Functional adaptations of the bacterial chaperone trigger factor to extreme environmental temperatures

Abstract

Summary Trigger factor (TF) is the first molecular chaperone interacting cotranslationally with virtually all nascent polypeptides synthesized by the ribosome in bacteria. Thermal adaptation of chaperone function was investigated in TFs from the Antarctic psychrophile Pseudoalteromonas haloplanktis, the mesophile Escherichia coli and the hyperthermophile Thermotoga maritima. This series covers nearly all temperatures encountered by bacteria. Although structurally homologous, these TFs display strikingly distinct properties that are related to the bacterial environmental temperature. The hyperthermophilic TF strongly binds model proteins during their folding and protects them from heat‐induced misfolding and aggregation. It decreases the folding rate and counteracts the fast folding rate imposed by high temperature. It also functions as a carrier of partially folded proteins for delivery to downstream chaperones ensuring final maturation. By contrast, the psychrophilic TF displays weak chaperone activities, showing that these functions are less important in cold conditions because protein folding, misfolding and aggregation are slowed down at low temperature. It efficiently catalyses prolyl isomerization at low temperature as a result of its increased cellular concentration rather than from an improved activity. Some chaperone properties of the mesophilic TF possibly reflect its function as a cold shock protein in E. coli.

Insights into thermoadaptation and the evolution of mesophily from the bacterial phylum Thermotogae

“…For example, the predicted chaperone TM1083 in T. maritima is thought to stabilize the DNA gyrase enzyme at temperatures near optimal growth (Canaves 2004). Moreover, the molecular chaperone trigger factor (TM0694) from T. maritima strongly binds model proteins and decreases their folding rate, while these activities are much weaker in the homologous trigger factor from the psychrophile Pseudoalteromonas haloplanktis, which instead shows increased prolyl isomerization (Godin-Roulling et al 2015). However, it should be noted that chaperones, although always highly expressed in thermophiles, are part of their high temperature response as well.…”

Cloning, characterization and anion inhibition studies of a new γ-carbonic anhydrase from the Antarctic bacterium Pseudoalteromonas haloplanktis

“…52 In the present paper, we describe the cloning, expression and purification of a c-CA identified in the genome of Pseudoalteromonas haloplanktis (formerly known as Alteromonas haloplanktis) 53 which is an obligate aerobic Gram-negative rod-like bacterium, isolated from seawater sampled along the Antarctic ice shelf. 54,55 The analysis of genomic DNA from the aforementioned psychrophilic bacterium revealed that it encodes CAs belonging to the b-and c-classes. Intriguingly, also the genome of this Gramnegative bacterium does not encode for a periplasmic a-CA, as seen for other Gram-negative bacteria and as mentioned above.…”

Genomic insights into temperature-dependent transcriptional responses of Kosmotoga olearia, a deep-biosphere bacterium that can grow from 20 to 79 °C

“…For instance, K. olearia has three temperature-responsive peptidylprolyl isomerase (PPIase) genes: two PpiC-type genes (Kole_1682 and Kole_0383) that are both highly expressed at 40 °C, and one FKBP-type gene (Kole_1745) that shows high expression at all temperatures except 77 °C (Table S5). At lower temperatures (e.g., 37 °C), these enzymes catalyze proline isomerization, which happens spontaneously at higher temperatures (Godin-Roulling et al 2015 ). However, the enzymes known to assist protein folding under cellular stress, chaperones [GroEL (Kole_1627) and Hsp70 (Kole_0886)] and protease Do (Kole_1599), were significantly down-regulated at 40 °C (Table S5; Fig.…”

“…At the moderately sub-optimal growth temperature of 40 °C, K. olearia cells face physiological challenges of proper protein folding (Godin-Roulling et al 2015 ), and of maintenance of a functional cell membrane (de Mendoza 2014 ). Our observation that at 40 °C, despite the lower growth rate, lipid metabolism genes were among the most highly expressed genes suggests that changes to the cell membrane composition are one of the most important adaptations for survival of K. olearia at lower temperatures.…”