Molecular chaperoning helps safeguarding mitochondrial integrity and motor functions in the Sahara silver ant Cataglyphis bombycina

Abstract

The Sahara silver ant Cataglyphis bombycina is one of the world’s most thermotolerant animals. Workers forage for heat-stricken arthropods during the hottest part of the day, when temperatures exceed 50 °C. However, the physiological adaptations needed to cope with such harsh conditions remain poorly studied in this desert species. Using transcriptomics, we screened for the most heat-responsive transcripts of C. bombycina with aim to better characterize the molecular mechanisms involved with macromolecular stability and cell survival to heat-stress. We identified 67 strongly and consistently expressed transcripts, and we show evidences of both evolutionary selection and specific heat-induction of mitochondrial-related molecular chaperones that have not been documented in Formicidae so far. This indicates clear focus of the silver ant’s heat-shock response in preserving mitochondrial integrity and energy production. The joined induction of small heat-shock proteins likely depicts the higher requirement of this insect for proper motor function in response to extreme burst of heat-stresses. We discuss how those physiological adaptations may effectively help workers resist and survive the scorching heat and burning ground of the midday Sahara Desert.

Adaptations to thermal stress in social insects: recent advances and future directions

“…the number of genes that are differentially expressed) differences in responses to environmental pressures in a variety of organisms, including plants, insects, molluscs, crustaceans, and fish (Ye et al ., 2014; Zhao et al ., 2014; Cañas et al ., 2015; Faddeeva et al ., 2015; Cheng, Hui, & Sha, 2019; Jesus et al ., 2019). In recent years, DGE studies in social insects have highlighted a number of genes that are involved in colony organisation and adaptation to environmental constraints (Ferreira et al ., 2013; Helmkampf et al ., 2016; Lucas, Romiguier, & Keller, 2017; Willot et al ., 2018; Holman et al ., 2019). However, such studies remain fairly rare, and many taxa are currently ignored.…”

“…Consistent with this finding, workers of a thermophilic seed‐harvester ant species ( Pogonomyrmex barbatus ) displayed greater constitutive expression and induction of hsp genes ( hsp83 , hsc70‐4 h1 , hsc70‐4 h2 , and hsp 40 ) in response to heat stress, compared to workers of a species found in more mesic habitats ( Aphaenogaster picea ) (Nguyen, Gotelli, & Cahan, 2016; Stanton‐Geddes et al ., 2016). In a study comparing Cataglyphis ants, constitutive expression of hsp70 was found to be correlated with local thermal conditions (Willot, Gueydan, & Aron, 2017; Willot et al ., 2018). Workers of the Saharan silver ant ( C. bombycina ) had high constitutive levels of Hsp70, even when they were in the nest, where the temperature was around 25°C (Gehring & Wehner, 1995; Willot, Gueydan, & Aron, 2017).…”

“…In the Saharan silver ant ( C. bombycina ), heat stress induces strong upregulation of hsp genes (Willot et al ., 2018), including hsc70‐5 and hsp60 , which encode Hsps involved in safeguarding mitochondrial integrity and function; unc‐89 , which encodes proteins involved in sarcomere assembly and organisation; and l(2)efl (from the Hsp20 family), which encodes proteins that affect the structural integrity of the cytoskeleton, organelle morphology, and the myofilaments. In this ant, it is crucial that muscle function is both structurally and metabolically maintained given that individuals need to run at high speeds to enhance convective cooling, reach thermal refuges as quickly as possible, and limit the time spent foraging on hot ground (Sommer & Wehner, 2012; Boulay et al ., 2017; Willot et al ., 2018). In the eastern honeybee ( Apis cerana ), upregulation of DnaJC3 (a member of the Hsp40 family) has been observed in the muscles and epidermis during both cold and heat stress (Zhang et al ., 2014; Zhang et al ., 2019).…”

Transcriptomic signatures of cold adaptation and heat stress in the winter ant (Prenolepis imparis)

“…We then ran two tests with these normalized data: (1) heat stressed ants (35˚C) versus control ants (21˚C) and (2) cold stressed ants (5˚C) versus control ants (21˚C). Transcripts were considered to be differentially expressed (DE) if i) the Benjamini and Hochberg adjusted false discovery rate (FDR) p-value was less than 0.01, ii) the absolute value of the fold-change (FC) � 2.0, and iii) the relative standard deviation (RSD) of expression between replicates was less than 0.4 [31].…”

“…There are very few studies of ants that have attempted to identify genes and pathways associated with a cold or hot stress response without a priori information. One recent study looked at gene expression in Cataglyphis bombycina during heat stress and documented induction of molecular chaperones [31]. However, we are unaware of studies that have documented genes induced during hot and cold stress in an ant with a preference for cold.…”