Five-year Cohort Study of Nosema Spp. in Germany: Does Climate Shape Virulence and Assertiveness of Nosema Ceranae?

Overview

Journal Appl Environ Microbiol

Specialties Environmental Health
Microbiology

Date 2010 Mar 16

PMID 20228103

Citations 75

Authors

Sebastian Gisder

Kati Hedtke

Nadine Mockel

Marie-Charlotte Frielitz

Andreas Linde

Elke Genersch

Affiliations

Soon will be listed here.

Abstract

Nosema ceranae and Nosema apis are two fungal pathogens belonging to the phylum Microsporidia and infecting the European honeybee, Apis mellifera. Recent studies have suggested that N. ceranae is more virulent than N. apis both at the individual insect level and at the colony level. Severe colony losses could be attributed to N. ceranae infections, and an unusual form of nosemosis is caused by this pathogen. In the present study, data from a 5-year cohort study of the prevalence of Nosema spp. in Germany, involving about 220 honeybee colonies and a total of 1,997 samples collected from these colonies each spring and autumn and analyzed via species-specific PCR-restriction fragment length polymorphism (RFLP), are described. Statistical analysis of the data revealed no relation between colony mortality and detectable levels of infection with N. ceranae or N. apis. In addition, N. apis is still more prevalent than N. ceranae in the cohort of the German bee population that was analyzed. A possible explanation for these findings could be the marked decrease in spore germination that was observed after even a short exposure to low temperatures (+4 degrees C) for N. ceranae only. Reduced or inhibited N. ceranae spore germination at low temperatures should hamper the infectivity and spread of this pathogen in climatic regions characterized by a rather cold winter season.

Citing Articles

Do diet and Fumagillin treatment impact Vairimorpha (Nosema) spp. (Microspora: Nosematidae) infections in honey bees (Hymenoptera: Apidae) and improve survival and growth of colonies overwintered in cold storage?.

DeGrandi-Hoffman G, Corby-Harris V, Graham H, Chambers M, Watkins deJong E, Snyder L J Econ Entomol. 2024; 117(6):2203-2218.

PMID: 39340838 PMC: 11682945. DOI: 10.1093/jee/toae187.

Current status of Nosema spp. infection cases in apis mellifera in eurasian countries and Ptp3 gene haplotypes in the Republic of Tatarstan, Russia.

Shamaev N, Shuralev E, Mukminov M Vet Res Commun. 2024; 48(4):2691-2698.

PMID: 38644458 DOI: 10.1007/s11259-024-10383-3.

Development of Enzyme-Linked Immunosorbent and Immunochromatography Assays for Diagnosing Infection in Honey Bees.

Lee J Insects. 2024; 15(1).

PMID: 38249065 PMC: 10816434. DOI: 10.3390/insects15010059.

A tale of two parasites: Responses of honey bees infected with Nosema ceranae and Lotmaria passim.

MacInnis C, Luong L, Pernal S Sci Rep. 2023; 13(1):22515.

PMID: 38110440 PMC: 10728187. DOI: 10.1038/s41598-023-49189-9.

Geographic population structure of the honeybee microsporidian parasite Vairimorpha (Nosema) ceranae in the South West Indian Ocean.

Blot N, Clemencet J, Jourda C, Lefeuvre P, Warrit N, Esnault O Sci Rep. 2023; 13(1):12122.

PMID: 37495608 PMC: 10372035. DOI: 10.1038/s41598-023-38905-0.

References

Klee J, Besana A, Genersch E, Gisder S, Nanetti A, Tam D . Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol. 2007; 96(1):1-10. DOI: 10.1016/j.jip.2007.02.014. View

Fries I . Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol. 2009; 103 Suppl 1:S73-9. DOI: 10.1016/j.jip.2009.06.017. View

Weber R, Bryan R, Schwartz D, Owen R . Human microsporidial infections. Clin Microbiol Rev. 1994; 7(4):426-61. PMC: 358336. DOI: 10.1128/CMR.7.4.426. View

Gatehouse H, Malone L . The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size. J Invertebr Pathol. 1998; 71(2):97-105. DOI: 10.1006/jipa.1997.4737. View

Higes M, Martin R, Meana A . Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol. 2006; 92(2):93-5. DOI: 10.1016/j.jip.2006.02.005. View

Higes M, Garcia-Palencia P, Martin-Hernandez R, Meana A . Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J Invertebr Pathol. 2007; 94(3):211-7. DOI: 10.1016/j.jip.2006.11.001. View

Martin-Hernandez R, Meana A, Prieto L, Salvador A, Garrido-Bailon E, Higes M . Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol. 2007; 73(20):6331-8. PMC: 2075036. DOI: 10.1128/AEM.00270-07. View

Cox-Foster D, Conlan S, Holmes E, Palacios G, Evans J, Moran N . A metagenomic survey of microbes in honey bee colony collapse disorder. Science. 2007; 318(5848):283-7. DOI: 10.1126/science.1146498. View

Chen Y, Evans J, Smith I, Pettis J . Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. J Invertebr Pathol. 2007; 97(2):186-8. DOI: 10.1016/j.jip.2007.07.010. View

10.

Williams G, Shafer A, Rogers R, Shutler D, Stewart D . First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and central USA. J Invertebr Pathol. 2007; 97(2):189-92. DOI: 10.1016/j.jip.2007.08.005. View

11.

Higes M, Martin-Hernandez R, Botias C, Bailon E, Gonzalez-Porto A, Barrios L . How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol. 2008; 10(10):2659-69. DOI: 10.1111/j.1462-2920.2008.01687.x. View

12.

Aizen M, Garibaldi L, Cunningham S, Klein A . Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr Biol. 2008; 18(20):1572-5. DOI: 10.1016/j.cub.2008.08.066. View

13.

Lee S, Corradi N, Byrnes 3rd E, Torres-Martinez S, Dietrich F, Keeling P . Microsporidia evolved from ancestral sexual fungi. Curr Biol. 2008; 18(21):1675-9. PMC: 2654606. DOI: 10.1016/j.cub.2008.09.030. View

14.

van Engelsdorp D, Hayes Jr J, Underwood R, Pettis J . A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008. PLoS One. 2008; 3(12):e4071. PMC: 2606032. DOI: 10.1371/journal.pone.0004071. View

15.

Mayack C, Naug D . Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J Invertebr Pathol. 2009; 100(3):185-8. DOI: 10.1016/j.jip.2008.12.001. View

16.

Martin-Hernandez R, Meana A, Garcia-Palencia P, Marin P, Botias C, Garrido-Bailon E . Effect of temperature on the biotic potential of honeybee microsporidia. Appl Environ Microbiol. 2009; 75(8):2554-7. PMC: 2675226. DOI: 10.1128/AEM.02908-08. View

17.

Chen Y, Evans J, Murphy C, Gutell R, Zuker M, Gundensen-Rindal D . Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera. J Eukaryot Microbiol. 2009; 56(2):142-7. PMC: 2779023. DOI: 10.1111/j.1550-7408.2008.00374.x. View

18.

Aizen M, Harder L . The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol. 2009; 19(11):915-8. DOI: 10.1016/j.cub.2009.03.071. View

19.

Invernizzi C, Abud C, Tomasco I, Harriet J, Ramallo G, Campa J . Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay. J Invertebr Pathol. 2009; 101(2):150-3. DOI: 10.1016/j.jip.2009.03.006. View

20.

vanEngelsdorp D, Evans J, Donovall L, Mullin C, Frazier M, Frazier J . "Entombed Pollen": A new condition in honey bee colonies associated with increased risk of colony mortality. J Invertebr Pathol. 2009; 101(2):147-9. DOI: 10.1016/j.jip.2009.03.008. View