Teething during sleep: Ultrastructural analysis of pharyngeal muscle and cuticular grinder during the molt in Caenorhabditis elegans.

Complex extracellular structures exist throughout phylogeny, but the dynamics of their formation and dissolution are often opaque. One example is the pharyngeal grinder of the nematode Caenorhabditis elegans, an extracellular structure that ruptures bacteria during feeding. During each larval transi...

Full description

Bibliographic Details
Main Authors: Alessandro P Sparacio, Nicholas F Trojanowski, Karen Snetselaar, Matthew D Nelson, David M Raizen
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0233059
_version_ 1819111503426486272
author Alessandro P Sparacio
Nicholas F Trojanowski
Karen Snetselaar
Matthew D Nelson
David M Raizen
author_facet Alessandro P Sparacio
Nicholas F Trojanowski
Karen Snetselaar
Matthew D Nelson
David M Raizen
author_sort Alessandro P Sparacio
collection DOAJ
description Complex extracellular structures exist throughout phylogeny, but the dynamics of their formation and dissolution are often opaque. One example is the pharyngeal grinder of the nematode Caenorhabditis elegans, an extracellular structure that ruptures bacteria during feeding. During each larval transition stage, called lethargus, the grinder is replaced with one of a larger size. Here, we characterize at the ultrastructural level the deconstruction of the larval grinder and the construction of the adult grinder during the fourth larval stage (L4)-to-adult transition. Early in L4 lethargus, pharyngeal muscle cells trans-differentiate from contractile to secretory cells, as evidenced by the appearance of clear and dense core vesicles and disruptions in sarcomere organization. This is followed, within minutes, by the dissolution of the L4 grinder and the formation and maturation of the adult grinder. Components of the nascent adult grinder are deposited basally, and are separated from the dissolving larval grinder by a visible apical layer. The complete grinder is a lamellated extracellular matrix comprised of five layers. Following grinder formation, pharyngeal muscle cells regain ultrastructural contractile properties, and muscle contractions resume. Our findings add to our understanding of how complex extracellular structures assemble and dissemble.
first_indexed 2024-12-22T03:58:39Z
format Article
id doaj.art-4bf508c64d5c41818c7a5ddbdfcd3b49
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-22T03:58:39Z
publishDate 2020-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-4bf508c64d5c41818c7a5ddbdfcd3b492022-12-21T18:39:48ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01155e023305910.1371/journal.pone.0233059Teething during sleep: Ultrastructural analysis of pharyngeal muscle and cuticular grinder during the molt in Caenorhabditis elegans.Alessandro P SparacioNicholas F TrojanowskiKaren SnetselaarMatthew D NelsonDavid M RaizenComplex extracellular structures exist throughout phylogeny, but the dynamics of their formation and dissolution are often opaque. One example is the pharyngeal grinder of the nematode Caenorhabditis elegans, an extracellular structure that ruptures bacteria during feeding. During each larval transition stage, called lethargus, the grinder is replaced with one of a larger size. Here, we characterize at the ultrastructural level the deconstruction of the larval grinder and the construction of the adult grinder during the fourth larval stage (L4)-to-adult transition. Early in L4 lethargus, pharyngeal muscle cells trans-differentiate from contractile to secretory cells, as evidenced by the appearance of clear and dense core vesicles and disruptions in sarcomere organization. This is followed, within minutes, by the dissolution of the L4 grinder and the formation and maturation of the adult grinder. Components of the nascent adult grinder are deposited basally, and are separated from the dissolving larval grinder by a visible apical layer. The complete grinder is a lamellated extracellular matrix comprised of five layers. Following grinder formation, pharyngeal muscle cells regain ultrastructural contractile properties, and muscle contractions resume. Our findings add to our understanding of how complex extracellular structures assemble and dissemble.https://doi.org/10.1371/journal.pone.0233059
spellingShingle Alessandro P Sparacio
Nicholas F Trojanowski
Karen Snetselaar
Matthew D Nelson
David M Raizen
Teething during sleep: Ultrastructural analysis of pharyngeal muscle and cuticular grinder during the molt in Caenorhabditis elegans.
PLoS ONE
title Teething during sleep: Ultrastructural analysis of pharyngeal muscle and cuticular grinder during the molt in Caenorhabditis elegans.
title_full Teething during sleep: Ultrastructural analysis of pharyngeal muscle and cuticular grinder during the molt in Caenorhabditis elegans.
title_fullStr Teething during sleep: Ultrastructural analysis of pharyngeal muscle and cuticular grinder during the molt in Caenorhabditis elegans.
title_full_unstemmed Teething during sleep: Ultrastructural analysis of pharyngeal muscle and cuticular grinder during the molt in Caenorhabditis elegans.
title_short Teething during sleep: Ultrastructural analysis of pharyngeal muscle and cuticular grinder during the molt in Caenorhabditis elegans.
title_sort teething during sleep ultrastructural analysis of pharyngeal muscle and cuticular grinder during the molt in caenorhabditis elegans
url https://doi.org/10.1371/journal.pone.0233059
work_keys_str_mv AT alessandropsparacio teethingduringsleepultrastructuralanalysisofpharyngealmuscleandcuticulargrinderduringthemoltincaenorhabditiselegans
AT nicholasftrojanowski teethingduringsleepultrastructuralanalysisofpharyngealmuscleandcuticulargrinderduringthemoltincaenorhabditiselegans
AT karensnetselaar teethingduringsleepultrastructuralanalysisofpharyngealmuscleandcuticulargrinderduringthemoltincaenorhabditiselegans
AT matthewdnelson teethingduringsleepultrastructuralanalysisofpharyngealmuscleandcuticulargrinderduringthemoltincaenorhabditiselegans
AT davidmraizen teethingduringsleepultrastructuralanalysisofpharyngealmuscleandcuticulargrinderduringthemoltincaenorhabditiselegans