High hydrostatic pressure adaptive strategies in an obligate piezophile Pyrococcus yayanosii

Abstract

Pyrococcus yayanosii CH1, as the first and only obligate piezophilic hyperthermophilic microorganism discovered to date, extends the physical and chemical limits of life on Earth. It was isolated from the Ashadze hydrothermal vent at 4,100 m depth. Multi-omics analyses were performed to study the mechanisms used by the cell to cope with high hydrostatic pressure variations. In silico analyses showed that the P. yayanosii genome is highly adapted to its harsh environment, with a loss of aromatic amino acid biosynthesis pathways and the high constitutive expression of the energy metabolism compared with other non-obligate piezophilic Pyrococcus species. Differential proteomics and transcriptomics analyses identified key hydrostatic pressure-responsive genes involved in translation, chemotaxis, energy metabolism (hydrogenases and formate metabolism) and Clustered Regularly Interspaced Short Palindromic Repeats sequences associated with Cellular apoptosis susceptibility proteins.

Figure 1. Four-way Venn diagram of orthologous genes calculated by reciprocal hits.

P. yayanosii (yellow), P. furiosus (green), P. horikoshii (blue) and P. abyssi (purple). Numbers shown in the Venn diagram correspond to the orthologous gene groups given in the respective patterns. arCOG categories represent the information storage and processing (orange palette), cellular processes and signaling (green palette), metabolism (blue palette) and poorly characterized genes (grey palette).

Figure 2. Venn diagram of protein and gene regulation in P. yayanosii.

Genes are shown in purple, and proteins in blue. Upregulated elements are marked in italics and downregulated elements in underlined.

Figure 3. Regulated clusters under low and high pressure.

(A) Ribosomal clusters, (B) Formate and hydrogenase clusters, (C) Sulfhydrogenase cluster. The arrows represent the genes, the ovals the RNA expression and the rectangles the protein expression results. Red indicates upregulation and blue indicates downregulation on conditions given on the left. The green bar corresponds to the cluster fdh2-mfh2-mnh2 that was described in T. onnurineus as responsible for formate metabolism. The purple bar corresponds to the Mbh cluster that was described in P. furiosus as involved in the reduction of protons to H₂.

Figure 4. Schematic representation of the main regulations observed at low and high pressure.

Here are represented the formate metabolism (green), Mbh Hydrogenase (light orange), Mbx sulfhydrogenase (blue), SHI and SHII sulfhydrogenase (dark orange), the chemotaxis system along the archaellum, CRISPR/cas system, membrane-bound ATPase and the translation and replication complexes. The transcriptomic regulation is presented on the left whereas the proteomic one is on the right side. Blue and red arrows represent the sub- and over-expression in stress conditions (20 or 80 MPa) compared to the optimum condition (52 MPa). The circle and arrow lines correspond to the regulation at respectively 20 and 80 MPa. The differences observed for the CRISPR/cas system is due to the opposite regulations of the different clusters.