Factors That Determine Microsporidia Infection and Host Specificity.
Genetic resistance
Host range
Host specificity
Microsporidia
Tissue specificity
Journal
Experientia supplementum (2012)
ISSN: 1664-431X
Titre abrégé: Exp Suppl
Pays: Switzerland
ID NLM: 101738007
Informations de publication
Date de publication:
2022
2022
Historique:
entrez:
11
5
2022
pubmed:
12
5
2022
medline:
17
5
2022
Statut:
ppublish
Résumé
Microsporidia are a large phylum of obligate intracellular parasites that infect an extremely diverse range of animals and protists. In this chapter, we review what is currently known about microsporidia host specificity and what factors influence microsporidia infection. Extensive sampling in nature from related hosts has provided insight into the host range of many microsporidia species. These field studies have been supported by experiments conducted in controlled laboratory environments which have helped to demonstrate host specificity. Together, these approaches have revealed that, while examples of generalist species exist, microsporidia specificity is often narrow, and species typically infect one or several closely related hosts. For microsporidia to successfully infect and complete their life cycle within a compatible host, several steps must occur, including spore germination, host cell invasion, and proliferation of the parasite within the host tissue. Many factors influence infection, including temperature, seasonality, nutrient availability, and the presence or absence of microbes, as well as the developmental stage, sex, and genetics of the host. Several studies have identified host genomic regions that influence resistance to microsporidia, and future work is likely to uncover molecular mechanisms of microsporidia host specificity in more detail.
Identifiants
pubmed: 35544000
doi: 10.1007/978-3-030-93306-7_4
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
91-114Informations de copyright
© 2022. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Aalto SL, Ketola T, Pulkkinen K (2014) No uniform associations between parasite prevalence and environmental nutrients. Ecology 95:2558–2568. https://doi.org/10.1890/13-2007.1
doi: 10.1890/13-2007.1
Andreadis TG (1984) Epizootiology of Nosema pyrausta in field populations of the European corn borer (Lepidoptera: Pyralidae). Environ Entomol 13:882–887. https://doi.org/10.1093/ee/13.3.882
doi: 10.1093/ee/13.3.882
Andreadis TG (1989) Host specificity of Amblyospora connecticus (Microsporida: Amblyosporidae), a polymorphic microsporidian parasite of Aedes cantator (Diptera: Culicidae). J Med Entomol 26:140–145. https://doi.org/10.1093/jmedent/26.3.140
doi: 10.1093/jmedent/26.3.140
pubmed: 2724310
Andreadis TG (1994) Host range tests with Edhazardia aedis (Microsporida: Culicosporidae) against Northern Nearctic mosquitoes. J Invertebr Pathol 64:46–51. https://doi.org/10.1006/jipa.1994.1067
doi: 10.1006/jipa.1994.1067
pubmed: 7914904
Andreadis TG, Simakova AV, Vossbrinck CR et al (2012) Ultrastructural characterization and comparative phylogenetic analysis of new microsporidia from Siberian mosquitoes: evidence for coevolution and host switching. J Invertebr Pathol 109:59–75. https://doi.org/10.1016/j.jip.2011.09.011
doi: 10.1016/j.jip.2011.09.011
pubmed: 22001630
Araújo-Coutinho CJPC, Nascimento ES, Figueiró R, Becnel JJ (2004) Seasonality and prevalence rates of microsporidia in Simulium pertinax (Diptera: Simuliidae) larvae in the region of Serra dos Órgãos, Rio de Janeiro, Brazil. J Invertebr Pathol 85:188–191. https://doi.org/10.1016/j.jip.2004.02.003
doi: 10.1016/j.jip.2004.02.003
pubmed: 15109902
Bacela-Spychalska K, Wróblewski P, Mamos T et al (2018) Europe-wide reassessment of Dictyocoela (microsporidia) infecting native and invasive amphipods (Crustacea): molecular versus ultrastructural traits. Sci Rep 8:8945. https://doi.org/10.1038/s41598-018-26879-3
doi: 10.1038/s41598-018-26879-3
pubmed: 29895884
pmcid: 5997659
Balla KM, Andersen EC, Kruglyak L, Troemel ER (2015) A wild C. elegans strain has enhanced epithelial immunity to a natural microsporidian parasite. PLoS Pathog 11:e1004583. https://doi.org/10.1371/journal.ppat.1004583
doi: 10.1371/journal.ppat.1004583
pubmed: 25680197
pmcid: 4334554
Balla KM, Lažetić V, Troemel ER (2019) Natural variation in the roles of C. elegans autophagy components during microsporidia infection. PLoS One 14:e0216011. https://doi.org/10.1371/journal.pone.0216011
doi: 10.1371/journal.pone.0216011
pubmed: 31013330
pmcid: 6478341
Becnel J (1992) Safety of Edhazardia aedis (Microspora: Amblyosporidae) for nontarget aquatic organisms. J Am Mosq Control Assoc 8(3):256–260
pubmed: 1357086
Becnel JJ, Johnson MA (1993) Mosquito host range and specificity of Edhazardia aedis (Microspora: Culicosporidae). J Am Mosq Control Assoc (USA) 9(3):269–274
Ben-Ami F, Rigaud T, Ebert D (2011) The expression of virulence during double infections by different parasites with conflicting host exploitation and transmission strategies. J Evol Biol 24:1307–1316. https://doi.org/10.1111/j.1420-9101.2011.02264.x
doi: 10.1111/j.1420-9101.2011.02264.x
pubmed: 21481055
Bjørnson S, Oi D (2014) Microsporidia biological control agents and pathogens of beneficial insects. In: Microsporidia. John Wiley & Sons, Chichester, pp 635–670
Blaser M, Schmid-Hempel P (2005) Determinants of virulence for the parasite Nosema whitei in its host Tribolium castaneum. J Invertebr Pathol 89:251–257. https://doi.org/10.1016/j.jip.2005.04.004
doi: 10.1016/j.jip.2005.04.004
pubmed: 15963529
Borges D, Guzman-Novoa E, Goodwin PH (2021) Effects of prebiotics and probiotics on honey bees (Apis mellifera) infected with the microsporidian parasite Nosema ceranae. Microorganisms 9:481. https://doi.org/10.3390/microorganisms9030481
doi: 10.3390/microorganisms9030481
pubmed: 33668904
pmcid: 7996622
Brown AMV, Kent ML, Adamson ML (2010) Low genetic variation in the salmon and trout parasite Loma salmonae (microsporidia) supports marine transmission and clarifies species boundaries. Dis Aquat Org 91:35–46. https://doi.org/10.3354/dao02246
doi: 10.3354/dao02246
Capaul M, Ebert D (2003) Parasite-mediated selection in experimental daphnia magna populations. Evolution 57:249–260. https://doi.org/10.1111/j.0014-3820.2003.tb00260.x
doi: 10.1111/j.0014-3820.2003.tb00260.x
pubmed: 12683522
Chen Y-W, Chung W-P, Wang C-H et al (2012) Nosema ceranae infection intensity highly correlates with temperature. J Invertebr Pathol 111:264–267. https://doi.org/10.1016/j.jip.2012.08.014
doi: 10.1016/j.jip.2012.08.014
pubmed: 22982233
Copley TR, Chen H, Giovenazzo P et al (2012) Prevalence and seasonality of Nosema species in Québec honey bees. Can Entomol 144:577–588. https://doi.org/10.4039/tce.2012.46
doi: 10.4039/tce.2012.46
Decaestecker E, Verreydt D, Meester LD, Declerck SAJ (2015) Parasite and nutrient enrichment effects on daphnia interspecific competition. Ecology 96:1421–1430. https://doi.org/10.1890/14-1167.1
doi: 10.1890/14-1167.1
pubmed: 26236854
Drozdova P, Madyarova E, Dimova M et al (2020) The diversity of microsporidian parasites infecting the Holarctic amphipod Gammarus lacustris from the Baikal region is dominated by the genus Dictyocoela. J Invertebr Pathol 170:107330. https://doi.org/10.1016/j.jip.2020.107330
doi: 10.1016/j.jip.2020.107330
pubmed: 31978415
Dunn AM, Smith JE (2001) Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes Infect 3:381–388. https://doi.org/10.1016/S1286-4579(01)01394-6
doi: 10.1016/S1286-4579(01)01394-6
pubmed: 11369275
El Jarkass HT, Reinke AW (2020) The ins and outs of host-microsporidia interactions during invasion, proliferation and exit. Cell Microbiol 22:e13247. https://doi.org/10.1111/cmi.13247
Forsgren E, Fries I (2010) Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet Parasitol 170:212–217. https://doi.org/10.1016/j.vetpar.2010.02.010
doi: 10.1016/j.vetpar.2010.02.010
pubmed: 20299152
Franchet A, Niehus S, Caravello G, Ferrandon D (2019) Phosphatidic acid as a limiting host metabolite for the proliferation of the microsporidium Tubulinosema ratisbonensis in drosophila flies. Nat Microbiol 4:645–655. https://doi.org/10.1038/s41564-018-0344-y
doi: 10.1038/s41564-018-0344-y
pubmed: 30692666
Gisder S, Horchler L, Pieper F et al (2020) Rapid gastrointestinal passage may protect Bombus terrestris from becoming a true host for Nosema ceranae. Appl Environ Microbiol 86:e00629–e00620
doi: 10.1128/AEM.00629-20
Gismondi E, Rigaud T, Beisel J-N, Cossu-Leguille C (2012) Microsporidia parasites disrupt the responses to cadmium exposure in a gammarid. Environ Pollut 160:17–23. https://doi.org/10.1016/j.envpol.2011.09.021
doi: 10.1016/j.envpol.2011.09.021
pubmed: 22035920
Grabner DS, Weigand AM, Leese F et al (2015) Invaders, natives and their enemies: distribution patterns of amphipods and their microsporidian parasites in the Ruhr Metropolis, Germany. Parasit Vectors 8:419. https://doi.org/10.1186/s13071-015-1036-6
doi: 10.1186/s13071-015-1036-6
pubmed: 26263904
pmcid: 4534018
Haag CR, Ebert D (2004) Parasite–mediated selection in experimental metapopulations of Daphnia magna. Proc R Soc Lond Ser B Biol Sci 271:2149–2155. https://doi.org/10.1098/rspb.2004.2841
doi: 10.1098/rspb.2004.2841
Han B, Takvorian PM, Weiss LM (2020) Invasion of host cells by microsporidia. Front Microbiol 11:172. https://doi.org/10.3389/fmicb.2020.00172
doi: 10.3389/fmicb.2020.00172
pubmed: 32132983
pmcid: 7040029
Hazard EI, Lofgren CS (1971) Tissue specificity and systematics of a Nosema in some species of Aedes, anopheles, and Cules. J Invertebr Pathol 18:16–24. https://doi.org/10.1016/0022-2011(91)90003-9
doi: 10.1016/0022-2011(91)90003-9
pubmed: 4398401
Hinney B, Sak B, Joachim A, Kváč M (2016) More than a rabbit’s tale – Encephalitozoon spp. in wild mammals and birds. Int J Parasitol: Parasites and Wildlife 5:76–87. https://doi.org/10.1016/j.ijppaw.2016.01.001
doi: 10.1016/j.ijppaw.2016.01.001
pmcid: 5439460
Huang Q, Kryger P, Le Conte Y et al (2014) Four quantitative trait loci associated with low Nosema ceranae (microsporidia) spore load in the honeybee Apis mellifera. Apidologie 45:248–256. https://doi.org/10.1007/s13592-013-0243-4
doi: 10.1007/s13592-013-0243-4
Ii ACG, Quandt CA (2020) A growing pandemic: a review of Nosema parasites in globally distributed domesticated and native bees. PLoS Pathog 16:e1008580. https://doi.org/10.1371/journal.ppat.1008580
doi: 10.1371/journal.ppat.1008580
Ironside JE, Wilkinson TJ, Rock J (2008) Distribution and host range of the microsporidian Pleistophora mulleri. J Eukaryot Microbiol 55:355–362. https://doi.org/10.1111/j.1550-7408.2008.00338.x
doi: 10.1111/j.1550-7408.2008.00338.x
pubmed: 18681850
Jack CJ, Uppala SS, Lucas HM, Sagili RR (2016) Effects of pollen dilution on infection of Nosema ceranae in honey bees. J Insect Physiol 87:12–19. https://doi.org/10.1016/j.jinsphys.2016.01.004
doi: 10.1016/j.jinsphys.2016.01.004
pubmed: 26802559
Jaroenlak P, Cammer M, Davydov A et al (2020) 3-dimensional organization and dynamics of the microsporidian polar tube invasion machinery. PLoS Pathog 16:e1008738. https://doi.org/10.1371/journal.ppat.1008738
doi: 10.1371/journal.ppat.1008738
pubmed: 32946515
pmcid: 7526891
Keller D, Kirk D, Luijckx P (2019) Four QTL underlie resistance to a microsporidian parasite that may drive genome evolution in its daphnia host. bioRxiv, 847194. https://doi.org/10.1101/847194
Kirk D, Jones N, Peacock S et al (2018) Empirical evidence that metabolic theory describes the temperature dependency of within-host parasite dynamics. PLoS Biol 16:e2004608. https://doi.org/10.1371/journal.pbio.2004608
doi: 10.1371/journal.pbio.2004608
pubmed: 29415043
pmcid: 5819823
Krebes L, Blank M, Frankowski J, Bastrop R (2010) Molecular characterisation of the microsporidia of the amphipod Gammarus duebeni across its natural range revealed hidden diversity, wide-ranging prevalence and potential for co-evolution. Infect Genet Evol 10:1027–1038. https://doi.org/10.1016/j.meegid.2010.06.011
doi: 10.1016/j.meegid.2010.06.011
pubmed: 20601176
Krebs M, Routtu J, Ebert D (2017) QTL mapping of a natural genetic polymorphism for long-term parasite persistence in daphnia populations. Parasitology 144:1686–1694. https://doi.org/10.1017/S0031182017001032
doi: 10.1017/S0031182017001032
pubmed: 28835307
Kucerova Z, Moura H, Visvesvara GS, Leitch GJ (2004) Differences between Brachiola (Nosema) algerae isolates of human and insect origin when tested using an in vitro spore germination assay Anda cultured cell infection assay. J Eukaryot Microbiol 51:339–343. https://doi.org/10.1111/j.1550-7408.2004.tb00577.x
doi: 10.1111/j.1550-7408.2004.tb00577.x
pubmed: 15218704
Lange CE (2005) The host and geographical range of the grasshopper pathogen Paranosema (Nosema) locustae revisited. J Orthoptera Res 14:137–141. https://doi.org/10.1665/1082-6467(2005)14[137:THAGRO]2.0.CO;2
doi: 10.1665/1082-6467(2005)14[137:THAGRO]2.0.CO;2
Lange CE (2010) Paranosema locustae (microsporidia) in grasshoppers (Orthoptera: Acridoidea) of Argentina: field host range expanded. Biocontrol Sci Tech 20:1047–1054. https://doi.org/10.1080/09583157.2010.505326
doi: 10.1080/09583157.2010.505326
Lange B, Kaufmann AP, Ebert D (2015) Genetic, ecological and geographic covariables explaining host range and specificity of a microsporidian parasite. J Anim Ecol 84:1711–1719. https://doi.org/10.1111/1365-2656.12421
doi: 10.1111/1365-2656.12421
pubmed: 26147623
Lange CE, Mariottini Y, Plischuk S, Cigliano MM (2020) Naturalized, newly-associated microsporidium continues causing epizootics and expanding its host range. Protistology 14:32–37
doi: 10.21685/1680-0826-2020-14-1-4
Larsen BB, Miller EC, Rhodes MK, Wiens JJ (2017) Inordinate fondness multiplied and redistributed: the number of species on earth and the new pie of life. Q Rev Biol 92:229–265. https://doi.org/10.1086/693564
doi: 10.1086/693564
Lass S, Ebert D (2006) Apparent seasonality of parasite dynamics: analysis of cyclic prevalence patterns. Proc R Soc B Biol Sci 273:199–206. https://doi.org/10.1098/rspb.2005.3310
doi: 10.1098/rspb.2005.3310
Legros M, Koella JC (2010) Experimental evolution of specialization by a microsporidian parasite. BMC Evol Biol 10:1–7. https://doi.org/10.1186/1471-2148-10-159
doi: 10.1186/1471-2148-10-159
Leitch GJ, Ceballos C (2008) Effects of host temperature and gastric and duodenal environments on microsporidia spore germination and infectivity of intestinal epithelial cells. Parasitol Res 104:35–42. https://doi.org/10.1007/s00436-008-1156-4
doi: 10.1007/s00436-008-1156-4
pubmed: 18751726
pmcid: 2737319
Li W, Feng Y, Santin M (2019) Host specificity of Enterocytozoon bieneusi and public health implications. Trends Parasitol 35:436–451. https://doi.org/10.1016/j.pt.2019.04.004
doi: 10.1016/j.pt.2019.04.004
pubmed: 31076351
Lievens EJP, Perreau J, Agnew P et al (2018) Decomposing parasite fitness reveals the basis of specialization in a two-host, two-parasite system. Evol Lett 2:390–405. https://doi.org/10.1002/evl3.65
doi: 10.1002/evl3.65
pubmed: 30283690
pmcid: 6121826
Lievens EJP, Rode NO, Landes J et al (2019) Long-term prevalence data reveals spillover dynamics in a multi-host (Artemia), multi-parasite (microsporidia) community. Int J Parasitol 49:471–480. https://doi.org/10.1016/j.ijpara.2019.01.002
doi: 10.1016/j.ijpara.2019.01.002
pubmed: 30904622
Lievens EJP, Michalakis Y, Lenormand T (2020) Trait-specific trade-offs prevent niche expansion in two parasites. J Evol Biol 33:1704–1714. https://doi.org/10.1111/jeb.13708
doi: 10.1111/jeb.13708
pubmed: 33040426
Luallen RJ, Reinke AW, Tong L et al (2016) Discovery of a natural microsporidian pathogen with a broad tissue tropism in Caenorhabditis elegans. PLoS Pathog 12:e1005724. https://doi.org/10.1371/journal.ppat.1005724
doi: 10.1371/journal.ppat.1005724
pubmed: 27362540
pmcid: 4928854
Malone LA (1984) Factors controlling in vitro hatching of Vairimorpha plodiae (Microspora) spores and their infectivity to Plodia interpunctella, Heliothis virescens, and Pieris brassicae. J Invertebr Pathol 44:192–197. https://doi.org/10.1016/0022-2011(84)90012-0
doi: 10.1016/0022-2011(84)90012-0
Martín-Hernández R, Bartolomé C, Chejanovsky N et al (2018) Nosema ceranae in Apis mellifera: a 12 years postdetection perspective. Environ Microbiol 20:1302–1329. https://doi.org/10.1111/1462-2920.14103
doi: 10.1111/1462-2920.14103
pubmed: 29575513
Milbrath MO, van Tran T, Huang W-F et al (2015) Comparative virulence and competition between Nosema apis and Nosema ceranae in honey bees (Apis mellifera). J Invertebr Pathol 125:9–15. https://doi.org/10.1016/j.jip.2014.12.006
doi: 10.1016/j.jip.2014.12.006
pubmed: 25527406
Murareanu BM, Sukhdeo R, Qu R et al (2021) Generation of a microsporidia species attribute database and analysis of the extensive ecological and phenotypic diversity of microsporidia. mBio 12:e01490–e01421
doi: 10.1128/mBio.01490-21
Narr CF, Ebert D, Bastille-Rousseau G, Frost PC (2019) Nutrient availability affects the prevalence of a microsporidian parasite. J Anim Ecol 88:579–590. https://doi.org/10.1111/1365-2656.12945
doi: 10.1111/1365-2656.12945
pubmed: 30636044
Natsopoulou ME, McMahon DP, Doublet V et al (2015) Interspecific competition in honeybee intracellular gut parasites is asymmetric and favours the spread of an emerging infectious disease. Proc R Soc B Biol Sci 282:20141896. https://doi.org/10.1098/rspb.2014.1896
doi: 10.1098/rspb.2014.1896
Oi DH, Valles SM, Briano JA (2010) Laboratory host specificity testing of the fire ant microsporidian pathogen Vairimorpha invictae (microsporidia: Burenellidae). Biol Control 53:331–336. https://doi.org/10.1016/j.biocontrol.2009.12.013
doi: 10.1016/j.biocontrol.2009.12.013
Olson RE, Pierce JR, Jacobson KC, Burreson EM (2004) Temporal changes in the prevalence of parasites in two Oregon estuary-dwelling fishes. J Parasitol 90:564–571
doi: 10.1645/GE-3057
Orlansky S, Ben-Ami F (2019) Genetic resistance and specificity in sister taxa of daphnia: insights from the range of host susceptibilities. Parasit Vectors 12:545. https://doi.org/10.1186/s13071-019-3795-y
doi: 10.1186/s13071-019-3795-y
pubmed: 31747976
pmcid: 6864995
Pilarska DK, Solter LF, Kereselidze M et al (2006) Microsporidian infections in Lymantria dispar larvae: interactions and effects of multiple species infections on pathogen horizontal transmission. J Invertebr Pathol 93:105–113. https://doi.org/10.1016/j.jip.2006.05.003
doi: 10.1016/j.jip.2006.05.003
pubmed: 16814805
Porrini MP, Sarlo EG, Medici SK et al (2011) Nosema ceranae development in Apis mellifera: influence of diet and infective inoculum. J Apic Res 50:35–41. https://doi.org/10.3896/IBRA.1.50.1.04
doi: 10.3896/IBRA.1.50.1.04
Porter SD, Valles SM, Davis TS et al (2007) Host specificity of the microsporidian pathogen vairimorpha invictae at five field sites with infected solenopsis invicta fire ant colonies in northern Argentina. Flen 90:447–452. https://doi.org/10.1653/0015-4040(2007)90[447:HSOTMP]2.0.CO;2
doi: 10.1653/0015-4040(2007)90[447:HSOTMP]2.0.CO;2
Preston CE, Agnello AM, Hajek AE (2020) Nosema maddoxi (microsporidia: Nosematidae) in brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), populations in the United States. Biol Control 144:104213. https://doi.org/10.1016/j.biocontrol.2020.104213
doi: 10.1016/j.biocontrol.2020.104213
Pulkkinen K (2007) Microparasite transmission to Daphnia magna decreases in the presence of conspecifics. Oecologia 154:45–53. https://doi.org/10.1007/s00442-007-0805-0
doi: 10.1007/s00442-007-0805-0
pubmed: 17657511
Quiles A, Bacela-Spychalska K, Teixeira M et al (2019) Microsporidian infections in the species complex Gammarus roeselii (Amphipoda) over its geographical range: evidence for both host–parasite co-diversification and recent host shifts. Parasit Vectors 12:327. https://doi.org/10.1186/s13071-019-3571-z
doi: 10.1186/s13071-019-3571-z
pubmed: 31253176
pmcid: 6599290
Quiles A, Wattier RA, Bacela-Spychalska K et al (2020) Dictyocoela microsporidia diversity and co-diversification with their host, a gammarid species complex (Crustacea, Amphipoda) with an old history of divergence and high endemic diversity. BMC Evol Biol 20:149. https://doi.org/10.1186/s12862-020-01719-z
doi: 10.1186/s12862-020-01719-z
pubmed: 33176694
pmcid: 7659068
Quiles A, Rigaud T, Wattier RA et al (2021) Wide geographic distribution of overlooked parasites: rare microsporidia in Gammarus balcanicus, a species complex with a high rate of endemism. Int J Parasitol: Parasites and Wildlife 14:121–129. https://doi.org/10.1016/j.ijppaw.2021.01.004
doi: 10.1016/j.ijppaw.2021.01.004
pmcid: 7876520
Raquel M-H, Aránzazu M, Lourdes P et al (2007) Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol 73:6331–6338. https://doi.org/10.1128/AEM.00270-07
doi: 10.1128/AEM.00270-07
Raquel M-H, Aránzazu M, Pilar G-P et al (2009) Effect of temperature on the biotic potential of honeybee microsporidia. Appl Environ Microbiol 75:2554–2557. https://doi.org/10.1128/AEM.02908-08
doi: 10.1128/AEM.02908-08
Reddy KC, Dror T, Underwood RS et al (2019) Antagonistic paralogs control a switch between growth and pathogen resistance in C. elegans. PLoS Pathog 15:e1007528. https://doi.org/10.1371/journal.ppat.1007528
doi: 10.1371/journal.ppat.1007528
pubmed: 30640956
pmcid: 6347328
Reinke AW, Troemel ER (2015) The development of genetic modification techniques in intracellular parasites and potential applications to microsporidia. PLoS Pathog 11:e1005283. https://doi.org/10.1371/journal.ppat.1005283
doi: 10.1371/journal.ppat.1005283
pubmed: 26720003
pmcid: 4699923
Reinke AW, Balla KM, Bennett EJ, Troemel ER (2017) Identification of microsporidia host-exposed proteins reveals a repertoire of rapidly evolving proteins. Nat Commun 8:14023. https://doi.org/10.1038/ncomms14023
doi: 10.1038/ncomms14023
pubmed: 28067236
pmcid: 5423893
Rode NO, Lievens EJP, Segard A et al (2013) Cryptic microsporidian parasites differentially affect invasive and native Artemia spp. Int J Parasitol 43:795–803. https://doi.org/10.1016/j.ijpara.2013.04.009
doi: 10.1016/j.ijpara.2013.04.009
pubmed: 23851079
Routtu J, Ebert D (2015) Genetic architecture of resistance in daphnia hosts against two species of host-specific parasites. Heredity (Edinb) 114:241–248. https://doi.org/10.1038/hdy.2014.97
doi: 10.1038/hdy.2014.97
Sanchez JG, Speare DJ, Markham RJF (2000) Normal and aberrant tissue distribution of Loma salmonae (Microspora) within rainbow trout, Oncorhynchus mykiss (Walbaum), following experimental infection at water temperatures within and outside of the xenoma-expression temperature boundaries. J Fish Dis 23:235–242. https://doi.org/10.1046/j.1365-2761.2000.00222.x
doi: 10.1046/j.1365-2761.2000.00222.x
Sanders JL, Watral V, Stidworthy MF, Kent ML (2016) Expansion of the known host range of the microsporidium, Pseudoloma neurophilia. Zebrafish 13(Suppl 1):S102–S106. https://doi.org/10.1089/zeb.2015.1214
doi: 10.1089/zeb.2015.1214
pubmed: 27182659
Shaw RW, Kent ML, Brown AMV et al (2000) Experimental and natural host specificity of Loma salmonae (microsporidia). Dis Aquat Org 40:131–136. https://doi.org/10.3354/dao040131
doi: 10.3354/dao040131
Solter LF (2006) Transmission as a predictor of ecological host specificity with a focus on vertical transmission of microsporidia. J Invertebr Pathol 92:132–140. https://doi.org/10.1016/j.jip.2006.03.008
doi: 10.1016/j.jip.2006.03.008
pubmed: 16777140
Solter LF, Maddox JV (1998) Physiological host specificity of microsporidia as an indicator of ecological host specificity. J Invertebr Pathol 71:207–216. https://doi.org/10.1006/jipa.1997.4740
doi: 10.1006/jipa.1997.4740
pubmed: 9538025
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. J Invertebr Pathol 69:135–150. https://doi.org/10.1006/jipa.1996.4650
doi: 10.1006/jipa.1996.4650
pubmed: 9056464
Solter LF, Pilarska DK, Vossbrinck CF (2000) Host specificity of microsporidia pathogenic to Forest Lepidoptera. Biol Control 19:48–56. https://doi.org/10.1006/bcon.2000.0845
doi: 10.1006/bcon.2000.0845
Solter LF, Maddox JV, Vossbrinck CR (2005) Physiological host specificity: a model using the European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae) and microsporidia of row crop and other stalk-boring hosts. J Invertebr Pathol 90:127–130. https://doi.org/10.1016/j.jip.2005.08.001
doi: 10.1016/j.jip.2005.08.001
pubmed: 16214162
Solter LF, Pilarska DK, McManus ML et al (2010) Host specificity of microsporidia pathogenic to the gypsy moth, Lymantria dispar (L.): field studies in Slovakia. J Invertebr Pathol 105:1–10. https://doi.org/10.1016/j.jip.2010.04.009
doi: 10.1016/j.jip.2010.04.009
pubmed: 20435042
Steele T, Singer RD, Bjørnson S (2020) Effects of temperature on larval development, alkaloid production and microsporidiosis in the two-spotted lady beetle, Adalia bipunctata L. (Coleoptera: Coccinellidae). J Invertebr Pathol 172(107353). https://doi.org/10.1016/j.jip.2020.107353
Steinhaus EA, Hughes KM (1949) Two newly described species of microsporidia from the potato Tuberworm, Gnorimoschema operculella (Zeller) (Lepidoptera, Gelechiidae). J Parasitol 35:67–75. https://doi.org/10.2307/3273388
doi: 10.2307/3273388
pubmed: 18111992
Stentiford GD, Ramilo A, Abollo E et al (2017) Hyperspora aquatica n.gn., n.sp. (microsporidia), hyperparasitic in Marteilia cochillia (Paramyxida), is closely related to crustacean-infecting microspordian taxa. Parasitology 144:186–199. https://doi.org/10.1017/S0031182016001633
doi: 10.1017/S0031182016001633
pubmed: 27748227
Stirnadel HA, Ebert D (1997) Prevalence, host specificity and impact on host fecundity of microparasites and Epibionts in three sympatric daphnia species. J Anim Ecol 66:212–222. https://doi.org/10.2307/6023
doi: 10.2307/6023
Takahashi S, Ogawa K (1997) Efficacy of elevated water temperature treatment of ayu infected with the microsporidian Glugea plecoglossi. Fish Pathol (Japan) 32:193–198
doi: 10.3147/jsfp.32.193
Tamim El Jarkass H, Mok C, Schertzberg MR, Fraser AG, Troemel ER, Reinke AW (2022) An intestinally secreted host factor limits bacterial colonization but promotes microsporidia invasion of C. elegans. eLife 11:e72458 https://doi.org/10.7554/eLife.72458
doi: 10.7554/eLife.72458
pubmed: 34994689
pmcid: 8806185
Tang KFJ, Han JE, Aranguren LF et al (2016) Dense populations of the microsporidian Enterocytozoon hepatopenaei (EHP) in feces of Penaeus vannamei exhibiting white feces syndrome and pathways of their transmission to healthy shrimp. J Invertebr Pathol 140:1–7. https://doi.org/10.1016/j.jip.2016.08.004
doi: 10.1016/j.jip.2016.08.004
pubmed: 27530403
Terry RS, Smith JE, Sharpe RG et al (2004) Widespread vertical transmission and associated host sex–ratio distortion within the eukaryotic phylum Microspora. Proc R Soc Lond Ser B Biol Sci 271:1783–1789. https://doi.org/10.1098/rspb.2004.2793
doi: 10.1098/rspb.2004.2793
Tokarev YS, Huang W-F, Solter LF et al (2020) A formal redefinition of the genera Nosema and Vairimorpha (microsporidia: Nosematidae) and reassignment of species based on molecular phylogenetics. J Invertebr Pathol 169:107279. https://doi.org/10.1016/j.jip.2019.107279
doi: 10.1016/j.jip.2019.107279
Traver BE, Williams MR, Fell RD (2012) Comparison of within hive sampling and seasonal activity of Nosema ceranae in honey bee colonies. J Invertebr Pathol 109:187–193. https://doi.org/10.1016/j.jip.2011.11.001
doi: 10.1016/j.jip.2011.11.001
pubmed: 22085836
Undeen A (1976) In vivo germination and host specificity of Nosema algerae in mosquitoes. J Invertebr Pathol. https://doi.org/10.1016/0022-2011(76)90094-X
Undeen AH, Maddox JV (1973) The infection of nonmosquito hosts by injection with spores of the microsporidan Nosema algerae. J Invertebr Pathol 22:258–265. https://doi.org/10.1016/0022-2011(73)90143-2
doi: 10.1016/0022-2011(73)90143-2
pubmed: 4206297
Valles SM, Oi DH, Porter SD (2010) Seasonal variation and the co-occurrence of four pathogens and a group of parasites among monogyne and polygyne fire ant colonies. Biol Control 54:342–348. https://doi.org/10.1016/j.biocontrol.2010.06.006
doi: 10.1016/j.biocontrol.2010.06.006
Vávra J, Lukeš J (2013) Chapter four – microsporidia and ‘the art of living together.’. In: Rollinson D (ed) Advances in parasitology. Academic Press, New York, pp 253–319
Vijendravarma RK, Godfray HCJ, Kraaijeveld AR (2008) Infection of Drosophila melanogaster by Tubulinosema kingi: stage-specific susceptibility and within-host proliferation. J Invertebr Pathol 99(2):239–241
doi: 10.1016/j.jip.2008.02.014
Wadi L, Reinke AW (2020) Evolution of microsporidia: an extremely successful group of eukaryotic intracellular parasites. PLoS Pathog 16:e1008276. https://doi.org/10.1371/journal.ppat.1008276
doi: 10.1371/journal.ppat.1008276
pubmed: 32053705
pmcid: 7017984
Wattier RA, Haine ER, Beguet J et al (2007) No genetic bottleneck or associated microparasite loss in invasive populations of a freshwater amphipod. Oikos 116:1941–1953. https://doi.org/10.1111/j.0030-1299.2007.15921.x
doi: 10.1111/j.0030-1299.2007.15921.x
Weiser J, Coluzzi M (1972) The microsporidian Plistophora culicis Weiser, 1946 in different mosquito hosts. Folia parasitologica 19(3):197–202
pubmed: 4151783
Willis AR, Zhao W, Sukhdeo R et al (2021) A parental transcriptional response to microsporidia infection induces inherited immunity in offspring. Science. Advances 7:eabf3114. https://doi.org/10.1126/sciadv.abf3114
doi: 10.1126/sciadv.abf3114
Yakovleva Y, Nassonova E, Lebedeva N et al (2020) The first case of microsporidiosis in paramecium. Parasitology 147:957–971. https://doi.org/10.1017/S0031182020000633
doi: 10.1017/S0031182020000633
pubmed: 32338239
Zhang G, Sachse M, Prevost M-C et al (2016) A large collection of novel nematode-infecting microsporidia and their diverse interactions with Caenorhabditis elegans and other related nematodes. PLoS Pathog 12:e1006093. https://doi.org/10.1371/journal.ppat.1006093
doi: 10.1371/journal.ppat.1006093
pubmed: 27942022
pmcid: 5179134