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Horizontal Gene Transfer in Pristionchus

The acquisition of genes from non-parental organisms occurs through a process called ‘horizontal gene transfer’. This phenomenon is frequently observed in prokaryotes and thought to be an important driving force for evolution. For example, bacteria can acquire antibiotic resistant genes from other bacteria, thus giving them an advantage to survive in hospitable environments. In contrast, horizontal gene transfer was long thought not to be frequently found in eukaryotes. However, work over the last decade revealed that an important exception to this is observed in the phylum nematoda where horizontal gene transfer has been repeatedly demonstrated. In particular, a small group of nematodes are parasitic to plants, and the genes encoding proteins to invade and digest plants have been shown to originate from bacteria and fungi. Interestingly, with the publication of the genome of the free-living nematode Pristionchus pacificus, we have found that this nematode also has horizontally acquired genes encoding for the enzyme cellulase (Dieterich et al. 2008). In nature, cellulose is the most abundant organic material produced by plants, although Pristionchus does not feed on plants themselves. Thus, it is a mystery why the cellulase genes were acquired in Pristionchus and subsequently expanded through gene duplications. Specifically, new evidence shows that in all Pristionchus spp. cellulase genes were attained and duplicated, which suggests these genes are under positive selection during evolution. For example, in our standard lab strain P. pacificus PS312, there are 8 copies of the cellulase genes in the genome and previous studies have shown that these cellulases are enzymatically active (Mayer et al. 2011).

Using genomics, genetics and state of the art genome-editing tools such as CRISPR, we are systematically studying the function of cellulase within the Pristionchus’ ecological niche. The available toolkit makes Pristionchus a unique system to study the function and ecological significance of horizontally acquired cellulases. This might also provide important insight for related genes independently acquired in plant parasitic nematodes. Furthermore, with new genomes coming out every day, and more and more horizontal gene transfer events are being detected, we hope that using the powerful Pristionchus evolutionary system, we will provide new insights into this important evolutionary phenomenon.

Neurobiology of Pristionchus pacificus

© Ralf Sommer/MPI for Developmental Biology, Tübingen

Many nematode species are capable of displaying a vast array of surprisingly complex behaviours. In Pristionchus pacificus one of the most striking behaviours, can be observed while feeding, as P. pacificus is a highly efficient predator, able to kill and feed upon the larvae of other nematodes to supplement its bacterial diet. As these feeding behaviours are absent from the model organism Caenorhabditis elegans, we are exploiting the P. pacificus system to investigate the evolution of novel behaviours and the nervous system itself. Predatory feeding in P. pacificus is dependent upon the phenotypically plastic but fixed mouth types termed the eurystomatous and stenostomatous morphs with only eurystomatous animals capable of predatory activities. In order to successfully engage in predatory feeding, P. pacificus also demonstrates a feeding mode switch whereby pharyngeal pumping is slowed and its teeth are stimulated, characteristics which are absent during bacterial feeding. 

In order to unravel the mechanisms regulating predation, we are combining connectomic, pharmacological, genetic and molecular approaches. Thus far we have revealed fundamental differences in the pharyngeal wiring between P. pacificus and C. elegans with several neurons implicated as candidates for regulating these behavioural modifications (Bumbarger et al., 2013). Additionally, we have identified a key role for the neurotransmitter serotonin (Wilecki et al., 2015), which we are currently investigating further through CRISPR generated mutations in crucial enzymes involved in its synthesis and transport. Finally, recent data has revealed novel mechanisms influencing prey selection, with extreme levels of specificity evident. Therefore, through these comparative studies of the neural mechanisms regulating the feeding behaviours of C. elegans and P. pacificus, we will provide insights into the evolution of complex behaviours and the corresponding modifications of the nervous system that facilitates these actions. This work is continued in the laboratories of Dr. Misako Okumura and Dr. James Lightfoot.

Laborjournal Article: Mutterliebe geht durch die Nase (PDF)

 



Scientists involved:

  • Dr. James Lightfoot, Postdoc

Selected References:

Lightfoot, J. W., Wilecki, M., Roedelsperger, C., Moreno, E., Susoy, V., Witte, H. & Sommer, R.J. (2019): Small peptide mediated nematode self-recognition prevents cannibalism. Science364, 86-89.

Moreno, E., Lightfoot, L. J., Lenuzzi M., & Sommer, R. J. (2019): Cilia drive developmental plasticity and are essential for efficient prey detection in predatory nematodes, Proc. Roy. Soc. B286, 1343.

Okumura, M., Wilecki, M. & Sommer, R. J. (2017): Serotonin drives predatory feeding behavior via synchronous feeding rhytms in the nematode Pristionchus pacificus. G37, 3745-3755.

Lightfoot, J., Wilecki, M., Okumura, M. & Sommer, R. J. (2016): Assaying predatory feeding behavior in Pristionchus and other nematodes. Jove., J. Vis. Exp.115: e54404.

Wilecki, M., Lightfoot, J. W., Susoy, V. & Sommer, R. J. (2015): Predatory feeding behaviour in Pristionchus nematodes is dependent on phenotypic plasticity and induced by serotonin. Journal of Experimental Biology218, 1306–1333.

Bumbarger, D. J., Riebesell, M., Rödelsperger, C. & Sommer, R. J. (2013): System-wide rewiring underlies behavioral differences in predatory and bacterial-feeding nematodes. Cell, 152, 109-119.