Biochemical diversity among sulfur-dependent, hyperthermophilic microorganisms

Abstract

Hyperthermophiles are a recently discovered group of microorganisms that grow at and above 90 degrees C. They currently comprise over 20 different genera, and except for two novel bacteria, all are classified as Archaea. The majority of these organisms are obligately anaerobic heterotrophs that reduce elemental sulfur (S degree) to H2S. The best studied from a biochemical perspective are the archaeon, Pyrococcus furiosus, and the bacterium, Thermotoga maritima, both of which are saccharolytic. P. furiosus is thought to contain a new type of Entner-Doudoroff pathway for the conversion of carbohydrates ultimately to acetate, H2 and CO2. The pathway is independent of nicotinamide nucleotides and involves novel types of ferredoxin-linked oxidoreductases, one of which has tungsten, a rarely used element, as a prosthetic group. The only site of energy conservation is at the level of acetyl CoA, which is the presence of ADP and phosphate is converted to acetate and ATP in a single step. In contrast, T. maritima utilizes a conventional Embden-Meyerhof pathway for sugar oxidation. P. furiosus also utilizes peptides as a sole carbon and energy source. Amino acid oxidation is thought to involve glutamate dehydrogenase together with at least three types of novel ferredoxin-linked oxidoreductases which catalyze the oxidation of 2-ketoglutarate, aryl pyruvates and formaldehyde. One of these enzymes also utilizes tungsten. In P. furiosus, virtually all of the reductant that is generated during the catabolism of both carbohydrates and peptides is channeled to a cytoplasmic hydrogenase. This enzyme is now termed sulhydrogenase, as it reduces both protons to H2 and S degrees (or polysulfide) to H2S. S degrees reduction appears to lead to the conservation of energy in P. furiosus but not in T. maritima, although the mechanism by which this occurs is not known.

Tungsten in biological systems

“…In an attempt to enhance the growth yields of P. furiosus, the addition of salts of elements such as V, Se, Cs, F, Pb, Rb and additional Ni to the mineral salts solution were unsuccessful, whereas the addition of W (10 /xM) and additional Fe (final concentration, 25 /zM) to the growth medium gave a 5-10 fold increase in cell yields (wet weight) from large scale fermenter runs. Although the effect of W on growth kinetics and final cell densities were not reported, this preliminary study clearly indicated a role for W in the metabolism of P. furiosus, and perhaps in other heterotrophic archaea ( [126], reviewed in [22,[36][37][38][129][130][131][132][133]). Moreover, it led to the purification of the first W-containing iron-sulfur protein from this organism [31 ].…”

Diversity of Thermophilic Anaerobes

“…95 Many Archaea were initially described as being obligately dependent on S 0 reduction for the production of energy. 61 However, Bonch-Osmolovskaya and Stetter showed that some so-called "sulfur-dependent" Archaea grow well in co-culture with hydrogen-using thermophilic methanogens in the absence of sulfur. This is possible through interspecies hydrogen transfer, whereby growth-inhibiting hydrogen (from H + used as an electron acceptor) is removed without sulfur serving as the electron acceptor.…”

Carbohydrate cycling in micro-organisms: what can C-NMR tell us?

“…The occurrence of the ED cycle was initially demonstrated in Xanthomonas phaseoli [73]. It is known to operate also in other proteobacteria^including Acetobacter, Agrobacterium, Azotobacter, Pseudomonas, Rhizobium, Thiobacillus [72], and other Xanthomonas species (Letisse and Lindley, personal communication)^but it has not been reported so far in other ED-utilising species, including the archaebacteria currently under investigation [74,75], or in other bacteria and fungi. Bacteria utilising the ED cycle have common metabolic characteristics, including the preferential utilisation of organic acids over carbohydrates and the ability to synthesise exopolysaccharides.…”