Independent evolutionary origins of functional polyamine biosynthetic enzyme fusions catalysing de novo diamine to triamine formation

Robert Green, Colin C. Hanfrey, Katherine A. Elliott, Diane E. Mccloskey, Xiaojing Wang, Sreenivas Kanugula, Anthony Pegg, Anthony J. Michael

Research output: Contribution to journalArticle

16 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)1109-1124
Number of pages16
JournalMolecular Microbiology
Volume81
Issue number4
DOIs
StatePublished - Aug 1 2011

Fingerprint

Proteobacteria
Diamines
Gene Fusion
Polyamines
Spermidine Synthase
Adenosylmethionine Decarboxylase
Spermidine
agmatine deiminase
Enzymes
Delftia acidovorans
Hydrocharitaceae
Chlorobi
Amidohydrolases
Escherichia coli
Nocardia
Horizontal Gene Transfer
Chlorophyta
Ornithine Decarboxylase
Salmonella enterica
Putrescine

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Molecular Biology

Cite this

Green, Robert ; Hanfrey, Colin C. ; Elliott, Katherine A. ; Mccloskey, Diane E. ; Wang, Xiaojing ; Kanugula, Sreenivas ; Pegg, Anthony ; Michael, Anthony J. / Independent evolutionary origins of functional polyamine biosynthetic enzyme fusions catalysing de novo diamine to triamine formation. In: Molecular Microbiology. 2011 ; Vol. 81, No. 4. pp. 1109-1124.
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Independent evolutionary origins of functional polyamine biosynthetic enzyme fusions catalysing de novo diamine to triamine formation. / Green, Robert; Hanfrey, Colin C.; Elliott, Katherine A.; Mccloskey, Diane E.; Wang, Xiaojing; Kanugula, Sreenivas; Pegg, Anthony; Michael, Anthony J.

In: Molecular Microbiology, Vol. 81, No. 4, 01.08.2011, p. 1109-1124.

Research output: Contribution to journalArticle

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