High quality genome assembly of the anhydrobiotic midge provides insights on a single chromosome-based emergence of extreme desiccation tolerance

Abstract

Non-biting midges (Chironomidae) are known to inhabit a wide range of environments, and certain species can tolerate extreme conditions, where the rest of insects cannot survive. In particular, the sleeping chironomid Polypedilum vanderplanki is known for the remarkable ability of its larvae to withstand almost complete desiccation by entering a state called anhydrobiosis. Chromosome numbers in chironomids are higher than in other dipterans and this extra genomic resource might facilitate rapid adaptation to novel environments. We used improved sequencing strategies to assemble a chromosome-level genome sequence for P. vanderplanki for deep comparative analysis of genomic location of genes associated with desiccation tolerance. Using whole genome-based cross-species and intra-species analysis, we provide evidence for the unique functional specialization of Chromosome 4 through extensive acquisition of novel genes. In contrast to other insect genomes, in the sleeping chironomid a uniquely high degree of subfunctionalization in paralogous anhydrobiosis genes occurs in this chromosome, as well as pseudogenization in a highly duplicated gene family. Our findings suggest that the Chromosome 4 in Polypedilum is a site of high genetic turnover, allowing it to act as a ‘sandbox’ for evolutionary experiments, thus facilitating the rapid adaptation of midges to harsh environments.

A Sodium-dependent Trehalose Transporter Contributes to Anhydrobiosis in Insect Cell Line, Pv11

“…The PPP is activated during rehydration of dried P. vanderplanki larvae, leading to synthesis of NADPH, which acts to drive the antioxidant system that alleviates the toxic effects of reactive oxygen species generated during rehydration (64). In Pv11 cells, Treh and Hex were highly expressed during trehalose pretreatment and rehydration (Supplement-Dataset S3) (13). In P. vanderplanki larvae, Treh expression is elevated just before desiccation, but it is not enzymically active.…”

“…The genome, gene predictions, annotations (accession number GCA_018290095.1) and RNA-Seq data (accession number GSE158443) from our previous study were downloaded from NCBI (13). Gene expression was quantified using RSEM v1.3.1 (--bowtie2) (66) and the following downstream analysis was performed using the Trinity package v2.15.1 (abundance_estimates_to_matrix.pl, run_DE_analysis.pl) (67).…”

Deciphering the Biological Enigma—Genomic Evolution Underlying Anhydrobiosis in the Phylum Tardigrada and the Chironomid Polypedilum vanderplanki

“…Furthermore, a higher nucleotide diversity, the loss of synteny blocks with other chironomids, and the accumulation of novel gene families was also observed on chromosome 4, highlighting the importance of this chromosome in the evolution of anhydrobiosis in Pol. vanderplanki [ 162 ]. Additionally, a recent preprint described the genome of the anhydrobiotic Pol.…”

“…vanderplanki genome shows synteny with the chromosomes of other mosquitoes, this was not the case for the genes on chromosome 4, suggesting extensive genetic turnover and recombination specific to this chromosome. Indeed, gene clustering analysis and annotation showed that numerous novel genes have accumulated on chromosome 4, causing the loss of synteny [ 162 ].…”

“…Other methods that can be used are long-read sequencing and Hi-C; recent applications have produced pseudo-chromosomal genome assemblies in both chironomids ( Pol. vanderplanki [ 162 ]) and tardigrades ( H. exemplaris [ 178 ]). The application of these methods will likely improve taxonomic coverage, enabling a more thorough analysis of genomic evolution within Tardigrada.…”