Genome and Evolutionary Analysis of Nosema ceranae: A Microsporidian Parasite of Honey Bees.

Qiang Huang,Wen Feng Li,Jay D. Evans,Jin Shan Xu,Xiao Qun Dang,Zheng Gang Ma,Rui Guo,Zhi Hao Wu,Yan Ping Chen

doi:10.3389/fmicb.2021.645353

Abstract

Microsporidia comprise a phylum of single cell, intracellular parasites and represent the earliest diverging branch in the fungal kingdom. The microsporidian parasite Nosema ceranae primarily infects honey bee gut epithelial cells, leading to impaired memory, suppressed host immune responses and colony collapse under certain circumstances. As the genome of N. ceranae is challenging to assembly due to very high genetic diversity and repetitive region, the genome was re-sequenced using long reads. We present a robust 8.8 Mbp genome assembly of 2,280 protein coding genes, including a high number of genes involved in transporting nutrients and energy, as well as drug resistance when compared with sister species Nosema apis. We also describe the loss of the critical protein Dicer in approximately half of the microsporidian species, giving new insights into the availability of RNA interference pathway in this group. Our results provided new insights into the pathogenesis of N. ceranae and a blueprint for treatment strategies that target this parasite without harming honey bees. The unique infectious apparatus polar filament and transportation pathway members can help to identify treatments to control this parasite.

Highlights

As the earliest branch from the fungal kingdom, microsporidia comprise a large and widespread group of obligate intracellular animal parasites (Keeling and Fast, 2002; Williams, 2009; CapellaGutiérrez et al, 2012)
The species maintained RNAi genes showed a number of transposable elements, which might contribute to the observed larger genome sizes (Ndikumana et al, 2017)
2,280 genes were predicted with an average length of 1,057 nucleotides per gene, all supported by transcriptomic reads (Table 1 and Supplementary File 1)

Summary

Introduction

As the earliest branch from the fungal kingdom, microsporidia comprise a large and widespread group of obligate intracellular animal parasites (Keeling and Fast, 2002; Williams, 2009; CapellaGutiérrez et al, 2012). Microsporidia showed substantial damage to the silkworm and fisheries industries and are a driving factor for honey bee colony losses which seriously threaten the agricultural economy and global food security (Higes et al, 2008; Aizen et al, 2009; Freeman and Sommerville, 2011; Stentiford et al, 2016; Santhoshkumar et al, 2017; Meng et al, 2018) In response to their intracellular parasitic life cycle, microsporidia have undergone massive reductions in gene content, including decayed glycolytic pathways, leading to extremely compact eukaryotic genomes Energy and resources needed for the proliferation of the parasite are acquired directly from the host, causing energetic stress (Mayack and Naug, 2009; Martin-Hernandez et al, 2011)

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