J Biol Chem. 2021 Sep 21. pii: S0021-9258(21)01022-X. [Epub ahead of print] 101219
Polyamines are fundamental molecules of life, and their deep evolutionary history is reflected in extensive biosynthetic diversification. The polyamines putrescine, agmatine and cadaverine, are produced by pyridoxal 5'-phosphate-dependent L-ornithine, L-arginine and L-lysine decarboxylases (ODC, ADC, LDC), respectively, from both the alanine racemase (AR) and aspartate aminotransferase (AAT) folds. Two homologous forms of AAT-fold decarboxylase are present in bacteria: an ancestral form and a derived, acid-inducible extended form containing an N-terminal fusion to the receiver-like domain of a bacterial response regulator. Only ADC was known from the ancestral form, and limited to the Firmicutes phylum, whereas extended forms of ADC, ODC and LDC are present in Proteobacteria and Firmicutes. Here, we report the discovery of ancestral form ODC, LDC, and bifunctional O/LDC, and extend the phylogenetic diversity of functionally characterized ancestral ADC, ODC and LDC to include phyla Fusobacteria, Caldiserica, Nitrospirae and Euryarchaeota. Using purified recombinant enzymes, we show that these ancestral forms have a nascent ability to decarboxylate kinetically less preferred amino acid substrates with low efficiency, and that product inhibition primarily affects preferred substrates. We also note a correlation between the presence of ancestral ODC and ornithine/arginine auxotrophy, and link this with a known symbiotic dependence on exogenous ornithine produced by species using the arginine deiminase system. Finally, we show that ADC, ODC and LDC activities emerged independently, in parallel, in the homologous AAT-fold ancestral and extended forms. The emergence of the same ODC, ADC, and LDC activities in the non-homologous AR-fold, suggests that polyamine biosynthesis may be inevitable.
Keywords: agmatine; arginine; cadaverine; decarboxylase; lysine; ornithine; polyamine; putrescine