Cilia drive developmental plasticity and are essential for efficient prey detection in predatory nematodes

Abstract

Cilia are complex organelles involved in a broad array of functions in eukaryotic organisms. Nematodes employ cilia for environmental sensing, which shapes developmental decisions and influences morphologically plastic traits and adaptive behaviours. Here, we assess the role of cilia in the nematode Pristionchus pacificus, and determine their importance in regulating the developmentally plastic mouth-form decision in addition to predatory feeding and self-recognition behaviours, all of which are not present in Caenorhabditis elegans . An analysis of a multitude of cilia-related mutants including representatives of the six protein subcomplexes required in intraflagellar transport (IFT) plus the regulatory factor X transcription factor daf-19 revealed that cilia are essential for processing the external cues influencing the mouth-form decision and for the efficient detection of prey. Surprisingly, we observed that loss-of-function mutations in the different IFT components resulted in contrasting mouth-form phenotypes and different degrees of predation deficiencies. This observation supports the idea that perturbing different IFT subcomplexes has different effects on signalling downstream of the cilium. Finally, self-recognition was maintained in the cilia deficient mutants tested, indicating that the mechanisms triggering self-recognition in P. pacificus may not require the presence of fully functional cilia.

Improving Transgenesis Efficiency and CRISPR-Associated Tools Through Codon Optimization and Native Intron Addition in Pristionchus Nematodes

“…The presence of teeth in P. pacificus facilitates an additional behavior as they are capable of predating the larvae of other nematodes. Here, it has been observed that the mouth-form dimorphism strongly correlates with the predation behavior, as only the morphs possessing two teeth are active predators, whereas the single-toothed morphs are strict bacterial feeders ( Wilecki et al 2015 ; Moreno et al 2019 ; Akduman et al 2020 ). Furthermore, the predatory behavior coincides with the existence of a self-recognition system ( Lightfoot et al 2019 ) and environmental responses distinct from C. elegans ( Hong and Sommer 2006 ; Moreno et al 2016 , 2017 ).…”

Linking Molecular Mechanisms and Evolutionary Consequences of Resource Polyphenism

“…Kin discrimination in this system largely depends on the identity of a hypervariable small peptide that is expressed in the nematodes’ body-wall epidermis (Lightfoot et al, 2019 ) and, otherwise, on overall genetic relatedness (Lightfoot et al, 2021 ). Although the cilia of anterior sensilla are required for prey assessment and environmental sensing in P. pacificus , self-recognition does not seem to require fully functioning cilia (Moreno et al, 2019 ), so it is not yet known how the peptide signal and genetic identity of others is detected.…”

Efficient visual screening of CRISPR/Cas9 genome editing in the nematode Pristionchus pacificus

“…Similar to C. elegans, the reproductive system of P. pacificus is hermaphroditic, and its genome has been sequenced (Dieterich et al, 2008), allowing CRISPR/Cas9 genome editing (Witte et al, 2015). Using this system, many mutants have been generated and analyzed to understand the molecular mechanisms of various phenomena, such as phenotypic plasticity (Moreno et al, 2019;Namdeo et al, 2018;Ragsdale & Ivers, 2016;Serobyan et al, 2016;Sieriebriennikov et al, 2017Sieriebriennikov et al, , 2018Sieriebriennikov et al, , 2020, feeding behaviors (Ishita et al, 2021;Okumura et al, 2017), self-recognition (Lightfoot et al, 2019), dauer development (Markov et al, 2016), and sensory systems (Carstensen et al, 2021;Moreno et al, 2017Moreno et al, , 2018Moreno et al, , 2019. Using CRISPR/Cas9 genome editing, the molecular mechanisms of these interesting characteristics of P. pacificus have been revealed to promote our understanding of developmental biology, neurobiology, and evolution.…”