Protein cold adaptation strategy via a unique seven-amino acid domain in the icefish ( Chionodraco hamatus ) PEPT1 transporter

Abstract

Adaptation of organisms to extreme environments requires proteins to work at thermodynamically unfavorable conditions. To adapt to subzero temperatures, proteins increase the flexibility of parts of, or even the whole, 3D structure to compensate for the lower thermal kinetic energy available at low temperatures. This may be achieved through single-site amino acid substitutions in regions of the protein that undergo large movements during the catalytic cycle, such as in enzymes or transporter proteins. Other strategies of cold adaptation involving changes in the primary amino acid sequence have not been documented yet. In Antarctic icefish ( Chionodraco hamatus ) peptide transporter 1 (PEPT1), the first transporter cloned from a vertebrate living at subzero temperatures, we came upon a unique principle of cold adaptation. A de novo domain composed of one to six repeats of seven amino acids (VDMSRKS), placed as an extra stretch in the cytosolic COOH-terminal region, contributed per se to cold adaptation. VDMSRKS was in a protein region uninvolved in transport activity and, notably, when transferred to the COOH terminus of a warm-adapted (rabbit) PEPT1, it conferred cold adaptation to the receiving protein. Overall, we provide a paradigm for protein cold adaptation that relies on insertion of a unique domain that confers greater affinity and maximal transport rates at low temperatures. Due to its ability to transfer a thermal trait, the VDMSRKS domain represents a useful tool for future cell biology or biotechnological applications.

Genetic control of plasticity of oil yield for combined abiotic stresses using a joint approach of crop modelling and genome‐wide association

“…In plants, these transporters are key players in nitrogen nutrition and therefore plantlet growth. The importance of oligopeptide transport to tolerate cold is corroborated by the demonstrated molecular adaptation of this transporter family in antarctic icefish ( Chionodraco hamatus ) adapted to sub‐zero temperatures (Maffia et al ; Rizzello et al ). The role in N nutrition of these transporters in animal and plants indicates that nutrient transport can be a limiting factor at low temperature that likely limits remobilization of seed stocks and/or absorption and transport of N from roots to aerial organs.…”

Teleost fish models in membrane transport research: the PEPT1(SLC15A1) H+–oligopeptide transporter as a case study

“…rabbit) and not to the zebrafish model. Interestingly, when functionally analysed, the Atlantic salmon PEPT1 exhibited only a slight pH dependence of the maximal transport rate (Rønnestad et al ) while the Antarctic icefish showed no pH dependence of the maximal transport rate (Rizzello et al ), which suggests conformance of both transporters to the rabbit/sea bass paradigm.…”

“…However, in the Antarctic icefish (polar poikilotherm living at −1.9°C; http://www.fishbase.org) it has recently been found that a de novo domain composed of one to six repeats of seven amino acids (VDMSRSK), placed as an extra stretch in the cytosolic COOH‐terminal region of PEPT1 (Supplemental Fig. S1), contributes in part – but per se – to cold adaptation (Rizzello et al ). VDMSRSK is in a protein region not involved in transport activity and, notably, when transferred to the COOH terminus of the rabbit (warm‐adapted) transporter, it confers cold adaptation to this protein.…”

Acquisition of alanyl‐alanine in an Agnathan: Characteristics of dipeptide transport across the hindgut of the Pacific hagfish Eptatretus stoutii

“…Interestingly, there was no significant change in L ‐ala‐ala uptake rate with altered mucosal pH (Figure ). This is distinct from studies in the nematode Caenorhabditis elegans , teleosts and mammals, which describe pH‐dependence of dipeptide uptake and an optimum uptake occurring from pH 5.5–6.0 (Benner et al ., ; Fujisawa et al ., ; Rizzello et al ., ; Spanier, ). Conversely, zebrafish Danio rerio (Hamilton 1822) have an elevated rate of transport at more alkaline pH (8.5).…”