Abstract

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 nonhomologous AR-fold suggests that polyamine biosynthesis may be inevitable.

Highlights

  • The polyamine spermidine is found throughout bacteria, archaea, and eukaryotes [1], and phylogenetic evidence indicates that it was synthesized in the Last Universal Common

  • Using various ancestral aADC and aODC amino acid sequences from bacteria with BLASTP searches of archaeal genomes, we identified a number of archaeal genomes encoding a single ancestral form aspartate aminotransferase (AAT)-fold decarboxylase homologue

  • The only known catalytic activity in the ancestral form AAT-fold decarboxylase homologues was the decarboxylation of L-arginine

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Summary

Introduction

The polyamine spermidine is found throughout bacteria, archaea, and eukaryotes [1], and phylogenetic evidence indicates that it was synthesized in the Last Universal Common. PCC 6803 essentially eliminated spermidine production even though an ancestral form AAT-fold SpeA homologue (WP_010871419; 40% protein identity to B. subtilis SpeA) is encoded in the genome [36].

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