Abstract
Arginine decarboxylases (ADCs; EC 4.1.1.19) from four different protein fold families are important for polyamine biosynthesis in bacteria, archaea, and plants. Biosynthetic alanine racemase fold (AR-fold) ADC is widespread in bacteria and plants. We report the discovery and characterization of an ancestral form of the AR-fold ADC in the bacterial Chloroflexi and Bacteroidetes phyla. The ancestral AR-fold ADC lacks a large insertion found in Escherichia coli and plant AR-fold ADC and is more similar to the lysine biosynthetic enzyme meso-diaminopimelate decarboxylase, from which it has evolved. An E. coli acid-inducible ADC belonging to the aspartate aminotransferase fold (AAT-fold) is involved in acid resistance but not polyamine biosynthesis. We report here that the acid-inducible AAT-fold ADC has evolved from a shorter, ancestral biosynthetic AAT-fold ADC by fusion of a response regulator receiver domain protein to the N terminus. Ancestral biosynthetic AAT-fold ADC appears to be limited to firmicute bacteria. The phylogenetic distribution of different forms of ADC distinguishes bacteria from archaea, euryarchaeota from crenarchaeota, double-membraned from single-membraned bacteria, and firmicutes from actinobacteria. Our findings extend to eight the different enzyme forms carrying out the activity described by EC 4.1.1.19. ADC gene clustering reveals that polyamine biosynthesis employs diverse and exchangeable synthetic modules. We show that in Bacillus subtilis, ADC and polyamines are essential for biofilm formation, and this appears to be an ancient, evolutionarily conserved function of polyamines in bacteria. Also of relevance to human health, we found that arginine decarboxylation is the dominant pathway for polyamine biosynthesis in human gut microbiota.
Highlights
Present address: School of Molecular Medical Sciences, Centre for Biomolecular Sciences, University of Nottingham, Nottingham NG7 2RD, United Kingdom
An Ancestral Form of the Alanine Racemase Fold of Biosynthetic Arginine Decarboxylase—The biosynthetic alanine racemase fold (AR-fold) arginine decarboxylase (ADC) has an interdomain insertion of between 90 and 105 amino acids compared with other enzymes of the same structural class (16)
The pyridoxal 5Ј-phosphate (PLP)-dependent AR-fold family of basic amino acid decarboxylases most probably evolved by gene duplication from DAPDC, the last step in the lysine biosynthetic pathway
Summary
The essential requirements for spermidine and agmatine in hypusine and agmatidine formation, respectively, obscure other core physiological functions of polyamines in eukaryotes and archaea. We show that the firmicute AAT-fold biosynthetic ADC is an ancestral form of the acid-inducible ADC found in E. coli and lacks the N-terminal wing domain necessary for decamer formation. The Bacillus subtilis biosynthetic AAT-fold ADC is shown to be essential for biofilm formation, establishing that polyamines are involved in biofilm formation in single-membraned as well as doubled-membraned bacteria. This indicates that a role in biofilm formation may be an ancient physiological function of polyamines in bacteria. We show that the ADC route for putrescine biosynthesis is the dominant pathway for polyamine formation in the human gut microbiota
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