Using molecular techniques, we documented the presence of Nosema ceranae in honeybees (Apis mellífera) from Argentina. Samples were collected from A. mellifera colonies in 38 districts of Buenos Aires province, Argentina. Molecular characterization was achieved with a multiplex PCR-based method, which allows parallel diagnosis of N. ceranae and N. osema apis. N. ceranae was identified in all the samples analyzed. Moreover, coinfections with N. apis were detected in Balcarce and Maipú districts. We identified three rRNA sequence variants of N. ceranae, which may represent diverse sources of bee importation. The results suggest that N. ceranae is widely distributed in Argentina and that the genetic variation observed between the different isolates could be related with the difference in the symptomatology found previously by our work group. Our results highlight the need to re-assess the health protocols currently in force so that they recognize N. ceranae as the main causal agent of Nosemosis in this country.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Anisimova M, Gascuel O (2006) Approximate likelihood ratio test for branches: a fast, accurate and powerful alternative. Syst Biol 55:539–552
Benson D, Karsch-Mzrachi I, Lipman DJ, Ostell J, Wheeler DL (2005) GenBank. Nucleic Acids Res 33:D34–D38
Burgher-MacLellan KL, Williams GR, Shutler D, MacKenzie K, Rogers REL (2010) Optimization of duplex real-time PCR with melting-curve analysis for detecting the microsporidian parasites Nosema apis and Nosema ceranae in Apis mellifera. Can Entomol 142:271–283
Cole R (1970) The application of the “triangulation” method for the purification of Nosema spores from insect tissues. J Invertebr Pathol 15:193–195
De Graaf D, Masschelein G, Vandergeynst F, De Brabander H, Jacobs F (1993) In vitro germination of Nosema apis (Microspora: Nosematidae) spores and its effect on their αα-Trehalose/d-Glucose ratio. J Invertebr Pathol 62:220–225
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J, Guindon S, Lefort V, Lescot M, Claverie J, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:w465–w469
Elias I, Lagergren J (2007) Fast computation of distance estimators. BMC Bioinforma 13:89
Faucon J, Mathieu I, Ribiére A, Drajnudel P, Zeggane S, Aurieres C, Aubert M (2002) Honey bee winter mortality in France in 1999 and 2000. Bee World 83:14–23
Felsenstein J (1989) Phylip—phylogeny inference package (version 3.2). Cladistics 5:164–166
Fries I (2010) Nosema cerane in European honey bees (Apis mellifera). J Invertebr Pathol 103:S73–S79
Fries I, Feng F, Da Silva A, Slemenda S, Pieniazek J (1996) Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur J Protistol 32:356–365
Fries I, Martín R, Meana A, García-Palencia P, Higes M (2006) Natural infections of Nosema ceranae in European honey bees. J Apic Res 45:230–233
Gascuel O (1997) BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14:685–695
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucl Acids Sym Ser 41:95–98
Higes M, Martín R, Meana A (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol 92:93–95
Higes M, García-Palencia P, Martín-Hernández R, Meana A (2007) Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J Invertebr Pathol 94:211–217
Huang W, Jiang J, Chen Y (2005) Complete rRNA sequence of the Nosema ceranae from honeybee (Apis mellifera). Dissertation, National Taiwan University, Taipei
Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinforma 17:754–755
Klee J, Besana A, Genersch E, Gisder S, Nanetti A, Tam D, Chinh T, Puerta F, Ruz J, Kryger P, Message D, Hatjina F, Korpela S, Fries I, Paxton R (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol 96:1–10
Martín-Hernández R, Meana A, Prieto I, Martínez Salvador A, Garrido-Bailón E, Higes M (2007) Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol 73:6331–6338
O’Mahony EM, Tay WT, Paxton RJ (2007) Multiple rRNA variants in a single spore of the microsporidian Nosema bombi. J Eukaryot Microbiol 54:103–109
Page R (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Poirot O, O’Toole E, Notredame C (2003) Tcoffee@igs: a web server for computing, evaluating and combining multiple sequence alignments. Nucleic Acids Res 31:3503–3506
Sarlo EG, Medici SK, Porrini MP, Eguaras MJ (2008) Presencia y distribución de Nosema ceranae en la región Sudeste de la provincia de Buenos Aires. 2do Congreso Argentino de Apicultura
Shafer AB, Williams GR, Shutler D, Rogers RE, Stewart DT (2009) Cophylogeny of Nosema (Microsporidia: Nosematidae) and bees (Hymenoptera: Apidae) suggests both cospeciation and a host switch. J Parasitol 95:198–203
Tay W, O’Mahoney E, Paxton R (2005) Complete rRNA gene sequences reveal that the microsporidian Nosema bombi infects diverse bumblebee (Bombus spp.) hosts and contains multiple polymorphic sites. J Eukaryot Microbiol 52:505–513
Vossbrinck CR, Maddox JV, Friedman S, Debrunner-Vossbrinck BA, Woese CR (1987) Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326:411–414
Weiss IM, Vossbrinck CR (1999) Molecular biology, molecular phylogeny, and molecular diagnostic approaches to the microsporidia. In: Wittner M, Weiss IM (eds) The microsporidia and microsporidiosis. ASM Press, Washington, DC, pp 129–171
Williams GR, Shafer A, Rogers R, Shutler D, Stewart D (2008) First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and Central USA. J Invertebr Pathol 97:189–192
We thank the Comisión de Investigaciones Científicas (CIC) and PICT 890 ANPCyT for financial support. We also want to thank the beekeepers who collected and sent us the samples of honeybees, because without their collaboration this work would not have been possible: Edelmar Abratte, Muselli Carlos, Delpiano Jorge, Baquero Alcides, Meschino Horacio, Paravicini Mauricio, Ormazabal, Fabi, Bartuche, Gonzalez Alfredo, Arévalo, Balbi, Poffer, Defeudis Leonardo, Hoffer, Robenaker, Schafen Ana, Izaguirre, Machín marta, Aguirre, Espié Jorge, Torchelli Mauricio, Quies Roberto, Lliteas Gustavo, Colombani Martín, Grupo Apibal, Frígoli Juan Carlos, Serritela, Tambascia.
About this article
Cite this article
Medici, S.K., Sarlo, E.G., Porrini, M.P. et al. Genetic variation and widespread dispersal of Nosema ceranae in Apis mellifera apiaries from Argentina. Parasitol Res 110, 859–864 (2012). https://doi.org/10.1007/s00436-011-2566-2
- Apis Mellifera
- High Resolution Melting
- Honeybee Coloni
- Buenos Aires Province
- Main Causal Agent