Complete genome of a unicellular parasite (Antonospora locustae) and transcriptional interactions with its host locust

Abstract

Microsporidia are a large group of unicellular parasites that infect insects and mammals. The simpler life cycle of microsporidia in insects provides a model system for understanding their evolution and molecular interactions with their hosts. However, no complete genome is available for insect-parasitic microsporidian species. The complete genome of Antonospora locustae, a microsporidian parasite that obligately infects insects, is reported here. The genome size of A. locustae is 3 170 203 nucleotides, composed of 17 chromosomes onto which a total of 1857 annotated genes have been mapped and detailed. A unique feature of the A. locustae genome is the presence of an ultra-low GC region of approximately 25 kb on 16 of the 17 chromosomes, in which the average GC content is only 20 %. Transcription profiling indicated that the ultra-low GC region of the parasite could be associated with differential regulation of host defences in the fat body to promote the parasite’s survival and propagation. Phylogenetic gene analysis showed that A. locustae, and the microsporidian family in general, is likely at an evolutionarily transitional position between prokaryotes and eukaryotes, and that it evolved independently. Transcriptomic analysis showed that A. locustae can systematically inhibit the locust phenoloxidase PPO, TCA and glyoxylate cycles, and PPAR pathways to escape melanization, and can activate host energy transfer pathways to support its reproduction in the fat body, which is an insect energy-producing organ. Our study provides a platform and model for studies of the molecular mechanisms of microsporidium–host interactions in an energy-producing organ and for understanding the evolution of microsporidia.

Nosema locustae (Protozoa, Microsporidia), a Biological Agent for Locust and Grasshopper Control

“…Genomic and protein sequences from N. locustae and several other single-celled organisms were used to study evolutionary relationships in genetic synteny and collinearity using the MCScanX method. Results showed that within the microsporidia, most genes exhibit good collinearity [45].…”

“…Understanding the molecular biology of N. locustae is fundamental in determining its biology and molecular interactions with the host and improving applications in its use for pest control. A complete genomic sequence of N. locustae has recently been revealed by Chen et al [45], which is a major achievement. Sequencing of its genome yielded 3,170,203 nucleotides, encoding for 1857 predicted genes, of which 1755 are single-exon genes, and 102 are multiple exon genes.…”

“…In addition to genomic sequencing, Chen et al [45] performed an analysis of locust midgut transcripts versus locust fat body transcripts from N. locustae infected locusts. They found that the abundant expression of locust antimicrobial peptides and other defense genes, such as peroxiredoxin and amine oxidase in the midgut, may explain the lower number of microsporidian spores in the midgut of the host.…”

Suppression of yolk formation, oviposition and egg quality of locust (Locusta migratoria manilensis) infected by Paranosema locustae

“…Paranosema ( Nosema ) locustae is an entomopathogenic fungus that only infects locusts. Since the 1980s, the fungus has shown great potential as a biological control in locust control ( 1 , 2 ). Locusts infected by P. locustae can spread the pathogen to other nearby locusts through horizontal transmission.…”

MicroRNA-6498-5p Inhibits Nosema bombycis Proliferation by Downregulating BmPLPP2 in Bombyx mori

“…Microsporidia have an extremely reduced genome ranging from 2.3 to 23 Mb, indicating an extreme dependence of the parasite on the host for biochemical processes [3,4]. There have been significant advances in the parasitological, evolutionary, and genomic research on microsporidia since multiple genome sequences were sequenced [5][6][7][8][9][10][11][12][13]. In addition, transcriptomics analysis of microsporidia infection in hosts has revealed a complicated and interconnected interaction in which microRNA (miRNA) as a key gene expression regulator is involved.…”