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Abstract

The gain of genetic information through a non-parental relationship is termed horizontal gene transfer (HGT). While this phenomenon has been demonstrated as an important evolutionary force in prokaryotes, HGT is not broadly recognized in eukaryotes due to its rare detection. However, one exception is in the phylum Nematoda, where multiple HGT events have occurred. Groups of plant-parasitic nematodes are well known for their acquisitions of genes from bacteria which are utilized to invade plants and digest plant materials. Pristionchus nematodes, although omnivorous free-living bacterial-feeders, have also acquired cellulase genes horizontally. Eight genes containing a cellulase domain have been detected in the P. pacificus genome that strongly suggests they are under positive selection. RNA-seq data revealed these genes are expressed at all life stages. In addition, a transcriptional reporter driven by the promoter of the major component cellulase-2 shows expression in the pharyngeal gland cells. Strikingly, upon starvation an additional robust secretory system expression is also induced. These cellulases are likely secreted to the environment where robust enzymatic activity can be detected. To further investigate the ecological meaning of cellulase in P. pacificus, we generated a cellulase null mutant by knocking out all eight cellulase genes using CRISPR/Cas9. The P. pacificus cellulase mutant behaved similarly compared to the wild type when grown on the standard food source E. coli OP50. However, when grown on bacteria capable of producing biofilm, a protective structure containing cellulose, the P. pacificus cellulase mutant developed significantly slower and had a potentially smaller brood size. Thus, our study demonstrates that the horizontally acquired cellulase can increase the fitness of Pristionchus and provided new insight into this evolutionary phenomenon in eukaryotes.