The Piezo-Hyperthermophilic Archaeon Thermococcus piezophilus Regulates Its Energy Efficiency System to Cope With Large Hydrostatic Pressure Variations

Abstract

Deep-sea ecosystems share a common physical parameter, namely high hydrostatic pressure (HHP). Some of the microorganisms isolated at great depths have a high physiological plasticity to face pressure variations. The adaptive strategies by which deep-sea microorganisms cope with HHP variations remain to be elucidated, especially considering the extent of their biotopes on Earth. Herein, we investigated the gene expression patterns of Thermococcus piezophilus, a piezohyperthermophilic archaeon isolated from the deepest hydrothermal vent known to date, under sub-optimal, optimal and supra-optimal pressures (0.1, 50, and 90 MPa, respectively). At stressful pressures [sub-optimal (0.1 MPa) and supra-optimal (90 MPa) conditions], no classical stress response was observed. Instead, we observed an unexpected transcriptional modulation of more than a hundred gene clusters, under the putative control of the master transcriptional regulator SurR, some of which are described as being involved in energy metabolism. This suggests a fine-tuning effect of HHP on the SurR regulon. Pressure could act on gene regulation, in addition to modulating their expression.

Keywords: hydrothermal; piezophile; pressure; thermococci; transcriptomics.

FIGURE 1

Read mapping and differential gene expression as a function of pressure variation. After normalization, the TPM were mapped on concatenated CDSs of T. piezophilus (A). Some of the pressure-regulated genes or gene clusters are highlighted. The concentric circles represent the 3 conditions. Each ray represents a gene expression level (B), ordered according to the position of the gene on the genome (indicated by the scale in the center). The logFC values were used for signal intensity and the color black was given for the maximum. Key genes of the hydrogenogenic/sulfidogenic metabolisms are displayed. These representations were made with Anvi’o (Eren et al., 2015). (C) Z-score hierarchical clustering heat map for visualization of the 3 biological replicates (a, b, and c) per pressure.

FIGURE 2

MBH, MBS, SHI, SHII, and SurR gene clusters regulated in hydrogenogenic/sulfidogenic metabolisms and their SurR binding motifs. (A) Mrp-Mbh; (B) Mrp-Mbs; (C) SHI; (D) SHII; (E) SurR and Pdo. Each gene is colored according to its differential expression condition (0.1 MPa in blue, 50 MPa in green, or 90 MPa in red). Triangles represent the SurR binding motifs. Red triangle is for the short binding motif (GTTn₃AAC) and blue triangle is for the long one (GTTn₃AACn₅GTT). The asterisk means that the motif carries a mutation. The other gene clusters regulated in hydrogenogenic/sulfidogenic metabolisms are shown in Supplementary Figure 2.

FIGURE 3

Schematic representation of the main transcriptional metabolic regulations observed at sub-optimal (0.1 MPa) and supra-optimal (90 MPa) pressures for growth. This figure is centered on the general metabolism and focuses notably on hydrogenases and energy conversion processes and on their transcriptional regulator SurR, in the context of adaptive response to hydrostatic pressure. Blue and red arrows represent the overexpression (up direction) and subexpression (down direction) of genes at sub-optimal (0.1 MPa), and supra-optimal (90 MPa) pressures for growth, respectively, compared to the optimal pressure for growth (50 MPa).