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Antioxidant system of desiccation-tolerant insect Polypedilum vanderplanki Alexander A. Nesmelov1*, Elena I. Shagimardanova1, Maria D. Logacheva2, Richard Cornette3, Takahiro Kikawada3, Oleg A. Gusev
1 2

1,3,4,5

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Institute of Fundamental Biology and Medicine, Kazan Federal Uni versity, Kazan 420008, Russia, Department of Bioengineering and Bioinformatics, Lomonosov Moscow State University, Moscow 119991, Russia, 3National Institute of Agrobiological Sciences (NIAS), Tsukuba 305-8602, Japan, 4ISS Science Project Office, Institute of Space and Astronautical Science, Japan Aerospace Exploration Agency ( JAXA), Tsukuba 305- 8505, Japan, 5PMI Riken, Yokohama Campus, Yokohama 230-0045, Japan, *nesmelov@gmail.com

Polypedilum vanderplanki is a small African chironomid able to revive after almost full desiccation at a larva stage. Despite of its relatively small size (around 7 mm), larva of this insect is the most complex desiccation-tolerant organism known at the date. Such an extreme adaptation implies an ability to cope with a severe damage of cell interior including protein aggregation and denaturation, perturbation of membranes and DNA damage. Comparative analysis of genome and transcriptome of P. vanderplanki and congeneric desiccation-sensitive chironomid P. nubifer help us to reveal genes and proteins that ensure desiccation tolerance. Particularly, P. vanderplanki genome contain an extended set of genes encoding proteins involved in antioxidant defense. An empowering of P. vanderplanki antioxidant system is closely related to an elevation of oxidative stress during water loss and in a desiccated state. Such an elevation is mediated by disruptions of the mitochondrial electron transport chain, reduction of the hydrating shell of macromolecules, an increase of ionic strength and pH change [1]. The number of antioxidant system genes in P. vanderplanki (54) is considerably higher than in P. nubifer and even higher than in the genome of the honey bee (38) whereas the latter is characterized far more higher metabolic rates [2]. The increase of a number of antioxidant genes in P. vanderplanki is not only a result of gene duplication and diversification. Molecular evolution of P. vanderplanki resulted also in an acquisition of new genes. Such new genes include two P. vanderplanki specific superoxide dismutases (SOD) that are not related to SOD's of P. nubifer based on another location and low sequence similarity. These P. vanderplanki specific enzymes become highly upregulated during anhydrobiosis cycle. P. vanderplanki genome contain the sole gene of manganese-containing mitochondrial SOD which belongs to a classic insect enzymes. Its


expression is not increased in desiccation despite of the fact that mitochondria are obviously the main source of reactive oxygen species (ROS). Unique SOD genes of P. vanderplanki that are upregulated in anhydrobiosis encode copper/zinc-containing dismutases that are usually considered as cytosolic/extracellular enzymes. Recently reported controllable process of localization of CuZn SOD into intramembrane space of mitochondria in human macrophages suggests that typical specialization of two types of SOD in the case of P. vanderplanki should be also revised [3]. An absence of gene encoding glutathione reductase suggests that P. vanderplanki antioxidant system glutathione does not serve as a main mediator of ROS scavenge and is at least partially substituted by thioredoxins. Such a substitution was already reported for Drosophila melanogaster. However, P. vanderplanki larva express 12 splice variants of glutathione peroxidase (GPx). Similarly to D. melanogaster they are expected to be thioredoxin-specific [4]. Among different variants of P. vanderplanki GPx eight are typical enzymes with three catalytic amino acid residues and highly conserved residues in proximal regions. However, in four variants catalytic glutamine is replaced by glycine and proximal downstream region is disturbed. In addition to an increase in the gene number (54 versus 27 in P. nubifer) some of antioxidant genes are upregulated in P. vanderplanki intrinsically or become upregulated during desiccation cycle. Transcriptomic data provides us interesting examples of differential expression of genes that are specific for P. vanderplanki and genes that are analogous to P. nubifer. During desiccation cycle in P. vanderplanki larva genes encoding catalase and glutaredoxin become upregulated in 2.5 and 6 times, accordingly. Expression of analogous genes of P. nubifer during desiccation cycle does not change. Taken together with well-known ability of P. vanderplanki to start a huge accumulation of trehalose at the onset of desiccation, these data demonstrate a presence of specific desiccation-sensitive system of differential gene regulation in P. vanderplanki.

This work was done in the frame of the Program of competitive growth of Kazan Federal University among world class academic centres and universities with support of grant by


Russian Scientific Foundation RNF-14-8-VP.

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