Evolutionary dynamics of origin and loss in the deep history of phospholipase D toxin genes

Matthew H J Cordes,Greta J Binford

doi:10.1186/s12862-018-1302-2

Matthew H J Cordes, Greta J Binford

Open Access

https://doi.org/10.1186/s12862-018-1302-2

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Journal: BMC ecology	Publication Date: Dec 1, 2018
Citations: 9	License type: open-access

Affiliation: University of Arizona, Lewis & Clark College

Abstract

BackgroundVenom-expressed sphingomyelinase D/phospholipase D (SMase D/PLD) enzymes evolved from the ubiquitous glycerophosphoryl diester phosphodiesterases (GDPD). Expression of GDPD-like SMaseD/PLD toxins in both arachnids and bacteria has inspired consideration of the relative contributions of lateral gene transfer and convergent recruitment in the evolutionary history of this lineage. Previous work recognized two distinct lineages, a SicTox-like (ST-like) clade including the arachnid toxins, and an Actinobacterial-toxin like (AT-like) clade including the bacterial toxins and numerous fungal homologs.ResultsHere we expand taxon sampling by homology detection to discover new GDPD-like SMase D/PLD homologs. The ST-like clade now includes homologs in a wider variety of arthropods along with a sister group in Cnidaria; the AT-like clade now includes additional fungal phyla and proteobacterial homologs; and we report a third clade expressed in diverse aquatic metazoan taxa, a few single-celled eukaryotes, and a few aquatic proteobacteria. GDPD-like SMaseD/PLDs have an ancient presence in chelicerates within the ST-like family and ctenophores within the Aquatic family. A rooted phylogenetic tree shows that the three clades derived from a basal paraphyletic group of proteobacterial GDPD-like SMase D/PLDs, some of which are on mobile genetic elements. GDPD-like SMase D/PLDs share a signature C-terminal motif and a shortened βα1 loop, features that distinguish them from GDPDs. The three major clades also have active site loop signatures that distinguish them from GDPDs and from each other. Analysis of molecular phylogenies with respect to organismal relationships reveals a dynamic evolutionary history including both lateral gene transfer and gene duplication/loss.ConclusionsThe GDPD-like SMaseD/PLD enzymes derive from a single ancient ancestor, likely proteobacterial, and radiated into diverse organismal lineages at least in part through lateral gene transfer.

Highlights

Venom-expressed sphingomyelinase D/phospholipase D (SMase D/PLD) enzymes evolved from the ubiquitous glycerophosphoryl diester phosphodiesterases (GDPD)
The disparate phylogenetic distribution of these enzymes, coupled with their common structural motifs and lack of hydrolytic chemistry, has fueled the question of how the taxonomic distribution of PLD toxins arose. Is it a product of convergent evolution from different GDPD ancestors, or of divergent evolution accompanied by lateral gene transfer [1,2,3]? We initially argued the case for lateral gene transfer based on the evidence of the synapomorphy of the C-terminal motif shared between bacterial and spider sphingomyelinase D enzymes (SMase D) [1]
Conserved domain searches (CD) showed that all the initial protein hits belong to the same broad sequence family as the Actinobacterial-toxin like (AT-like) and ST-like family sequences, and not other domain families within the broad GDPD superfamily

Summary

Introduction

Venom-expressed sphingomyelinase D/phospholipase D (SMase D/PLD) enzymes evolved from the ubiquitous glycerophosphoryl diester phosphodiesterases (GDPD). Expression of GDPD-like SMaseD/PLD toxins in both arachnids and bacteria has inspired consideration of the relative contributions of lateral gene transfer and convergent recruitment in the evolutionary history of this lineage. As new sequence data become available, we can better assess the relative importance of convergence, including independent recruitment from widespread gene families, and lateral gene transfer (LGT) in the origin of novel phenotypes. Felicori and coworkers [2] recently expanded the known distribution of homologs to include: 11 genera in four orders of fungi; spider taxa with sequenced genomes (Araneomorph Stegodyphus & mygalomorph Acanthoscurria), two new genera of ixodine ticks, predatory mites (Metaseiulus) and dust house mites (Dermatophagiodes); two new suborders of Actinomycetales bacteria (Streptomyces, Austwickia) and a genus of proteobacteria in the order Burkholderiales (Burkholderia). A phylogenetic analysis supported two major clades, a SicTox-like (ST-like) clade that includes the arachnid toxins, and an Actinobacterial-toxin like (AT-like) clade that includes the bacterial toxins as well as fungal homologs, with the Burkholderia homolog a singleton outside of both broader groups [2]

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