The burrowing behavior of the nematode Caenorhabditis elegans: a new assay for the study of neuromuscular disorders

Abstract

The nematode Caenorhabditis elegans has been a powerful model system for the study of key muscle genes relevant to human neuromuscular function and disorders. The behavioral robustness of C. elegans, however, has hindered its use in the study of certain neuromuscular disorders because many worm models of human disease show only subtle phenotypes while crawling. By contrast, in their natural habitat, C. elegans likely spends much of the time burrowing through the soil matrix. We developed a burrowing assay to challenge motor output by placing worms in agar-filled pipettes of increasing densities. We find that burrowing involves distinct kinematics and turning strategies from crawling that vary with the properties of the substrate. We show that mutants mimicking Duchenne muscular dystrophy by lacking a functional ortholog of the dystrophin protein, DYS-1, crawl normally but are severely impaired in burrowing. Muscular degeneration in the dys-1 mutant is hastened and exacerbated by burrowing, while wild-type shows no such damage. To test whether neuromuscular integrity might be compensated genetically in the dys-1 mutant, we performed a genetic screen and isolated several suppressor mutants with proficient burrowing in a dys-1 mutant background. Further study of burrowing in C. elegans will enhance the study of diseases affecting neuromuscular integrity, and will provide insights into the natural behavior of this and other nematodes.

Ichnological evidence for meiofaunal bilaterians from the terminal Ediacaran and earliest Cambrian of Brazil

“…Organisms without body appendages possessing only longitudinal muscles, such as nematodes 46 , are restricted to sinusoidal locomotion as they lack the antagonistic circular muscles necessary for peristalsis. Nematodes are common bioturbators of modern muddy sediments and can create open mucuslined burrows of a size range comparable to that of the Brazilian M. minima (Fig.…”

Caenorhabditis elegans locomotion is affected by internalized paramagnetic nanoparticles in the presence of magnetic field

“…5E, 5F). More body bends possibly indicate a more W-shaped locomotion, which has been described previously in burrowing worms, as opposed to the Sshaped crawling or C-shaped swimming motion (63). Since burrowing requires the effort to move in a viscous medium, one could assume that Group 100 animals crawling in MF have to apply effort to push also their way forward, thus they integrate more bends to their locomotion.…”

Analysis of the NK2 homeobox gene ceh-24 reveals sublateral motor neuron control of left-right turning during sleep

“…Recent work is starting to establish assays for the study of such types of locomotion. One example is burrowing, with a downward tendency, using magnetic cues for orientation (Beron et al, 2015; Vidal-Gadea et al, 2015). Another is nictation, a dispersal behavior, in which dauer larvae stand on their tails displaying undulating body movements trying to attach to a larger animal in order to get dispersed and potentially reach new food sources (Lee et al, 2012).…”

“…Simple dorsal and ventral contractions can hardly explain three-dimensional movements, which would require additional left-right body movements and thus a more complex regulation of musculature though a separate innervation of each muscle quadrant. C. elegans shows a number of additional types of movements that appear to be more complex than locomotion on a plane surface such as burrowing into substrates, nictation, which is a dispersal behavior during which worms assume an upright posture, and turning from their left to their right side (Lee et al, 2012; Beron et al, 2015; Vidal-Gadea et al, 2015). Left-right turning, or flipping, occurs mostly during lethargus.…”