Genome sequence of Picrophilus torridus and its implications for life around pH 0

Abstract

The euryarchaea Picrophilus torridus and Picrophilus oshimae are able to grow around pH 0 at up to 65 degrees C, thus they represent the most thermoacidophilic organisms known. Several features that may contribute to the thermoacidophilic survival strategy of P. torridus were deduced from analysis of its 1.55-megabase genome. P. torridus has the smallest genome among nonparasitic aerobic microorganisms growing on organic substrates and simultaneously the highest coding density among thermoacidophiles. An exceptionally high ratio of secondary over ATP-consuming primary transport systems demonstrates that the high proton concentration in the surrounding medium is extensively used for transport processes. Certain genes that may be particularly supportive for the extreme lifestyle of P. torridus appear to have been internalized into the genome of the Picrophilus lineage by horizontal gene transfer from crenarchaea and bacteria. Finally, it is noteworthy that the thermoacidophiles from phylogenetically distant branches of the Archaea apparently share an unexpectedly large pool of genes.

Fig. 1.

16S rRNA phylogenetic tree. Highlighted are the two thermoacidophilic groups of the archaea. Sequences were aligned with the clustalw algorithm. The tree was build by neighbor joining by using the Kimura 2-parameter for distance calculation.

Fig. 2.

Occurrence of homologous ORFs in P. torridus, T. acidophilum, and S. solfataricus. The size of the circles is proportional to the size of the genomes.

Fig. 3.

Overview of the transport, central metabolism, and energy production in P. torridus. Sugar, peptide, and amino acid uptake systems are shown in red, drug exporters are shown in pink, trace elements transport systems are shown in green, other and hypothetical transporters are shown in gray. Bold numbers mark the number of each transporter. Protein translocation systems are shown in violet, and the components of the respiratory chain are shown in yellow. A total of 93 secondary and 17 primary transporters were found in the genome sequence, resulting in an unusual ratio of 5.6:1. So far, no aldolase gene is found. Enzyme activity essays indicate a functional nonphosphorylated Entner Doudoroff pathway for glucolysis (unpublished data). Pathways for the respiration of the organic acids acetate, lactate, and propanoate were identified. NADH₂ and reduced ferredoxin is produced in the P. torridus central carbon metabolism but the final reducing compound of the NADH-oxidoreductase is still unknown as no electron-input module for it was detected.