Ferroplasma and relatives, recently discovered cell wall‐lacking archaea making a living in extremely acid, heavy metal‐rich environments

Abstract

SummaryFor several decades, the bacterium Acidithiobacillus (previously Thiobacillus ) has been considered to be the principal acidophilic sulfur-and iron-oxidizing microbe inhabiting acidic environments rich in ores of iron and other heavy metals, responsible for the metal solubilization and leaching from such ores, and has become the paradigm of such microbes. However, during the last few years, new studies of a number of acidic environments, particularly mining waste waters, acidic pools, etc., in diverse geographical locations have revealed the presence of new cell walllacking archaea related to the recently described, acidophilic, ferrous-iron oxidizing Ferroplasma acidiphilum. These mesophilic and moderately thermophilic microbes, representing the family Ferroplasmaceae, were numerically significant members of the microbial consortia of the habitats studied, are able to mobilize metals from sulfide ores, e.g. pyrite, arsenopyrite and copper-containing sulfides, and are more acid-resistant than iron and sulfur oxidizing bacteria exhibiting similar eco-physiological properties. Ferroplasma cell membranes contain novel caldarchaetidylglycerol tetraether lipids, which have extremely low proton permeabilities, as a result of the bulky isoprenoid core, and which are probably a major contributor to the extreme acid tolerance of these cell wall-less microbes. Surprisingly, several intracellular enzymes, including an ATP-dependent DNA ligase have pH optima close to that of the external environment rather than of the cytoplasm. Ferroplasma spp. are probably the major players in the biogeochemical cycling of sulfur and sulfide metals in highly acidic environments, and may have considerable potential for biotechnological applications such as biomining and biocatalysis under extreme conditions.

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

“…''Ferroplasma acidarmanus'' Fer1 (hereafter referred to as F. acidarmanus Fer1) is an acidophilic archaeon, which was first identified as a dominant prokaryote in the acid-drainage biofilm at Iron Mountain in Northern California (Dopson et al 2004;Edwards et al 2000;Golyshina and Timmis 2005;Tyson et al 2004). F. acidarmanus Fer1 is mesophilic, with optimal growth at about 40°C, but it survives in extremely acidic conditions, with optimal growth at pH 1.2.…”

“…F. acidarmanus Fer1 is mesophilic, with optimal growth at about 40°C, but it survives in extremely acidic conditions, with optimal growth at pH 1.2. This group of Archaea plays important roles in geochemical iron and sulphur cycles and has also been implicated as a major contributor in the process of acid mine drainage, which causes considerable environmental damage by the release of metal-rich acidic effluents into groundwater (Dopson et al 2004;Edwards et al 2000;Golyshina and Timmis 2005;Schleper et al 2005). Coupling these points with its unusual microbiology, identification of factors involved in the metabolism of F. acidarmanus Fer1 holds considerable interest for both applied and basic sciences.…”

“…The only family of cultured acidophiles among the Crenarchaeota are the Sulfolobaceae, which grow at pH 2-4 (Makarova and Koonin 2003;Makarova and Koonin 2005;She et al 2001). 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 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 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). Thus, the cytoplasmic conditions of these organisms are distinct from their environment, which is aided by the fact that their single cytoplasmic membrane has low permeability to protons (Golyshina et al 2006;Golyshina and Timmis 2005).…”