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°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.

Characterization of an ATP-dependent DNA ligase from the acidophilic archaeon “Ferroplasma acidarmanus” Fer1

“…The Euryarchaeota contains several members that grow at extremely low pH, including F. acidarmanus Fer1 and the other identified member of this family, F. acidiphilum (Edwards et al 2000;Golyshina and Timmis 2005). The Ferroplasmaceae lie within the order of Thermoplasmatales, which also contains the other characterized acidophiles, the Thermoplasmaceae and Picrophilaceae (Darland et al 1970;Futterer et al 2004;Golyshina et al 2006;Golyshina and Timmis 2005). The Thermoplasmatales are able to grow at very low pH, typically <pH 2, with Picrophilus torridus and F. acidarmanus Fer1 being the most extreme with growth observed at pH 0 (Dopson et al 2004;Futterer et al 2004).…”

“…The Ferroplasmaceae lie within the order of Thermoplasmatales, which also contains the other characterized acidophiles, the Thermoplasmaceae and Picrophilaceae (Darland et al 1970;Futterer et al 2004;Golyshina et al 2006;Golyshina and Timmis 2005). The Thermoplasmatales are able to grow at very low pH, typically <pH 2, with Picrophilus torridus and F. acidarmanus Fer1 being the most extreme with growth observed at pH 0 (Dopson et al 2004;Futterer et al 2004). However, all of these organisms are believed to maintain an intracellular pH of around 5 (Golyshina et al 2006;Golyshina and Timmis 2005;Macalady et al 2004;Searcy 1976).…”

Transcriptomic analysis reveals how a lack of potassium ions increases Sulfolobus acidocaldarius sensitivity to pH changes

“…Several reports provide circumstantial evidence that the acidophile membrane potential is created by potassium, and to a lesser extent, sodium ions. These include that cations (potassium ions are the most effective) are required for respiration-linked proton extrusion in Sulfolobus species (Sch€ afer, 1996); generation of a membrane potential in Acidithiobacillus thiooxidans requires the presence of cations, with potassium being the most efficient (Suzuki et al, 1999); and the presence of numerous putative cation transporters found in the genome of acidophiles (Chen et al, 2005;Fütterer et al, 2004;She et al, 2001;Tyson et al, 2004). However, the mechanism for membrane potential generation is poorly understood (Slonczewski et al, 2009).…”

“…Acidophiles utilize a number of methods to maintain a near neutral intracellular pH. These include an internal positive membrane potential suggested to be generated by cations (Cox et al, 1979); primary proton transporters during electron transport (Ferguson & Ingledew, 2008); secondary proton transporters (Fütterer et al, 2004); proton-tight membranes [based on tetra-ether lipids in archaea (van de Vossenberg et al, 1998)]; and proton-consuming reactions (Mangold et al, 2013). High external concentrations of anions such as chloride are particularly toxic to acidophiles as the cells import competing ions (including protons) to balance the osmotic pressure that dissipates the trans-membrane proton gradient causing cell death (Suzuki et al, 1999).…”

GATC Methylation by Dam methylase in archaea: its roles and possible transcription regulation by an FFRP

“…In addition, two more enzymes in this group were found in genomes sequenced recently, i.e. Picrophilus torridus 39) and Methanococcus maripaludis 40) (Fig. 3a).…”