Neofunctionalization of S-adenosylmethionine decarboxylase into pyruvoyl-dependent L-ornithine and L-arginine decarboxylases is widespread in bacteria and archaea

• Published in: The Journal of biological chemistry Vol. 299; no. 8; p. 105005
• Main Authors: Li, Bin, Liang, Jue, Phillips, Margaret A., Michael, Anthony J.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01-08-2023; American Society for Biochemistry and Molecular Biology
• Subjects: Adenosylmethionine Decarboxylase - genetics; Adenosylmethionine Decarboxylase - metabolism; agmatine; Archaea - genetics; Archaea - metabolism; arginine; Arginine - genetics; Bacteria - metabolism; Carboxy-Lyases - genetics; Carboxy-Lyases - metabolism; decarboxylase; neofunctionalization; Ornithine; Ornithine Decarboxylase - metabolism; Phylogeny; polyamine; Polyamines - metabolism; putrescine; pyruvoyl; S-adenosylmethionine; SpdSyn/SpeE; decarboxylase; AIH/AguA; NCAPH/AguB; agmatine; HSS; ODC/SpeC; S-adenosylmethionine; ADC/SpeA; polyamine; AdoMetDC/SpeD; ornithine; MAG; arginine; AUH; HGT; PLP; SpeY; CASDH; CASDC; neofunctionalization; putrescine; pyruvoyl
• ISSN: 0021-9258; 1083-351X
• DOI: 10.1016/j.jbc.2023.105005

S-adenosylmethionine decarboxylase (AdoMetDC/SpeD) is a key polyamine biosynthetic enzyme required for conversion of putrescine to spermidine. Autocatalytic self-processing of the AdoMetDC/SpeD proenzyme generates a pyruvoyl cofactor from an internal serine. Recently, we discovered that diverse bacteriophages encode AdoMetDC/SpeD homologs that lack AdoMetDC activity and instead decarboxylate L-ornithine or L-arginine. We reasoned that neofunctionalized AdoMetDC/SpeD homologs were unlikely to have emerged in bacteriophages and were probably acquired from ancestral bacterial hosts. To test this hypothesis, we sought to identify candidate AdoMetDC/SpeD homologs encoding L-ornithine and L-arginine decarboxylases in bacteria and archaea. We searched for the anomalous presence of AdoMetDC/SpeD homologs in the absence of its obligatory partner enzyme spermidine synthase, or the presence of two AdoMetDC/SpeD homologs encoded in the same genome. Biochemical characterization of candidate neofunctionalized genes confirmed lack of AdoMetDC activity, and functional presence of L-ornithine or L-arginine decarboxylase activity in proteins from phyla Actinomycetota, Armatimonadota, Planctomycetota, Melainabacteria, Perigrinibacteria, Atribacteria, Chloroflexota, Sumerlaeota, Omnitrophota, Lentisphaerota, and Euryarchaeota, the bacterial candidate phyla radiation and DPANN archaea, and the δ-Proteobacteria class. Phylogenetic analysis indicated that L-arginine decarboxylases emerged at least three times from AdoMetDC/SpeD, whereas L-ornithine decarboxylases arose only once, potentially from the AdoMetDC/SpeD-derived L-arginine decarboxylases, revealing unsuspected polyamine metabolic plasticity. Horizontal transfer of the neofunctionalized genes appears to be the more prevalent mode of dissemination. We identified fusion proteins of bona fide AdoMetDC/SpeD with homologous L-ornithine decarboxylases that possess two, unprecedented internal protein-derived pyruvoyl cofactors. These fusion proteins suggest a plausible model for the evolution of the eukaryotic AdoMetDC.