Abstract
The microsporidium Nosema pyrausta (Paillot) Weiser, 1961 plays an important role in the mortality of the European corn borer Ostrinia nubilalis (Hübner, 1796), and shows high virulence to the beet webworm Loxostege sticticalis (Linnaeus, 1761). In contrast, the greater wax moth Galleria mellonella (Linnaeus, 1758) and the gypsy moth Lymantria dispar (Linnaeus, 1758) are referred to as resistant hosts, slightly susceptible to this microparasite. The goal of the present study was to test N. pyrausta against a broad range of lepidopteran species with different taxonomy, physiology, and ecology. The susceptibility to N. pyrausta spores fluctuated greatly among members of various families and superfamilies of Lepidoptera. As many as 13 species tested were found to be refractory (not able to support the development of the microsporidium), including three species of Yponomeutoidea, four species of Papilionoidea, one species of Pyraloidea, two species of Bombycoidea, and three species of Noctuoidea. The species found to be susceptible (with a high proportion of specimens displaying developed infection) included: Evergestis forficalis (Linnaeus, 1758) (Crambidae), Aglais urticae (Linnaeus, 1758) (Nymphalidae), and Dendrolimus sibiricus Chetverikov, 1908 (Lasiocampidae). The species newly found to be highly susceptible (high proportion of infected insects accompanied with high levels of early mortality) were: Spodoptera exigua (Hübner, 1808) (Noctuidae) and Aglais io (Linnaeus, 1758). Large quantities of spores can be produced in vivo using substitute laboratory host A. urticae. These results confirm previous observations that physiological host range of microsporidia (observed under experimental conditions) is broader than the ecological one (observed in nature).
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215 (3): 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Andreadis TG, Maier CT, Lemmon CR (1996) Orthosomella lambdinae n. sp. (Microsporida: Unikaryonidae) from the Spring Hemlock Looper, Lambdina athasaria (Lepidoptera: Geometridae). Journal of Invertebrate Pathology 67 (2): 169–177. https://doi.org/10.1006/jipa.1996.0025
Andreeva IV, Shatalova EI, Khodakova AV (2021) The diamondback moth Plutella xylostella: ecological and biological aspects, harmfulness, population control. Plant Protection News 104: 28–39. https://doi.org/10.31993/2308-6459-2021-104-1-14947 [In Russian]
Bass D, Czech L, Williams BAP, Berney C, Dunthorn M, Mahé F, Torruella G, Stentiford GD, Williams TA (2018) Clarifying the Relationships between Microsporidia and Cryptomycota. Journal of Eukaryotic Microbiology 65 (6): 773–782. https://doi.org/10.1111/jeu.12519
Bhat SA, Bashir I, Kamili AS (2009) Microsporidiosis of silkworm, Bombyx mori L. (Lepidoptera-Bombycidae): a review. African Journal of Agricultural Research 4 (11): 1519– 1523. https://academicjournals.org/journal/AJAR/article-full-text-pdf/39FAD8E32259
Cali A, Garhy ME (1991) Ultrastructural study of the development of Pleistophora schubergi Zwölfer, 1927 (Protozoa, Microsporida) in larvae of the spruce budworm, Choristoneura fumiferana and its subsequent taxonomic change to the genus Endoreticulatus. Journal of Protozoology 38 (3): 271–278. https://doi.org/10.1111/j.1550-7408.1991.tb04442.x
Canning EU, Barker RJ, Nicholas JP, Page AM (1985) The ultrastructure of three microsporidia from winter moth, Operophtera brumata (L.), and the establishment of a new genus Cystosporogenes n.g. for Pleistophora operophterae (Canning, 1960). Systematic Parasitology 7 (3): 213–225. https://link.springer.com/article/10.1007/BF00011452
Corsaro D, Wylezich C, Venditti D, Michel R, Walochnik J, Wegensteiner R (2019) Filling gaps in the microsporidian tree: rDNA phylogeny of Chytridiopsis typographi (Microsporidia: Chytridiopsida). Parasitology Research 118 (1): 169–180. https://doi.org/10.1007/s00436-018-6130-1
van Frankenhuyzen K, Nystrom C, Liu Y (2007) Vertical transmission of Nosema fumiferanae (Microsporidia: Nosematidae) and consequences for distribution, post-diapause emergence and dispersal of second-instar larvae of the spruce budworm, Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae). Journal of Invertebrate Pathology 96 (2): 173–182. https://doi.org/10.1016/j.jip.2007.03.017
Franz JM, Huger AM (1970) Microsporidia causing the collapse of an outbreak of the green tortrix Tortrix viridana L. in Germany. Proceedings: 4th International Colloquium on Insect Pathology. College Park, MD, 48–53.
Frolov AN (2019) Patterns of pest population dynamics and phytosanitary forecast. Plant Protection News 3 (101): 4–33. https://doi.org/10.31993/2308-6459-2019-3(101)-4-33
Grushevaya IV, Ignatieva AN, Malysh SM, Senderskiy IV, Zubarev IV, Kononchuk AG (2018) Spore dimorphism in Nosema pyrausta (Microsporidia, Nosematidae): from morphological evidence to molecular genetic verification. Acta Protozoologica 57: 49–52. https://doi.org/10.4467/16890027AP.18.004.8398
Grushevaya I, Ignatieva A, Tokarev Y (2020) Susceptibility of three species of the genus Ostrinia (Lepidoptera: Crambidae) to Nosema pyrausta (microsporidia: Nosematida). BIO Web of Conferences 21: 00040. https://doi.org/10.1051/bioconf/20202100040
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
Hall IM (1952) Observations on Perezia pyraustae Paillot, a microsporidian parasite of the European corn borer. Journal of Parasitology 38: 48–52. https://doi.org/10.2307/3274171
Hebert PD, Penton EH, Burns JM, Janzen DH, Halwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences USA 101 (41): 14812–14817. https://doi.org/10.1073/pnas.0406166101
Hopper JV, Huang WF, Solter LF, Mills NJ (2016) Pathogenicity, morphology, and characterization of a Nosema fumiferanae isolate (Microsporidia: Nosematidae) from the light brown apple moth, Epiphyas postvittana (Lepidoptera: Tortricidae) in California. Journal of Invertebrate Pathology 134: 38–47. https://doi.org/10.1016/j.jip.2016.01.001
Issi IV (1986) Microsporidia as a phylum of parasitic protozoa. Protozoology 10: 1–136. [In Russian].
Issi IV (2020) Development of Microsporidiology in Russia. Plant Protection News 103: 161–176. https://doi.org/10.31993/2308-6459-2020-103-3-4972 [In Russian]
Issi IV, Dolgikh VV, Sokolova YY, Tokarev YS (2005) Factors of pathogenicity of Microsporidia, the intracellular parasites of insects. Plant Protection News 3: 15–23. [In Russian]
Jeffords MR, Maddox JV, McManus ML, Webb RE, Wieber A (1989) Evaluation of the over- wintering success of two European microsporidia inoculatively released into gypsy moth populations in Maryland, USA. Journal of Invertebrate Pathology 53: 235–240. https://doi.org/10.1016/0022-2011(89)90012-8
Kirichenko NI, Baranchikov YN, Vidal S (2009) Performance of the potentially invasive Siberian moth Dendrolimus superans sibiricus on coniferous species in Europe. Agricultural and Forest Entomology 11: 247–254. https://doi.org/10.1111/j.1461-9563.2009.00437.x
Kononchuk AG, Martemyanov VV, Ignatieva AN, Belousova IA, Inoue MN, Tokarev YS (2021) Susceptibility of the gypsy moth Lymantria dispar (Lepidoptera: Erebidae) to Nosema pyrausta (Microsporidia: Nosematidae). Insects 12: 447. https://doi.org/10.3390/insects12050447
LeBrun EG, Jones M, Plowes RM, Gilbert LE (2022) Pathogen-mediated natural and manipulated population collapse in an invasive social insect. Proceedings of the National Academy of Sciences USA 119 (14): e2114558119. https://doi.org/10.1073/pnas.2114558119
Lewis LC, Bruck DJ, Prasifha JR, Raun ES (2009) Nosema pyrausta: Its biology, history, and potential role in a landscape of transgenic insecticidal crops. Biological Control 48 (3):223–231. https://doi.org/10.1016/j.biocontrol.2008.10.009
Lipa J, Madziara-Borusiewicz K (1976) Microsporidians parasitizing the green tortrix (Tortrix viridana L.) in Poland and their role in the collapse of the tortrix outbreak in Puszcza Niepolomicka during 1970–1974. Acta Protozoologica 15: 529–536.
Malysh YM, Tokarev YS, Sitnikova NV, Kononchuk AG, Grushetskaya TA, Frolov AN (2011) Incidence of microsporidian infection of stem borers of the genus Ostrinia (Lepidoptera: Crambidae) in the Krasnodar Territory. Parazitologiia 45: 234–244. [In Russian]
Malysh JM, Tokarev YS, Sitnicova NV, Martemyanov VV, Frolov AN, Issi IV (2013) Tubulinosema loxostegi sp. n. (Microsporidia: Tubulinosematidae) from the beet webworm Loxostege sticticalis L. (Lepidoptera: Crambidae) in Western Siberia. Acta Protozoologica 52: 299–308. http://doi.org/10.4467/16890027AP.13.027.1319
Malysh JM, Ignatieva AN, Artokhin KS, Frolov AN, Tokarev YS (2018) Natural infection of the beet webworm Loxostege sticticalis L. (Lepidoptera: Crambidae) with three Microsporidia and host switching in Nosema ceranae. Parasitology Research 117: 3039–3044. http://doi.org/10.1007/s00436-018-5987-3
Malysh JM, Kononchuk AG, Frolov AN (2019) Detection of microsporidia infecting beet webworm Loxostege sticticalis (Pyraloidea: Crambidae) in European part of Russia in 2006–2008. Plant Protection News 2: 45–51. https://doi.org/10.31993/2308-6459-2019-2(100)-45-51
Malysh JM, Chertkova EA, Tokarev YS (2021) The microsporidium Nosema pyrausta as a potent microbial control agent of the beet webworm Loxostege sticticalis. Journal of Invertebrate Pathology 186: 107675. https://doi.org/10.1016/j.jip.2021.107675
McManus ML, Solter L (2003) Microsporidian pathogens in European gypsy moth populations. Proceedings: Ecology, survey, and management of forest insects. USDA Forest Service, Northeastern Research Station - General Technical Report NE-311: 44–51.
Onstad DW (1993) Thresholds and density dependence: the roles of pathogen and insect densities in disease dynamics. Biological Control 3: 353–356.
Pelissie B, Ponsard S, Tokarev YS, Audiot Ph, Pelissier C, Sabatier R, Meusnier S, Chaufaux J, Delos M, Campan E, Malysh JM, Frolov AN, Bourguet D (2010) Did the introduction of maize into Europe provide enemy-free space to O. nubilalis? – Parasitism differences between two sibling species of the genus Ostrinia. Journal of Evolutionary Biology 23: 350–361. https://doi.org/10.1111/j.1420-9101.2009.01903.x
Shigano T, Hatakeyama Y, Nishimoto N, Watanabe M, Yamamoto Y, Wijonarko A, Ohbayashi T, Iwano H (2015) Variety and diversity of microsporidia isolated from the common cutworm Spodoptera litura in Chichijima, Ogasawara Islands. Journal of Insect Biotechnology and Sericology 84 (3): 69–73. https://doi.org/10.11416/jibs.84.3_069
Solter LF, Maddox JV (1998) Physiological host specificity of microsporidia as an indicator of ecological host specificity. Journal of Invertebrate Pathology 71 (3): 207–216. https://doi.org/10.1006/jipa.1997.4740
Solter LF, Maddox JV, McManus ML (1997) Host specificity of microsporidia (Protista: Microspora) from European populations of Lymantria dispar (Lepidoptera: Lymantriidae) to indigenous North American Lepidoptera. Journal of Invertebrate Pathology 69: 135– 150. https://doi.org/10.1006/jipa.1996.4650
Solter LF, Pilarska DK, McManus ML, Zúbrik M, Patočka J, Huang WF, Novotný J (2010) Host specificity of microsporidia pathogenic to the gypsy moth, Lymantria dispar (L.): Field studies in Slovakia. Journal of Invertebrate Pathology 105: 1–10. https://doi.org/10.1016/j.jip.2010.04.009
Tokarev YS, Malysh JM, Kononchuk AG, Seliverstova EV, Frolov AN, Issi IV (2015) Redefinition of Nosema pyrausta (Perezia pyraustae Paillot 1927) basing upon ultrastructural and molecular phylogenetic studies. Parasitology Research 114: 759–761. https://doi.org/10.1007/s00436-014-4272-3
Tokarev YS, Grizanova EV, Ignatieva AN, Dubovskiy IM (2018) Greater wax moth Galleria mellonella (Lepidoptera: Pyralidae) as a resistant model host for Nosema pyrausta (Microsporidia: Nosematidae). Journal of Invertebrate Pathology 157: 1–3. https://doi.org/10.1016/j.jip.2018.07.002
Tokarev YS, Huang WF, Solter LF, Malysh JM, Becnel JJ, Vossbrinck CR (2020) A formal redefinition of the genera Nosema and Vairimorpha (Microsporidia: Nosematidae) and reassignment of species based on molecular phylogenetics. Journal of Invertebrate Pathology 169: 107279. https://doi.org/10.1016/j.jip.2019.107279
Vilcinskas A (2019) Pathogens associated with invasive or introduced insects threaten the health and diversity of native species. Current Opinion in Insect Science 33: 43–48. https://doi.org/10.1016/j.cois.2019.03.004
Vogelweith F, Thiery D, Moret Y, Moreau J (2013) Immunocompetence increases with larval body size in a phytophagous moth. Physiological Entomology 38: 219–225. https://doi.org/10.1111/phen.12025
Weiss LM, Vossbrinck CR (1999) Molecular biology, molecular phylogeny, and molecular diagnostic approaches to the Microsporidia. In: Wittner M, Weiss LM (Eds) The Microsporidia and Microsporidiosis. ASM Press, Washington, 129–171. https://doi.org/10.1128/9781555818227.ch4
Zimmermann G, Huger AM, Langenbruch GA, Kleespies RG (2016) Pathogens of the European corn borer, Ostrinia nubilalis, with special regard to the microsporidium Nosema pyrausta. Journal of Pest Science 89: 329–346. https://doi.org/10.1007/s10340-016-0749-4
Genbank accession numbers:
https://www.ncbi.nlm.nih.gov/nuccore/HM566196
https://www.ncbi.nlm.nih.gov/nuccore/GU828662
https://www.ncbi.nlm.nih.gov/nuccore/KC836092
https://www.ncbi.nlm.nih.gov/nuccore/U26532
https://www.ncbi.nlm.nih.gov/nuccore/FN434087
https://www.ncbi.nlm.nih.gov/nuccore/LC422335
https://www.ncbi.nlm.nih.gov/nuccore/MG456600
https://www.ncbi.nlm.nih.gov/nuccore/D85503
https://www.ncbi.nlm.nih.gov/nuccore/ON256647 (will be made publicly available when the paper will be published; available at authors by request)
Acta Biologica Sibirica is a golden publisher, as we allow self-archiving, but most importantly we are fully transparent about your rights.
Authors may present and discuss their findings ahead of publication: at biological or scientific conferences, on preprint servers, in public databases, and in blogs, wikis, tweets, and other informal communication channels.
ABS allows authors to deposit manuscripts (currently under review or those for intended submission to ABS) in non-commercial, pre-print servers such as ArXiv.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).