Evolution and multiplicity of arginine decarboxylases in polyamine biosynthesis and essential role in Bacillus subtilis biofilm formation

Matthew Burrell, Colin C. Hanfrey, Ewan J. Murray, Nicola R. Stanley-Wall, Anthony J. Michael

Research output: Contribution to journalArticle

55 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)39224-39238
Number of pages15
JournalJournal of Biological Chemistry
Volume285
Issue number50
DOIs
StatePublished - Dec 10 2010

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Biosynthesis
Alanine Racemase
Polyamines
Biofilms
Bacilli
Bacillus subtilis
Bacteria
Aspartate Aminotransferases
Archaea
Escherichia coli
Acids
Crenarchaeota
Euryarchaeota
Chloroflexi
Acid resistance
Bacteroidetes
Decarboxylation
Carboxy-Lyases
Actinobacteria
Enzymes

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Molecular Biology

Cite this

Evolution and multiplicity of arginine decarboxylases in polyamine biosynthesis and essential role in Bacillus subtilis biofilm formation. / Burrell, Matthew; Hanfrey, Colin C.; Murray, Ewan J.; Stanley-Wall, Nicola R.; Michael, Anthony J.

In: Journal of Biological Chemistry, Vol. 285, No. 50, 10.12.2010, p. 39224-39238.

Research output: Contribution to journalArticle

Burrell, Matthew ; Hanfrey, Colin C. ; Murray, Ewan J. ; Stanley-Wall, Nicola R. ; Michael, Anthony J. / Evolution and multiplicity of arginine decarboxylases in polyamine biosynthesis and essential role in Bacillus subtilis biofilm formation. In: Journal of Biological Chemistry. 2010 ; Vol. 285, No. 50. pp. 39224-39238.
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