Microbial Ecology

, Volume 77, Issue 4, pp 877–889 | Cite as

Genetic and Genome Analyses Reveal Genetically Distinct Populations of the Bee Pathogen Nosema ceranae from Thailand

  • Melissa J. Peters
  • Guntima Suwannapong
  • Adrian Pelin
  • Nicolas CorradiEmail author
Environmental Microbiology


The recent global decline in Western honeybee (Apis mellifera) populations is of great concern for pollination and honey production worldwide. Declining honeybee populations are frequently infected by the microsporidian pathogen Nosema ceranae. This species was originally described in the Asiatic honeybee (Apis cerana), and its identification in global A. mellifera hives could result from a recent host transfer. Recent genome studies have found that global populations of this parasite are polyploid and that humans may have fueled their global expansion. To better understand N. ceranae biology, we investigated its genetic diversity within part of their native range (Thailand) and among different hosts (A. mellifera, A. cerana) using both PCR and genome-based methods. We find that Thai N. ceranae populations share many SNPs with other global populations and appear to be clonal. However, in stark contrast with previous studies, we found that these populations also carry many SNPs not found elsewhere, indicating that these populations have evolved in their current geographic location for some time. Our genome analyses also indicate the potential presence of diploidy within Thai populations of N. ceranae.


Microsporidia Nosema ceranae Honeybees Small ribosomal subunit RNA gene Next-generation sequencing Genome diversity 



We are grateful to Eric Chen, Nathan Liang, and Stephanie Mathieu for the assistance in the laboratory. NC’s work is supported by the Discovery program from the Natural Sciences and Engineering Research Council of Canada (NSERC-Discovery) and an Early Researcher Award from the Ontario Ministry of Research and Innovation (ER13-09-190).

Conflict of Interest

The authors declare that they have no conflicts of interests.

Supplementary material

248_2018_1268_Fig6_ESM.png (1.9 mb)
Fig. S1

Discontinuous sequence alignment of a region of the SSU gene. Includes the novel Nosema sequence detected in Thai honeybee populations (top row), N. ceranae (middle row), and N. apis (bottom row). Asterisks (*) indicate sites without polymorphisms and SNPs are highlighted in white. (PNG 1927 kb)

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High Resolution Image (TIF 184318 kb)
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Fig. S2

SNP allele frequency distributions for the Thailand populations of N. ceranae. Frequencies are based on read counts of bi-allelic SNPs within each genome. (PNG 245 kb)

248_2018_1268_MOESM2_ESM.tif (259.7 mb)
High Resolution Image (TIF 265962 kb)
248_2018_1268_Fig8_ESM.png (1.1 mb)
Fig. S3

SNP density of scaffolds containing evidence for loss of heterozygosity (LOH) in the genome of N. ceranae populations from Thailand. SNPs were plotted in a 1 kb window and the regions exhibiting LOH are indicated. LOH present in scaffolds JPQZ01000016.1 and JPQZ01000026.1 are specific to Thailand populations. (PNG 1153 kb)

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High Resolution Image (TIF 434371 kb)
248_2018_1268_Fig9_ESM.png (73 kb)
Fig. S4

Distribution of average Watterson’s θ values for coding regions within N. ceranae populations from Thailand. The top 1% of genes are indicated in the boxed region and the average exome-wide θ is indicated by the dotted line. (PNG 72 kb)

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High Resolution Image (TIF 213286 kb)
248_2018_1268_Fig10_ESM.png (1.5 mb)
Fig. S5

Linkage disequilibrium (r2) plotted along the three largest scaffolds of Thailand populations of N. ceranae. (PNG 1574 kb)

248_2018_1268_MOESM5_ESM.tif (380 mb)
High Resolution Image (TIF 389122 kb)
248_2018_1268_Fig11_ESM.png (447 kb)
Fig. S6

Linkage disequilibrium decay plotted as mean r2 as a function of distance between SNPs on the three largest scaffolds of N. ceranae. Gray area surrounding the curve indicates standard deviation from the mean at each distance. (PNG 447 kb)

248_2018_1268_MOESM6_ESM.tif (190.8 mb)
High Resolution Image (TIF 195391 kb)
248_2018_1268_MOESM7_ESM.docx (13 kb)
Table S1 Sample and sequencing coverage information for populations of N. ceranae sent for Illumina sequencing. (DOCX 13 kb)
248_2018_1268_MOESM8_ESM.docx (17 kb)
Table S2 Predicted functions for genes within regions exhibiting loss of heterozygosity (LOH). (DOCX 17 kb)
248_2018_1268_MOESM9_ESM.docx (21 kb)
Table S3 The top 50 coding regions with the highest Watterson’s θ values for each population of N. ceranae from Thailand and their predicted gene functions. (DOCX 20 kb)


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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Melissa J. Peters
    • 1
  • Guntima Suwannapong
    • 2
  • Adrian Pelin
    • 3
    • 4
  • Nicolas Corradi
    • 1
    Email author
  1. 1.Department of BiologyUniversity of OttawaOttawaCanada
  2. 2.Department of BiologyBurapha UniversityChon BuriThailand
  3. 3.Department of BiochemistryUniversity of OttawaOttawaCanada
  4. 4.Center for Cancer TherapeuticsOttawa Hospital Research InstituteOttawaCanada

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