Evolution and multifarious horizontal transfer of an alternative biosynthetic pathway for the alternative polyamine sym-homospermidine

Frances L. Shaw, Katherine A. Elliott, Lisa N. Kinch, Christine Fuell, Margaret A. Phillips, Anthony J. Michael

Research output: Contribution to journalArticle

34 Citations (Scopus)

Abstract

Polyamines are small flexible organic polycations found in almost all cells. They likely existed in the last universal common ancestor of all extant life, and yet relatively little is understood about their biological function, especially in bacteria and archaea. Unlike eukaryotes, where the predominant polyamine is spermidine, bacteria may contain instead an alternative polyamine, sym-homospermidine. We demonstrate that homospermidine synthase (HSS) has evolved vertically, primarily in the α-Proteobacteria, but enzymatically active, diverse HSS orthologues have spread by horizontal gene transfer to other bacteria, bacteriophage, archaea, eukaryotes, and viruses. By expressing diverse HSS orthologues in Escherichia coli, we demonstrate in vivo the production of co-products diaminopropane and N1-aminobutylcadaverine, in addition to sym-homospermidine. We show that sym-homospermidine is required for normal growth of the α-proteobacterium Rhizobium leguminosarum. However, sym-homospermidine can be replaced, for growth restoration, by the structural analogues spermidine and sym-norspermidine, suggesting that the symmetrical or unsymmetrical form and carbon backbone length are not critical for polyamine function in growth. We found that the HSS enzyme evolved from the alternative spermidine biosynthetic pathway enzyme carboxyspermidine dehydrogenase. The structure of HSS is related to lysine metabolic enzymes, and HSS and carboxyspermidine dehydrogenase evolved from the aspartate family of pathways. Finally, we show that other bacterial phyla such as Cyanobacteria and some α-Proteobacteria synthesize sym-homospermidine by an HSS-independent pathway, very probably based on deoxyhypusine synthase orthologues, similar to the alternative homospermidine synthase found in some plants. Thus, bacteria can contain alternative biosynthetic pathways for both spermidine and sym-norspermidine and distinct alternative pathways for sym-homospermidine.

Original languageEnglish (US)
Pages (from-to)14711-14723
Number of pages13
JournalJournal of Biological Chemistry
Volume285
Issue number19
DOIs
StatePublished - May 7 2010

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Biosynthetic Pathways
Polyamines
Spermidine
Proteobacteria
Bacteria
Archaea
Eukaryota
Oxidoreductases
Enzymes
Growth
Rhizobium leguminosarum
Gene transfer
Horizontal Gene Transfer
Bacteriophages
sym-homospermidine
homospermidine synthetase
Cyanobacteria
Viruses
Aspartic Acid
Escherichia coli

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Molecular Biology

Cite this

Evolution and multifarious horizontal transfer of an alternative biosynthetic pathway for the alternative polyamine sym-homospermidine. / Shaw, Frances L.; Elliott, Katherine A.; Kinch, Lisa N.; Fuell, Christine; Phillips, Margaret A.; Michael, Anthony J.

In: Journal of Biological Chemistry, Vol. 285, No. 19, 07.05.2010, p. 14711-14723.

Research output: Contribution to journalArticle

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