Abstract
Haloferax volcanii uses extracellular DNA as a source for carbon, nitrogen, and phosphorous. However, it can also grow to a limited extend in the absence of added phosphorous, indicating that it contains an intracellular phosphate storage molecule. As Hfx. volcanii is polyploid, it was investigated whether DNA might be used as storage polymer, in addition to its role as genetic material. It could be verified that during phosphate starvation cells multiply by distributing as well as by degrading their chromosomes. In contrast, the number of ribosomes stayed constant, revealing that ribosomes are distributed to descendant cells, but not degraded. These results suggest that the phosphate of phosphate-containing biomolecules (other than DNA and RNA) originates from that stored in DNA, not in rRNA. Adding phosphate to chromosome depleted cells rapidly restores polyploidy. Quantification of desiccation survival of cells with different ploidy levels showed that under phosphate starvation Hfx. volcanii diminishes genetic advantages of polyploidy in favor of cell multiplication. The consequences of the usage of genomic DNA as phosphate storage polymer are discussed as well as the hypothesis that DNA might have initially evolved in evolution as a storage polymer, and the various genetic benefits evolved later.
Highlights
The advantages of polyploidy that led to its development in evolution has long been discussed in the framework of eukaryotes, because prokaryotes were long thought to be typically monoploid, which is often erroneously termed ‘‘haploid’’
We add an additional evolutionary advantage of polyploidy that does not require the pre-existence of homologous recombination, namely the usage of genomic DNA as a storage polymer
Here we show that nutrient availability determines ploidy level and that extracellular and intracellular genomic DNA is used as a storage polymer
Summary
The advantages of polyploidy that led to its development in evolution has long been discussed in the framework of eukaryotes, because prokaryotes were long thought to be typically monoploid (a single copy of the chromosome before replication), which is often erroneously termed ‘‘haploid’’. Evolutionary explanations for organisms with homologous sets of chromosomes have long been linked to the invention of sexual reproduction [1], and have been developed from mathematical modeling using population genetics principles and assumptions Those analyses indicate that ploidy levels $2 n could be selectively advantageous by preventing the expression of deleterious recessive alleles [2]. Though interesting and biological relevant, this polyploidy system probably has evolved rather late in evolution because a giant cell size requires a cytoskeleton and advanced intracellular transport. Another example is the bacterium Deinococcus radiodurans, which survives high doses of ionizing radiation that generate hundreds of double strand breaks. The experiments revealing that a prokaryotic species uses DNA as a storage polymer were performed with Haloferax volcanii, a halophilic archaeon
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