Comparative proteomics of stenotopic caddisfly Crunoecia irrorata identifies acclimation strategies to warming

Abstract

Species' ecological preferences are often deduced from habitat characteristics thought to represent more or less optimal conditions for physiological functioning. Evolution has led to stenotopic and eurytopic species, the former having decreased niche breadths and lower tolerances to environmental variability. Species inhabiting freshwater springs are often described as being stenotopic specialists, adapted to the stable thermal conditions found in these habitats. Whether due to past local adaptation these species have evolved or have lost intra‐generational adaptive mechanisms to cope with increasing thermal variability has, to our knowledge, never been investigated. By studying how the proteome of a stenotopic species changes as a result of increasing temperatures, we investigate if the absence or attenuation of molecular mechanisms is indicative of local adaptation to freshwater springs. An understanding of compensatory mechanisms is especially relevant as spring specialists will experience thermal conditions beyond their physiological limits due to climate change. In this study, the stenotopic species Crunoecia irrorata (Trichoptera: Lepidostomatidae, Curtis 1834) was acclimated to 10, 15 and 20°C for 168 hr. We constructed a homology‐based database and via liquid chromatography‐tandem mass spectrometry (LC‐MS/MS)‐based shotgun proteomics identified 1,358 proteins. Differentially abundant proteins and protein norms of reaction revealed candidate proteins and molecular mechanisms facilitating compensatory responses such as trehalose metabolism, tracheal system alteration and heat‐shock protein regulation. A species‐specific understanding of compensatory physiologies challenges the characterization of species as having narrow tolerances to environmental variability if that characterization is based on occurrences and habitat characteristics alone.

Mountain stoneflies may tolerate warming streams: Evidence from organismal physiology and gene expression

“…In this study, we explored the thermal physiology of high-elevation stoneflies inhabiting the meltwater of rapidly fading glaciers and snowfields in the Rocky Mountains. Our focal species are representative of an entire community that may be at risk of climate-induced extirpation (Giersch et al, 2017;Hotaling, Foley, et al, 2019;Tronstad et al, (Ebner et al, 2019;Gamboa, Tsuchiya, Matsumoto, Iwata, & Watanabe, 2017). Broadly, our findings and those of others (e.g., Ebner et al, 2019;Muhlfeld et al, 2020;Shah, Gill, et al, 2017;Treanor, Giersch, Kappenman, Muhlfeld, & Webb, 2013), challenge the prevailing notion that aquatic insect larvae living in extremely cold mountain streams cannot survive warming.…”

“…This knowledge gap is particularly important in light of the widely held assumption that aquatic insects living at high elevations are cold‐adapted stenotherms that will not tolerate warming streams (Giersch et al., 2015; Jacobsen et al., 2012). Recent evidence that the thermal maxima of high‐elevation stream taxa can exceed maximum water temperatures (e.g., Shah, Gill, et al., 2017), that spring‐dwelling cold stenotherms exhibit little variability in heat shock protein (HSP) expression across temperatures (e.g., Ebner, Ritz, & Von Fumetti, 2019), and that meltwater‐associated invertebrate communities persist despite widespread deglaciation (Muhlfeld et al., 2020) all challenge this assumption, raising new questions about whether climate warming directly threatens headwater biodiversity. To better understand the degree to which headwater species can tolerate warming, links between relevant traits at the organismal (thermal stress) and cellular (e.g., gene expression) level are needed.…”

Abiotic and past climatic conditions drive protein abundance variation among natural populations of the caddisfly Crunoecia irrorata

“…Integral parts of the cellular stress response include the evolutionary conserved heat-shock- and cold-shock-response (HSR and CSR), characterized by the expression of heat-shock proteins (Hsps). Putatively cold-adapted species have been shown to constitutively express Hsps to facilitate protein folding at low temperatures 128 , 129 , a phenomenon also observed in C. irrorata 46 . Here, we observed constitutive and increasing but also decreasing Hsp reaction norms with increasing in situ temperatures (Fig.…”

“…Enzyme specificity was set to fully tryptic, with a maximum of two missed cleavages. MS/MS spectra were searched against a previously described database consisting of translated gene-prediction sequences of Trichoptera species 46 , additionally including candidate protein-coding regions of Rhyacophila fasciata 47 ; BioProject: PRJNA219600). All searches included a contaminants database (as implemented in MaxQuant, 267 sequences).…”

Physiological adaptations to sugar‐mimic alkaloids: Insights from Bombyx mori for long‐term adaption and short‐term response

“…Sugar‐mimic alkaloids inhibit midgut hydrolysis activity thereby restraining trehalase uptake and trehalose utilization (Agrawal & Konno, 2009; Konno et al., 2006). Tret 1 mediates the bidirectional transfer of trehalose synthesized in the fat body (Ebner, Ritz, & Fumetti, 2019). In this study, Tret1 was upregulated after both sugar‐mimic alkaloid treatments.…”