Page 222 - The Biochemistry of Inorganic Polyphosphates

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Polyphosphates in chemical and biological evolution
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adenine as compared with other nitrogenous bases, under conditions similar to those which
probably occurred in the pre-biological stage of the Earth’s development. It was also shown
that adenine is much more resistant to various types of radiation, which undoubtedly played
an important part in the processes taking place on the primeval Earth. A series of brilliant
investigations carried out by Ponnamperurna and co-workers (Ponnamperuma et al., 1963;
Rabinowitz et al., 1968; Schwartz and Ponnamperuma, 1968) demonstrated that adenosine
and adenosine polyphosphates could have been formed under conditions similar to those
which existed on the Earth at the time when life first appeared. It is very important to note
that in these investigations the abiogenic formation of ATP took place only in the presence
of ethyl polyphosphates or labile inorganic PolyPs. This makes even more plausible the
hypothesis that inorganic PolyPs, rather than ATP, were the first to appear and to function
as acceptors and donors of phosphate in primitive organisms.
At the following stages of evolution, three domains of extant life (Bacteria, Archaea,
Eucarya) have emerged from a multiphenotypical population of primarily chemolithoau-
thotrophic pre-cells by cellularization and further evolution (Woese et al., 1990; Kandler,
1993). In modern prokaryotes, in addition to the functions of energy and phosphate reserve,
the function of gene-activity control has become very significant. This function might arise
already in the RNA world, because of the great ability of PolyPs to form complexes with
RNA via divalent cations. It is not improbable that such complexes affected the catalytic
and replication properties of RNA molecules at this early stage of evolution.
The contemporary organisms with a low degree of organization are still heavily de-
pendent on the environment, and for this reason they need to possess a mechanism for
conserving large amounts of active phosphate. One such mechanism for the storage of ac-
tive phosphate in contemporary microorganisms, both prokaryotes and eukaryotes, remains
the accumulation of PolyPs, which renders them independent of the changes in their ex-
ternal environment to a substantial extent. Furthermore, an important factor leading to the
retention in contemporary organisms of the ability to accumulate high-molecular-weight
PolyPs appears to be the lack of balance of their metabolism. The accumulation of PolyPs
in these organisms appears to be an efficient means of detoxifying free P i and storing it in an
active form as PolyPs, so that they can be utilized for rapid growth once favourable condi-
tions for their development appear. In this case, the phosphorus and energy contained in the
PolyPs must greatly facilitate the rapid and simultaneous synthesis of large amounts of the
nucleic acids required at an early stage of rapid growth and cell division. If a microorganism
cannot accumulate PolyPs, the excess of P i in the medium becomes an unfavourable factor.
For example, the halophilic archae Halobacterium salinarium has no ability to synthesize
PolyPs in great amounts (Smirnov et al., 2002a,b). Thus, it accumulates P i in the form of
magnesium phosphate under P i excess in the medium. This leads to certain changes in cell
morphology and death of some part of the population.
The cells of the higher, multicellular organisms are to a lesser extent dependent on the
environment, and as a result the ability to accumulate large amounts of inorganic polyphos-
phates could have been lost during the evolutionary process. In certain highly specialized
organs in animals, in particular, the muscles, the requirement for a long-term depot of ac-
tivated phosphate again arose in the course of evolution because of the rhythmic nature of
muscular contraction. In this case, still more specialized forms of phosphorus and energy
storage appeared, namely, arginine phosphate and creatine phosphate. However, the active
phosphate stored in these phosphagens is both accumulated and utilized in muscle tissue