0.02957-0
| All Time | Past 365 days | Past 30 Days | |
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Ultrastructural detection of intracellular bacterial symbionts in the wood-inhabiting nematode Bursaphelenchus mucronatus (Nematoda: Aphelenchoididae)
In: NematologySearch for other papers by Vladimir V. Yushin in
Current site
Google Scholar
PubMed
Search for other papers by Lyubov A. Gliznutsa in
Current site
Google Scholar
PubMed
Search for other papers by Alexander Ryss in
Current site
Google Scholar
PubMed
Summary
Ultrastructural observations of the wood-inhabiting fungal- and plant-feeding nematode, Bursaphelenchus mucronatus, revealed intracellular bacteria in the male and female gonads. In males, bacteria were present inside the testis epithelial cells, spermatocytes, spermatids and immature spermatozoa. Spermatheca of females contained amoeboid pseudopod-bearing mature spermatozoa with bacteria closely associated with the sperm nucleus. Tissues of the females studied were free from bacteria. The gram-negative bacteria in their localisation, size, ultrastructure, and especially characteristic internal bundle of parallel filaments, were identified preliminary as related to the genus Cardinium (Bacteroidetes), which includes obligate endosymbionts of diverse arthropods and is known to be associated with several species of plant-parasitic nematodes.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 797 | 427 | 58 |
| Full Text Views | 40 | 7 | 3 |
| PDF Views & Downloads | 88 | 9 | 2 |
