Gene expression changes governing extreme dehydration tolerance in an Antarctic insect

Abstract

Among terrestrial organisms, arthropods are especially susceptible to dehydration, given their small body size and high surface area to volume ratio. This challenge is particularly acute for polar arthropods that face near-constant desiccating conditions, as water is frozen and thus unavailable for much of the year. The molecular mechanisms that govern extreme dehydration tolerance in insects remain largely undefined. In this study, we used RNA sequencing to quantify transcriptional mechanisms of extreme dehydration tolerance in the Antarctic midge, Belgica antarctica, the world's southernmost insect and only insect endemic to Antarctica. Larvae of B. antarctica are remarkably tolerant of dehydration, surviving losses up to 70% of their body water. Gene expression changes in response to dehydration indicated up-regulation of cellular recycling pathways including the ubiquitin-mediated proteasome and autophagy, with concurrent down-regulation of genes involved in general metabolism and ATP production. Metabolomics results revealed shifts in metabolite pools that correlated closely with changes in gene expression, indicating that coordinated changes in gene expression and metabolism are a critical component of the dehydration response. Finally, using comparative genomics, we compared our gene expression results with a transcriptomic dataset for the Arctic collembolan, Megaphorura arctica. Although B. antarctica and M. arctica are adapted to similar environments, our analysis indicated very little overlap in expression profiles between these two arthropods. Whereas several orthologous genes showed similar expression patterns, transcriptional changes were largely species specific, indicating these polar arthropods have developed distinct transcriptional mechanisms to cope with similar desiccating conditions. physiological ecology | environmental stress

Mechanistic underpinnings of dehydration stress in the American dog tick revealed through RNA-Seq and metabolomics

“…Another potentially important gene that was up-regulated was a homolog of heat shock protein (Hsp)70. Hsps have been well studied in arthropod dehydration (Benoit and Denlinger, 2010) and up-regulation of Hsp70 has been noted during dehydration in various species Hayward et al, 2004;Teets et al, 2012). Hsps can act to prevent protein damage through chaperone activity or target damaged proteins to recycle peptides and amino acids (Feder and Hofmann, 1999;Goldberg, 2003).…”

The protective effect of rapid cold-hardening develops more quickly in frozen versus supercooled larvae of the Antarctic midge, Belgica antarctica

“…Considering the relatively long duration of the exposure (i.e. days), this dehydration-induced increase in freeze tolerance was likely accompanied by changes in gene expression (Teets et al, 2012a;Teets et al, 2013a). Because the RCH response occurs too quickly to allow changes in mRNA levels (Teets et al, 2012b), future study is needed to examine whether cellular dehydration without chilling could elicit larval cold-hardening within minutes to hours.…”

Contrasting strategies of resistance vs. tolerance to desiccation in two polar dipterans

“…The Arctic dipteran Heleomyza borealis utilizes desiccation resistance, while the Antarctic dipteran Eretmoptera murphyi principally uses desiccation tolerance. Divergence between Antarctic and Arctic invertebrates has also been shown between Belgica antarctica and Megaphorura arctica, which utilize distinct molecular mechanisms in response to desiccation (Teets et al 2012). Desiccation was found to induce cross-tolerance to low temperatures, but not high temperatures, in E. murphyi.…”

“…Larvae accumulate glycerol and trehalose, which are suggested as being replacements for lost water and/or an aid to the production of amorphous sugar glasses (Danks 2000;Benoit, LopezMartinez et al 2007;Michaud et al 2008;Bahrndorff et al 2009;Benoit et al 2009;Hengherr et al 2009;Clarke et al 2013). Protein denaturation is also ameliorated via the up-regulation of HSPs in response to desiccation Teets et al 2012), and the fluidity of the membrane maintained using enzymes such as D9 FAD desaturase (LopezMartinez et al 2009). Further physiological mechanisms induced in response to desiccation include oxidative damage repair through the accumulation of antioxidants , the minimization of mechanical stress via the restructuring of the cytoskeleton (Li et al 2009), the inhibition of apoptosis through the regulation of autophagy and the suppression of metabolism (Teets et al 2012).…”

“…Protein denaturation is also ameliorated via the up-regulation of HSPs in response to desiccation Teets et al 2012), and the fluidity of the membrane maintained using enzymes such as D9 FAD desaturase (LopezMartinez et al 2009). Further physiological mechanisms induced in response to desiccation include oxidative damage repair through the accumulation of antioxidants , the minimization of mechanical stress via the restructuring of the cytoskeleton (Li et al 2009), the inhibition of apoptosis through the regulation of autophagy and the suppression of metabolism (Teets et al 2012). Larvae of B. antarctica therefore possess a suite of physiological responses against injuries resulting from desiccation.…”