Co-option of bacteriophage lysozyme genes by bivalve genomes

Abstract

Eukaryotes have occasionally acquired genetic material through horizontal gene transfer (HGT). However, little is known about the evolutionary and functional significance of such acquisitions. Lysozymes are ubiquitous enzymes that degrade bacterial cell walls. Here, we provide evidence that two subclasses of bivalves (Heterodonta and Palaeoheterodonta) acquired a lysozyme gene via HGT, building on earlier findings. Phylogenetic analyses place the bivalve lysozyme genes within the clade of bacteriophage lysozyme genes, indicating that the bivalves acquired the phage-type lysozyme genes from bacteriophages, either directly or through intermediate hosts. These bivalve lysozyme genes underwent dramatic structural changes after their co-option, including intron gain and fusion with other genes. Moreover, evidence suggests that recurrent gene duplication occurred in the bivalve lysozyme genes. Finally, we show the co-opted lysozymes exhibit a capacity for antibacterial action, potentially augmenting the immune function of related bivalves. This represents an intriguing evolutionary strategy in the eukaryote–microbe arms race, in which the genetic materials of bacteriophages are co-opted by eukaryotes, and then used by eukaryotes to combat bacteria, using a shared weapon against a common enemy.

Features of a novel protein, rusticalin, from the ascidian Styela rustica reveal ancestral horizontal gene transfer event

“…It is further confirmed by an analysis of noncoding regions of C. intestinalis rusticalin-like gene, which contained a sequence similar to the bacteriophage A500 recombination site [30]. While many cases of HGT are described based on sequence similarity alone [15, 53–59], in the case of rusticalin we also demonstrated strong evidence of the mechanism of transfer by identifying the recombination site.…”

Freshwater mussels (Unionidae) brought into captivity exhibit up-regulation of genes involved in stress and energy metabolism

“…Most studies have described no adverse effects of ciliate presence in freshwater mussels 69 , 70 . However, it is important to note that genomes of freshwater mussels are poorly understood, and these BLAST hits could be due to a paucity of comparative genomic resources and knowledge of horizontal gene transfer in bivalves 71 . Only 19% of our transcriptome received BLAST hits, leaving most assembled transcripts with no known putative function, a direct consequence of a lack of fully annotated freshwater mussel genomes.…”

Amino acid sequence associated with bacteriophage recombination site helps to reveal genes potentially acquired through horizontal gene transfer

“…Some domains associated with cysteine-rich repeats were described earlier as HGT participants. For example, phage lysozyme was found to be horizontally transferred in bivalve mollusks genome [ 57 ] and Glycoside hydrolase domain was probably inserted independently into multiple genomes: in Bacteriophages, Archaea and in three clades of Eukarya [ 44 ]. We found Peptidase M15 domain in Fungi and Metazoa ( Trichoplax adhaerens ) and Amidase_2 domain in tree lineages of Metazoa (Chordata, Molluska and Arthropoda) (Supplementary Table T 1 ).…”