title: Independent evolutionary origins of functional polyamine biosynthetic enzyme fusions catalysing de novo diamine to triamine formation.
abstract: We have identified gene fusions of polyamine biosynthetic enzymes S-adenosylmethionine decarboxylase (AdoMetDC, speD) and aminopropyltransferase (speE) orthologues in diverse bacterial phyla. Both domains are functionally active and we demonstrate the novel de novo synthesis of the triamine spermidine from the diamine putrescine by fusion enzymes from β-proteobacterium Delftia acidovorans and δ-proteobacterium Syntrophus aciditrophicus, in a ΔspeDE gene deletion strain of Salmonella enterica sv. Typhimurium. Fusion proteins from marine α-proteobacterium Candidatus Pelagibacter ubique, actinobacterium Nocardia farcinica, chlorobi species Chloroherpeton thalassium, and β-proteobacterium D. acidovorans each produce a different profile of non-native polyamines including sym-norspermidine when expressed in Escherichia coli. The different aminopropyltransferase activities together with phylogenetic analysis confirm independent evolutionary origins for some fusions. Comparative genomic analysis strongly indicates that gene fusions arose by merger of adjacent open reading frames. Independent fusion events, and horizontal and vertical gene transfer contributed to the scattered phyletic distribution of the gene fusions. Surprisingly, expression of fusion genes in E. coli and S. Typhimurium revealed novel latent spermidine catabolic activity producing non-native 1,3-diaminopropane in these species. We have also identified fusions of polyamine biosynthetic enzymes agmatine deiminase and N-carbamoylputrescine amidohydrolase in archaea, and of S-adenosylmethionine decarboxylase and ornithine decarboxylase in the single-celled green alga Micromonas.
authors.affiliation: Institute of Food Research, Norwich Research Park, Colney, Norwich NR47UA, UK.
authors.forename: Robert
authors.initials: R
authors.lastname: Green
authors.forename: Colin C
authors.initials: CC
authors.lastname: Hanfrey
authors.forename: Katherine A
authors.initials: KA
authors.lastname: Elliott
authors.forename: Diane E
authors.initials: DE
authors.lastname: McCloskey
authors.forename: Xiaojing
authors.initials: X
authors.lastname: Wang
authors.forename: Sreenivas
authors.initials: S
authors.lastname: Kanugula
authors.forename: Anthony E
authors.initials: AE
authors.lastname: Pegg
authors.forename: Anthony J
authors.initials: AJ
authors.lastname: Michael
mesh_terms: D012437:Adenosylmethionine Decarboxylase / Q000235:genetics* / Q000378:metabolism; D001105:Archaea / Q000235:genetics / Q000378:metabolism; D001419:Bacteria / Q000235:genetics / Q000378:metabolism; D053898:Biosynthetic Pathways / Q000235:genetics*; D019143:Evolution, Molecular; D050939:Gene Fusion; D011700:Putrescine / Q000378:metabolism*; D013095:Spermidine / Q000378:metabolism*; D011436:Spermidine Synthase / Q000235:genetics* / Q000378:metabolism
chemical_list: D011436:Spermidine Synthase; D012437:Adenosylmethionine Decarboxylase; D013095:Spermidine; D011700:Putrescine