Worm bagging

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Worm bagging (also referred to as facultative vivipary or endotokia matricida) is a form of vivipary observed in nematodes, namely Caenorhabditis elegans . The process is characterized by eggs hatching within the parent and the larvae proceeding to consume and emerge from the parent. [1]

Contents

History

While the phenomenon was mentioned as a result of fluorodeoxyuridine treatment as early as 1979 [2] and egg-laying mutants were identified in 1984, [1] the natural circumstances and mechanisms resulting in this behavior were not fully explored until 2003. [3] [4] From this point, modest explorations of the mechanisms underlying this behavior have been observed.

Proximate causes

Bagging will occur in vulvaless [5] or egg-laying mutants [6] of C. elegans but can also be induced in wild-type strains. [4] Identified stressors that can induce bagging are starvation, high salt concentration, and antagonistic bacteria. [4]

It has been observed in larval development, that the WRT-5 protein is secreted into the pharyngeal lumen and the pharyngeal expression changes in a cycle that is connected to the molting cycle. Deletion mutations in wrt-5 cause embryonic lethality, which are temperature sensitive and more severe at 15 degrees C than at 25 degrees C. Additionally, Animals that hatch exhibit variable abnormal morphology, for example, bagging worms, blistering, molting defects, or Roller phenotypes. [7]

Internal hatching is initiated by genes and is not restricted to the widely used laboratory strain N2. Internal hatching is rare when worms are maintained under standard laboratory conditions. However, axenic condition which is a transfer from solid to liquid medium along with adverse environmental conditions, such as starvation, exposure to harsh compounds, and bacteria can increase the frequency of worm bags. [8]

In a study C. elegans were starved and in stressful conditions such as a high salt environment. As a result there was a connection drawn between the pathway leading to the dauer stage and the pathway leading to bagging. Bagging was seen to be induced under stress, and was reversible if worms were relieved of the stress before internal larvae caused too much damage to the adult. Also, there was evidence of larvae developing in the adult and consuming parent body contents prior to emerging from the parent body. [9]

Ultimate causes

Larvae of internal hatching could have gonad damage, which reduces fitness of those individuals. Internally hatched larvae also survived equally as well or even better than externally hatched worms. This means that worm bagging does not negatively influence the size or survival of the offspring. [8] The destruction of the mother provides nutrients to the offspring, which is an efficient transfer of nutrients. [9] [10] In environments that lead to the starvation of individuals, worm bagging is beneficial because it improves the chances of offspring survival and the passing of their genes. If worm bagging does not occur in these environments, offspring will have an increased chance of starvation and removing their genes from the gene pool.

Other Species

Aside from C. elegans, Bagging is known to occur in other nematode species including: Haemonchus contortus, Mehdinema allii, and Metacrobeles amblyurus. [2] This phenomenon may be conserved among these species because it is a “life-history trait”. [4] Offspring survivability is enhanced through bagging in a stressful environment as the young are physically protected through development to the larval stage and nourished through consumption of the parent body. [4]

Future Research

While egg-laying mutants have been characterized, [6] the natural processes that result in facultative vivipary have not been fully explored. Aging-related degeneration of the egg-laying system has been implicated in egg retention [8] but the mechanism by which starvation signals result in this process has not been described. Experiments demonstrating time-dependent up/downregulation of genes (in nervous and vulval cells) throughout the span of the process would provide insight into the proximate causes. This research may provide insight into the mechanisms involved in the induction of egg-laying and may also improve understanding of birthing signals in higher organisms.

Related Research Articles

<i>Caenorhabditis elegans</i> Free-living species of nematode

Caenorhabditis elegans is a free-living transparent nematode about 1 mm in length that lives in temperate soil environments. It is the type species of its genus. The name is a blend of the Greek caeno- (recent), rhabditis (rod-like) and Latin elegans (elegant). In 1900, Maupas initially named it Rhabditides elegans. Osche placed it in the subgenus Caenorhabditis in 1952, and in 1955, Dougherty raised Caenorhabditis to the status of genus.

<span class="mw-page-title-main">H. Robert Horvitz</span> American biologist

Howard Robert Horvitz ForMemRS NAS AAA&S APS NAM is an American biologist best known for his research on the nematode worm Caenorhabditis elegans, for which he was awarded the 2002 Nobel Prize in Physiology or Medicine, together with Sydney Brenner and John E. Sulston, whose "seminal discoveries concerning the genetic regulation of organ development and programmed cell death" were "important for medical research and have shed new light on the pathogenesis of many diseases".

<span class="mw-page-title-main">John Sulston</span> British biologist and academic (1942–2018)

Sir John Edward Sulston was a British biologist and academic who won the Nobel Prize in Physiology or Medicine for his work on the cell lineage and genome of the worm Caenorhabditis elegans in 2002 with his colleagues Sydney Brenner and Robert Horvitz at the MRC Laboratory of Molecular Biology. He was a leader in human genome research and Chair of the Institute for Science, Ethics and Innovation at the University of Manchester. Sulston was in favour of science in the public interest, such as free public access of scientific information and against the patenting of genes and the privatisation of genetic technologies.

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WormBook is an open access, comprehensive collection of original, peer-reviewed chapters covering topics related to the biology of the nematode worm Caenorhabditis elegans . WormBook also includes WormMethods, an up-to-date collection of methods and protocols for C. elegans researchers.

Caenorhabditis briggsae is a small nematode, closely related to Caenorhabditis elegans. The differences between the two species are subtle. The male tail in C. briggsae has a slightly different morphology from C. elegans. Other differences include changes in vulval precursor competence and the placement of the excretory duct opening. C. briggsae is frequently used to study the differences between it and the more intimately understood C. elegans, especially at the DNA and protein sequence level. Several mutant strains of C. briggsae have also been isolated that facilitate genetic analysis of this organism. C. briggsae, like C. elegans, is a hermaphrodite. The genome sequence for C. briggsae was determined in 2003.

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<span class="mw-page-title-main">Animal testing on invertebrates</span> Overview article

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<span class="mw-page-title-main">Cornelia Bargmann</span> American neurobiologist

Cornelia Isabella "Cori" Bargmann is an American neurobiologist. She is known for her work on the genetic and neural circuit mechanisms of behavior using C. elegans, particularly the mechanisms of olfaction in the worm. She has been elected to the National Academy of Sciences and had been a Howard Hughes Medical Institute investigator at UCSF and then Rockefeller University from 1995 to 2016. She was the Head of Science at the Chan Zuckerberg Initiative from 2016 to 2022. In 2012 she was awarded the $1 million Kavli Prize, and in 2013 the $3 million Breakthrough Prize in Life Sciences.

<span class="mw-page-title-main">Nematode</span> Phylum of worms with tubular digestive systems with openings at both ends

The nematodes, roundworms or eelworms constitute the phylum Nematoda. They are a diverse animal phylum inhabiting a broad range of environments. Most species are free-living, feeding on microorganisms, but there are many that are parasitic. The parasitic worms (helminths) are the cause of soil-transmitted helminthiases.

The nematode worm Caenorhabditis elegans was first studied in the laboratory by Victor Nigon and Ellsworth Dougherty in the 1940s, but came to prominence after being adopted by Sydney Brenner in 1963 as a model organism for the study of developmental biology using genetics. In 1974, Brenner published the results of his first genetic screen, which isolated hundreds of mutants with morphological and functional phenotypes, such as being uncoordinated. In the 1980s, John Sulston and co-workers identified the lineage of all 959 cells in the adult hermaphrodite, the first genes were cloned, and the physical map began to be constructed. In 1998, the worm became the first multi-cellular organism to have its genome sequenced. Notable research using C. elegans includes the discoveries of caspases, RNA interference, and microRNAs. Six scientists have won the Nobel prize for their work on C. elegans.

<span class="mw-page-title-main">Daf-16</span> Ortholog

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mir-48 microRNA is a microRNA which is found in nematodes, in which it controls developmental timing. It acts in the heterochronic pathway, where it controls the timing of cell fate decisions in the vulva and hypodermis during larval development.

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<span class="mw-page-title-main">Cell lineage</span> Developmental history of a tissue or organ

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References

  1. 1 2 Trent, C; Tsuing, N; Horvitz, HR (1983). "Egg-laying defective mutants of the nematode Caenorhabditis elegans". Genetics. 104 (4): 619–647. doi:10.1093/genetics/104.4.619. PMC   1202130 . PMID   11813735.
  2. 1 2 Mitchell, DH; Stiles, JW; Santelli, J; Sanadi, DR (1979). "Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine". Journal of Gerontology. 34 (1): 28–36. doi:10.1093/geronj/34.1.28. PMID   153363.
  3. ↑ Caswell-Chen, Edward; Chen, Jianjun (1 June 2003). "Why Caenorhabditis elegans adults sacrifice their bodies to progeny". Nematology. 5 (4): 641–645. doi:10.1163/156854103322683355.
  4. 1 2 3 4 5 Chen J, Caswell-Chen EP. Facultative Vivipary is a Life-History Trait in Caenorhabditis elegans. Journal of Nematology. 2004;36(2):107–113.
  5. ↑ Horvitz, H. R.; Sulston, J. E. (1980). "Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans". Genetics. 96 (2): 435–454. doi:10.1093/genetics/96.2.435. PMC   1214309 . PMID   7262539.
  6. 1 2 Trent, C.; Tsuing, N.; Horvitz, H. R. (1983). "Egg-laying defective mutants of the nematode Caenorhabditis elegans". Genetics. 104 (4): 619–647. doi:10.1093/genetics/104.4.619. PMC   1202130 . PMID   11813735.
  7. ↑ Hao, Limin; Aspöck, Gudrun; Bürglin, Thomas R. (February 2006). "The hedgehog-related gene wrt-5 is essential for hypodermal development in Caenorhabditis elegans". Developmental Biology. 290 (2): 323–336. doi:10.1016/j.ydbio.2005.11.028. PMID   16413526.
  8. 1 2 3 Mosser, Thomas; Matic, Ivan; Leroy, Magali (15 November 2011). "Bacterium-Induced Internal Egg Hatching Frequency Is Predictive of Life Span in Caenorhabditis elegans Populations". Applied and Environmental Microbiology. 77 (22): 8189–8192. Bibcode:2011ApEnM..77.8189M. doi:10.1128/AEM.06357-11. PMC   3208991 . PMID   21926203.
  9. 1 2 Jianjun Chen et al. (2003) International Worm Meeting “Bagging as a part of the C. elegans life cycle.” (paper) - WormBase : Nematode Information Resource. (n.d.).
  10. ↑ Pickett, Christopher L.; Kornfeld, Kerry (August 2013). "Age-related degeneration of the egg-laying system promotes matricidal hatching in Caenorhabditis elegans". Aging Cell. 12 (4): 544–553. doi:10.1111/acel.12079. PMC   4020343 . PMID   23551912.
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