Spermine and thermospermine synthases emerged multiple times during eukaryote evolution

TL;DR

This paper explores how the enzymes that produce spermine and thermospermine evolved multiple times across different eukaryotic lineages through various mechanisms.

Contribution

The study reveals the distinct evolutionary origins and mechanisms of spermine and thermospermine synthases across diverse eukaryotic groups.

Findings

Animal lineage SpmSyn was horizontally acquired from bacteria before the emergence of Choanoflagellata.

Fungal and plant SpmSyn evolved through gene duplication and neofunctionalization.

TspmSyn in plants likely originated via endosymbiotic gene transfer from cyanobacteria.

Abstract

The polyamines spermine and thermospermine are differentially distributed throughout eukaryotic phyla. It is unlikely that they were present in the Last Eukaryotic Common Ancestor, thus their biosynthetic enzymes, spermine synthase (SpmSyn) and thermospermine synthase (TspmSyn) emerged during eukaryotic evolution. Herein, we show the different evolutionary mechanisms by which functionally validated SpmSyns and TspmSyns evolved, and their phylogenetic distribution in eukaryotes. Animal lineage SpmSyn was horizontally acquired as a bacterial S-adenosylmethionine decarboxylase-SpmSyn fusion protein before the emergence of the single-celled closest relatives of animals, the Choanoflagellata. SpmSyn has been lost from comb jellies, some sponge species, and was lost from most free-living and parasitic worms. Corals encode two SpmSyn homologs, one of which has evolved into a TspmSyn. In fungi, SpmSyn evolved by gene duplication of spermidine synthase and subsequent neofunctionalization early in the budding yeast Saccharomycotina subphylum. Similarly, the plant SpmSyn evolved by gene duplication of spermidine synthase and then neofunctionalization in lycophytes, coincident with the emergence of vascularization. TspmSyn is found throughout plants and green algae, but lost from wild and domesticated barley. It was likely acquired by endosymbiotic gene transfer from the cyanobacterial ancestor of the chloroplast, although the closest homolog of plant TspmSyn is from the Chloroflexota. TspmSyn homologs evolved into SpmSyns in red algae and into spermidine synthase in glaucophyte algae. Chloroflexota-type TspmSyns are found in many protist phyla, often correlated with secondary endosymbiosis of red or green algae, but were acquired by horizontal gene transfer in phyla that have not possessed algal plastids.

Figures