Page 217 - The Biochemistry of Inorganic Polyphosphates

15:45
Char Count= 0
March 9, 2004
WU095/Kulaev
WU095-10
Polyphosphates and pyrophosphates 201
fermentation of hexoses to lactic acid and ethanol. This suggestion was based first of
all on a very reasonable assumption that when life originated on Earth the atmosphere
did not contain oxygen but possessed reducing properties, and that a variety of organic
substances were present in abundance on the Earth’s surface. Secondly, all retained and
most essential energy-providing mechanisms encountered in living organisms today (the
cleavage of hexoses during respiration and the pentose phosphate and photosynthetic cycles)
involveanaerobicfermentationreactions.Fromtheseconsiderations,itmaybededucedwith
a reasonable degree of certainty that in primitive living organisms the principal, and perhaps
the only, energy-providing process was anaerobic fermentation of hexoses, which seemed
to be already present in the ‘primeval soup’.
On the basis of results (Uryson and Kulaev, 1968; 1970; Kulaev et al., 1971; Szymona
et al., 1962), Kulaev (1971) has suggested that the energy-providing processes involved in
glycolysis were mediated in the earliest organisms by high-molecular-weight PolyPs rather
than by ATP and pyrophosphate.
In certain contemporary organisms, for instance, bacteria and fungi, 3-phospho-D-
glyceroyl-phosphate:polyphosphate phosphotransferase activity was found (Kulaev and
Bobyk, 1971; Kulaev et al., 1971). The phosphate was transferred from 1,3-
diphosphoglyceric acid, not to ADP to form ATP, as one could expect from the Meyerhof–
Embden–Parnas scheme, but directly to PolyP. This fossil reaction was most expressed in
an adenine deficient yeast mutant under cell adaptation to ATP depletion.
The second ‘fossil’ reaction is phosphorylation of glucose, not by ATP but by PolyP.
The polyphosphate hexokinase activity was detected only in the phylogenetically ancient
organisms, which are closely related to each other (Table 10.1). It can be seen from the
latter that in the more ancient representatives of this group of microorganisms such as the
Micrococci, Tetracocci, Mycococci, and the propionic bacteria, polyphosphate hexokinase
activity exceeded that of ATP hexokinase, whereas in phylogenetically younger repre-
sentatives ATP hexokinase activity was substantially higher than that of polyphosphate
hexokinase.
As was shown by Phillips and co-workers (Phillips et al., 1993, 1999), PolyP and ATP
glucokinase activities are catalysed by a single enzyme. The data obtained by the investi-
gation of kinetic parameters of purified enzyme from some bacteria suggest a hypothesis of
gradual transition from PolyP to ATP as a phosphoryl donor in the course of evolution. Ac-
cording to 16s RNA sequence analysis (Stackelbrandt and Woese, 1981), Propionibacteria
are phylogenetically older than Mycobacteria. The purified enzymes of Propionibacterium
shermanii, Mycobacterium tuberculosis and Propionibacterium arabinosum differ in their
preference for PolyP. When the substrate specificity constant k cat /K m ratios, for the utiliza-
tion of PolyP and ATP were compared, it was found that the ratios decreased progressively
with the enzymes from older to younger organisms (Phillips et al., 1999). These results
show that utilization of PolyP as a donor of active phosphate in the phosphorylation of
glucose is apparently more ancient from the evolutionary point of view than utilization of
ATP.
The above experimental findings support the view of Belozersky (1958) who suggested
that the high-molecular-weight PolyPs in the earliest organisms functioned in the same way
as ATP in the contemporary organisms. Lipmann (1965) and Oparin (1965) also confirmed
this suggestion. They indicate that the high-molecular-weight PolyPs may be primarily
involved in protobionts in the coupling of glycolysis with the phosphorylation of sugars, for