Host microbe interactions in Caenorhabditis elegans

Last updated
Electron micrograph of Caenorhabditis elegans Electron micrograph of ''Caenorhabditis elegans''.jpg
Electron micrograph of Caenorhabditis elegans

Caenorhabditis elegans - microbe interactions are defined as any interaction that encompasses the association with microbes that temporarily or permanently live in or on the nematode C. elegans. The microbes can engage in a commensal, mutualistic or pathogenic interaction with the host. These include bacterial, viral, unicellular eukaryotic, and fungal interactions. In nature C. elegans harbours a diverse set of microbes. [1] In contrast, C. elegans strains that are cultivated in laboratories for research purposes have lost the natural associated microbial communities and are commonly maintained on a single bacterial strain, Escherichia coli OP50. However, E. coli OP50 does not allow for reverse genetic screens because RNAi libraries have only been generated in strain HT115. This limits the ability to study bacterial effects on host phenotypes. [2] The host microbe interactions of C. elegans are closely studied because of their orthologs in humans. [2] Therefore, the better we understand the host interactions of C. elegans the better we can understand the host interactions within the human body.

Contents

Natural ecology

Imbalance between our knowledge of C. elegans biology gained by laboratory discoveries versus C. elegans natural ecology Imbalance.jpg
Imbalance between our knowledge of C. elegans biology gained by laboratory discoveries versus C. elegans natural ecology

C. elegans is a well-established model organism in different research fields, yet its ecology however is only poorly understood. They have a short development cycle only lasting three days with a total life span of about two weeks. [2] C. elegans were previously considered a soil-living nematode, [3] [4] [5] but in the last 10 years it was shown that natural habitats of C. elegans are microbe-rich, such as compost heaps, rotten plant material, and rotten fruits. [3] [6] [7] [8] [9] Most of the studies on C. elegans are based on the N2 strain, which has adapted to laboratory conditions. [10] [11] [12] Only in the last few years the natural ecology of C. elegans has been studied in more detail [13] and one current research focus is its interaction with microbes. [14] As C. elegans feeds on bacteria (microbivory), the intestine of worms isolated from the wild is usually filled with a large number of bacteria. [9] [15] [16] In contrast to the very high diversity of bacteria in the natural habitat of C. elegans, the lab strains are only fed with one bacterial strain, the Escherichia coli derivate OP50 . [17] OP50 was not co-isolated with C. elegans from nature, but was rather used because of its high convenience for laboratory maintenance. [18] Bleaching is a common method in the laboratory to clean C. elegans of contaminations and to synchronize a population of worms. [19] During bleaching the worms are treated with 5N NaOH and household bleach, leading to the death of all worms and survival of only the nematode eggs. [19] The larvae hatching from these eggs lack any microbes, as none of the currently known C. elegans-associated microbes can be transferred vertically. Since most laboratory strains are kept under these gnotobiotic conditions, nothing is known about the composition of the C. elegans microbiota. [20] The ecology of C. elegans can only be fully understood in the light of the multiple interactions with the microorganisms, which it encounters in the wild. The effect of microbes on C. elegans can vary from beneficial to lethal.

Beneficial microbes

In its natural habitat C. elegans is constantly confronted with a variety of bacteria that could have both negative and positive effects on its fitness. To date, most research on C. elegans-microbe interactions focused on interactions with pathogens. Only recently, some studies addressed the role of commensal and mutualistic bacteria on C. elegans fitness. In these studies, C. elegans was exposed to various soil bacteria, either isolated in a different context or from C. elegans lab strains transferred to soil. [21] [22] These bacteria can affect C. elegans either directly through specific metabolites, or they can cause a change in the environmental conditions and thus induce a physiological response in the host. [21] Beneficial bacteria can have a positive effect on the lifespan, generate certain pathogen resistances, or influence the development of C. elegans.

Lifespan extension

Pseudomonas Pseudomonas.jpg
Pseudomonas

The lifespan of C. elegans is prolonged when grown on plates with Pseudomonas sp. or Bacillus megaterium compared to individuals living on E.coli. [21] The lifespan extension mediated by B. megaterium is greater than that caused by Pseudomonas sp.. As determined by microarray analysis (a method, which allows the identification of C. elegans genes that are differentially expressed in response to different bacteria), 14 immune defence genes were up-regulated when C. elegans was grown on B. megaterium, while only two were up-regulated when fed with Pseudomonas sp. In addition to immune defence genes, other upregulated genes are involved in the synthesis of collagen and other cuticle components, indicating that the cuticle might play an important role in the interaction with microbes. Although some of the genes are known to be important for C. elegans lifespan extension, the precise underlying mechanisms still remain unclear. [21]

Protection against microbes

The microbial communities residing inside the host body have now been recognized to be important for effective immune responses. [22] Yet the molecular mechanisms underlying this protection are largely unknown. Bacteria can help the host to fight against pathogens either by directly stimulating the immune response or by competing with the pathogenic bacteria for available resources. [23] [24] In C. elegans, some associated bacteria seem to generate protection against pathogens. For example, when C. elegans is grown on Bacillus megaterium or Pseudomonas mendocina , worms are more resistant to infection with the pathogenic bacterium Pseudomonas aeruginosa [21], which is a common bacterium in C. elegans’ natural environment and therefore a potential natural pathogen. [25] This protection is characterized by prolonged survival on P. aeruginosa in combination with a delayed colonization of C. elegans by the pathogen. Due to its comparatively large size B. megaterium is not an optimal food source for C. elegans, [26] resulting in a delayed development and a reduced reproductive rate. The ability of B. megaterium to enhance resistance against the infection with P. aeruginosa seems to be linked to the decrease in reproductive rate. However, the protection against P. aeruginosa infection provided by P. mendocina is reproduction independent, and depends on the p38 mitogen-activated protein kinase pathway. P. mendocina is able to activate the p38 MAPK pathway and thus to stimulate the immune response of C. elegans against the pathogen. [22] A common way for an organism to protect itself against microbes is to increase fecundation to increase the surviving individuals in the face of an attack. This defense against parasites are genetically linked to stress response pathways and dependent on the innate immune system. [27]

Effects on development

Caenorhabditis elegans late embryonic development

Under natural conditions it might be advantageous for C. elegans to develop as fast as possible to be able to reproduce rapidly. The bacterium Comamonas DA1877 accelerates the development of C. elegans. [28] Neither TOR (target of rapamycin), nor insulin signalling seem to mediate this effect on the accelerated development. It is thus possible that secreted metabolites of Comamonas, which might be sensed by C. elegans, lead to faster development. Worms that were fed with Comamonas DA1877 also showed a reduced number of offspring and a reduced lifespan. [28] [29] Another microbe that accelerates C. elegans' growth are L . sphaericus. This bacteria significantly increased the growth rate of C. elegans when compared to their normal diet of E. coli OP50. [30] C. elegans are mostly grown and observed in a controlled laboratory with a controlled diet, therefore, they may show differential growth rates with naturally occurring microbes.

Pathogenic microbes

In its natural environment C. elegans is confronted with a variety of different potential pathogens. C. elegans has been used intensively as a model organism for studying host-pathogen interactions and the immune system. [5] [31] These studies revealed that C. elegans has well-functioning innate immune defenses. The first line of defense is the extremely tough cuticle that provides an external barrier against pathogen invasion. [32] In addition, several conserved signaling pathways contribute to defense, including the DAF-2/DAF-16 insulin-like receptor pathway and several MAP kinase pathways, which activate physiological immune responses. [33] Finally, pathogen avoidance behavior represents another line of C. elegans immune defense. [34] All these defense mechanisms do not work independently, but jointly to ensure an optimal defense response against pathogens. [31] Many microorganisms were found to be pathogenic for C. elegans under laboratory conditions. To identify potential C. elegans pathogens, worms in the L4 larval stage are transferred to a medium that contains the organism of interest, which is a bacterium in most cases. Pathogenicity of the organism can be inferred by measuring the lifespan of worms. There are several known human pathogens that have a negative effect on C. elegans survival. Pathogenic bacteria can also form biofilms, whose sticky exopolymer matrix could impede C. elegans motility [35] and cloaks bacterial quorum sensing chemoattractants from predator detection. [36] Biofilms can secrete iron siderophores which can be detected by C.elegans [37] . However, only very few natural C. elegans pathogens are currently known. [5]

Eukaryotic microbes

One of the best studied natural pathogens of C. elegans is the microsporidium Nematocida parisii , which was directly isolated from wild-caught C. elegans. N. parisii is an intracellular parasite that is exclusively transmitted horizontally from one animal to another. The microsporidian spores are likely to exit the cells by disrupting a conserved cytoskeletal structure in the intestine called the terminal web. It seems that none of the known immune pathways of C. elegans is involved in mediating resistance against N. parisii. Microsporidia were found in several nematodes isolated from different locations, indicating that microsporidia are common natural parasites of C. elegans. The N. parisii-C. elegans system represents a very useful tool to study infection mechanisms of intracellular parasites. [5] Additionally, a new species of microsporidia was recently found in a wild caught C. elegans that genome sequencing places in the same genus Nematocida as prior microsporidia seen in these nematodes. This new species was named Nematocida displodere, after a phenotype seen in late infected worms that explode at the vulva to release infectious spores. N. displodere was shown to infect a broad range of tissues and cell types in C. elegans, including the epidermis, muscle, neurons, intestine, seam cells, and coelomocytes. Strangely, the majority of intestinal infection fails to grow to later parasite stages, while the muscle and epidermal infection thrives. [38] This is in stark contrast to N. parisii which infects and completes its entire life cycle in the C. elegans intestine. These related Nematocida species are being used to study the host and pathogen mechanisms responsible for allowing or blocking eukaryotic parasite growth in different tissue niches. Another eukaryotic pathogen is the fungus Drechmeria coniospora, which has not been directly co-isolated with C. elegans from nature, but is still considered to be a natural pathogen of C. elegans. D. coniospora attaches to the cuticle of the worm at the vulva, mouth, and anus and its hyphae penetrate the cuticle. In this way D. coniospora infects the worm from the outside, while the majority of bacterial pathogens infect the worm from the intestinal lumen. [39] [40]

Viral pathogens

In 2011 the first naturally associated virus was isolated from C. elegans found outside of a laboratory. The Orsay virus is an RNA virus that is closely related to nodaviruses. The virus is not stably integrated into the host genome. It is transmitted horizontally under laboratory conditions. An antiviral RNAi pathway is essential for C. elegans resistance against Orsay virus infection. [41] To date there has not been a virus, other intracellular pathogens, or multicellular parasite that have been able to affect the nematode. Because of this we cannot use C. elegans as an experimental system for these interactions. In 2005, two reports have shown that vesicular stomatitis virus (VSV), an arbovirus with a many invertebrate and vertebrate host range, could replicate in primary cells derived from C. elegans embryos. [42]

Bacterial pathogens

Caenorhabditis elegans intestine infected with Bacillus thuringiensis ''Caenorhabditis elegans'' intestine infected with ''Bacillus thuringiensis''.jpg
Caenorhabditis elegans intestine infected with Bacillus thuringiensis

Two bacterial strains of the genus Leucobacter were co-isolated from nature with the two Caenorhabditis species C. briggsae and C. n. spp 11, and named Verde 1 and Verde 2. These two Leucobacter strains showed contrasting pathogenic effects in C. elegans. Worms that were infected with Verde 2 produced a deformed anal region (“Dar” phenotype), while infections with Verde 1 resulted in slower growth due to coating of the cuticle with the bacterial strain. In liquid culture Verde 1 infected worms stuck together with their tails and formed so called “worm stars”. The trapped worms cannot free themselves and eventually die. After death C. elegans is then used as a food source for the bacteria. Only larvae in the L4 stage seem to be able to escape by autotomy. They split their bodies into half, so that the anterior half can escape. The “half-worms” remain viable for several days. [43] The Gram-positive bacterium Bacillus thuringiensis is likely associated with C. elegans in nature. B. thuringiensis is a soil bacterium that is often used in infection experiments with C. elegans. [44] [45] It produces spore-forming toxins, called crystal (Cry) toxins, which are associated with spores. These are jointly taken up by C. elegans orally. Inside the host, the toxins bind to the surface of intestinal cells, where the formation of pores in intestinal cells is induced, causing their destruction. The resulting change in milieu in the gut leads to germination of the spores, which subsequently proliferate in the worm body. [46] [47] [48] An aspect of the C. elegans–B. thuringiensis system is the high variability in pathogenicity between different strains. [45] [48] There are highly pathogenic strains, but also strains that are less or even non-pathogenic. [45] [48]

See also

Related Research Articles

<i>Bacillus thuringiensis</i> Species of bacteria used as an insecticide

Bacillus thuringiensis is a gram-positive, soil-dwelling bacterium, the most commonly used biological pesticide worldwide. B. thuringiensis also occurs naturally in the gut of caterpillars of various types of moths and butterflies, as well on leaf surfaces, aquatic environments, animal feces, insect-rich environments, and flour mills and grain-storage facilities. It has also been observed to parasitize other moths such as Cadra calidella—in laboratory experiments working with C. calidella, many of the moths were diseased due to this parasite.

<span class="mw-page-title-main">Biofilm</span> Aggregation of bacteria or cells on a surface

A biofilm comprises any syntrophic consortium of microorganisms in which cells stick to each other and often also to a surface. These adherent cells become embedded within a slimy extracellular matrix that is composed of extracellular polymeric substances (EPSs). The cells within the biofilm produce the EPS components, which are typically a polymeric conglomeration of extracellular polysaccharides, proteins, lipids and DNA. Because they have three-dimensional structure and represent a community lifestyle for microorganisms, they have been metaphorically described as "cities for microbes".

<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">Lipopolysaccharide</span> Class of molecules found in the outer membrane of Gram-negative bacteria

Lipopolysaccharides (LPS) are large molecules consisting of a lipid and a polysaccharide that are bacterial toxins. They are composed of an O-antigen, an outer core, and an inner core all joined by covalent bonds, and are found in the bacterial capsule, the outermost membrane of cell envelope of Gram-negative bacteria, such as E. coli and Salmonella. Today, the term endotoxin is often used synonymously with LPS, although there are a few endotoxins that are not related to LPS, such as the so-called delta endotoxin proteins produced by Bacillus thuringiensis.

<i>Pseudomonas aeruginosa</i> Species of bacterium

Pseudomonas aeruginosa is a common encapsulated, Gram-negative, aerobic–facultatively anaerobic, rod-shaped bacterium that can cause disease in plants and animals, including humans. A species of considerable medical importance, P. aeruginosa is a multidrug resistant pathogen recognized for its ubiquity, its intrinsically advanced antibiotic resistance mechanisms, and its association with serious illnesses – hospital-acquired infections such as ventilator-associated pneumonia and various sepsis syndromes.

Adhesins are cell-surface components or appendages of bacteria that facilitate adhesion or adherence to other cells or to surfaces, usually in the host they are infecting or living in. Adhesins are a type of virulence factor.

<span class="mw-page-title-main">Lysogenic cycle</span> Process of virus reproduction

Lysogeny, or the lysogenic cycle, is one of two cycles of viral reproduction. Lysogeny is characterized by integration of the bacteriophage nucleic acid into the host bacterium's genome or formation of a circular replicon in the bacterial cytoplasm. In this condition the bacterium continues to live and reproduce normally, while the bacteriophage lies in a dormant state in the host cell. The genetic material of the bacteriophage, called a prophage, can be transmitted to daughter cells at each subsequent cell division, and later events can release it, causing proliferation of new phages via the lytic cycle.

<i>Pseudomonas syringae</i> Species of bacterium

Pseudomonas syringae is a rod-shaped, Gram-negative bacterium with polar flagella. As a plant pathogen, it can infect a wide range of species, and exists as over 50 different pathovars, all of which are available to researchers from international culture collections such as the NCPPB, ICMP, and others.

<span class="mw-page-title-main">Pathogenic bacteria</span> Disease-causing bacteria

Pathogenic bacteria are bacteria that can cause disease. This article focuses on the bacteria that are pathogenic to humans. Most species of bacteria are harmless and are often beneficial but others can cause infectious diseases. The number of these pathogenic species in humans is estimated to be fewer than a hundred. By contrast, several thousand species are part of the gut flora present in the digestive tract.

<span class="mw-page-title-main">Lactonase</span> Class of enzymes

Lactonase (EC 3.1.1.81, acyl-homoserine lactonase; systematic name N-acyl-L-homoserine-lactone lactonohydrolase) is a metalloenzyme, produced by certain species of bacteria, which targets and inactivates acylated homoserine lactones (AHLs). It catalyzes the reaction

<i>Bacillus anthracis</i> Species of bacterium

Bacillus anthracis is a gram-positive and rod-shaped bacterium that causes anthrax, a deadly disease to livestock and, occasionally, to humans. It is the only permanent (obligate) pathogen within the genus Bacillus. Its infection is a type of zoonosis, as it is transmitted from animals to humans. It was discovered by a German physician Robert Koch in 1876, and became the first bacterium to be experimentally shown as a pathogen. The discovery was also the first scientific evidence for the germ theory of diseases.

Pathogenomics is a field which uses high-throughput screening technology and bioinformatics to study encoded microbe resistance, as well as virulence factors (VFs), which enable a microorganism to infect a host and possibly cause disease. This includes studying genomes of pathogens which cannot be cultured outside of a host. In the past, researchers and medical professionals found it difficult to study and understand pathogenic traits of infectious organisms. With newer technology, pathogen genomes can be identified and sequenced in a much shorter time and at a lower cost, thus improving the ability to diagnose, treat, and even predict and prevent pathogenic infections and disease. It has also allowed researchers to better understand genome evolution events - gene loss, gain, duplication, rearrangement - and how those events impact pathogen resistance and ability to cause disease. This influx of information has created a need for bioinformatics tools and databases to analyze and make the vast amounts of data accessible to researchers, and it has raised ethical questions about the wisdom of reconstructing previously extinct and deadly pathogens in order to better understand virulence.

Host–parasite coevolution is a special case of coevolution, where a host and a parasite continually adapt to each other. This can create an evolutionary arms race between them. A more benign possibility is of an evolutionary trade-off between transmission and virulence in the parasite, as if it kills its host too quickly, the parasite will not be able to reproduce either. Another theory, the Red Queen hypothesis, proposes that since both host and parasite have to keep on evolving to keep up with each other, and since sexual reproduction continually creates new combinations of genes, parasitism favours sexual reproduction in the host.

Jonathan Alan Hodgkin is a British biochemist, Professor of Genetics at the University of Oxford and an emeritus fellow of Keble College, Oxford.

In biology, a pathogen, in the oldest and broadest sense, is any organism or agent that can produce disease. A pathogen may also be referred to as an infectious agent, or simply a germ.

The host–pathogen interaction is defined as how microbes or viruses sustain themselves within host organisms on a molecular, cellular, organismal or population level. This term is most commonly used to refer to disease-causing microorganisms although they may not cause illness in all hosts. Because of this, the definition has been expanded to how known pathogens survive within their host, whether they cause disease or not.

<span class="mw-page-title-main">Frederick M. Ausubel</span> American molecular biologist

Frederick M Ausubel is an American molecular biologist and professor of genetics at Harvard Medical School in Boston and is the Karl Winnacker Distinguished Investigator in the Department of Molecular Biology, Massachusetts General Hospital, Boston., Massachusetts.

Nematocida parisii is a parasitic species of Microsporidia fungi found in wild isolates of the common nematode, Caenorhabditis elegans. The fungus forms spores and replicates in the intestines before leaving the host.

Caenorhabditis tropicalis is a species of Caenorhabditis nematodes, belonging to the Elegans super-group and Elegans group within the genus. It is a close relative of C. wallacei.C. tropicalis is collected frequently in tropical South America, Caribbean islands, and various islands in the Indian and Pacific Oceans from rotting fruit, flowers and stems. C. tropicalis was referred to as “C. sp. 11” prior to 2014.

Worm bagging 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.

References

  1. ↑ Samuel, Buck S.; Rowedder, Holli; Braendle, Christian; Félix, Marie-Anne; Ruvkun, Gary (2016-07-05). "Caenorhabditis elegans responses to bacteria from its natural habitats". Proceedings of the National Academy of Sciences of the United States of America. 113 (27): E3941–3949. Bibcode:2016PNAS..113E3941S. doi: 10.1073/pnas.1607183113 . ISSN   1091-6490. PMC   4941482 . PMID   27317746.
  2. 1 2 3 Zhang, Jingyan; Holdorf, Amy D; Walhout, Albertha JM (August 2017). "C. elegans and its bacterial diet as a model for systems-level understanding of host–microbiota interactions". Current Opinion in Biotechnology. 46: 74–80. doi:10.1016/j.copbio.2017.01.008. PMC   5544573 . PMID   28189107.
  3. 1 2 Haber, M; Schüngel, M; Putz, A; Müller, S; Hasert, B; Schulenburg, H (2004). "Evolutionary history of Caenorhabditis elegans inferred from microsatellites: evidence for spatial and temporal genetic differentiation and the occurrence of outbreeding". Mol Biol Evol. 22 (1): 160–173. doi: 10.1093/molbev/msh264 . PMID   15371529.
  4. ↑ Nørhave, NJ; Spurgeon, D; Svendsen, C; Cedergreen, N (2012). "How does growth temperature affect cadmium toxicity measured on different life history traits in the soil nematode Caenorhabditis elegans?". Environ Toxicol Chem. 31 (4): 787–793. doi:10.1002/etc.1746. PMID   22253140. S2CID   21375636.
  5. 1 2 3 4 Troemel, ER; Félix, M-A; Whiteman, NK; Barrière, A; Ausubel, FM (2008). "Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans". PLOS Biol. 6 (12): 2736–2752. doi: 10.1371/journal.pbio.0060309 . PMC   2596862 . PMID   19071962.
  6. ↑ Barrière A, Félix MA (2007). "Temporal dynamics and linkage disequilibrium in natural Caenorhabditis elegans populations". Genetics. 176 (2): 999–1011. doi:10.1534/genetics.106.067223. PMC   1894625 . PMID   17409084.
  7. ↑ Kiontke KC, Félix MA, Ailion M, Rockman MV, Braendle C, Pénigault JB, Fitch DH (2011). "A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits". BMC Evol Biol. 11: 339. doi: 10.1186/1471-2148-11-339 . PMC   3277298 . PMID   22103856.
  8. ↑ Blaxter M, Denver DR (2012). "The worm in the world and the world in the worm". BMC Biol. 10: 57. doi: 10.1186/1741-7007-10-57 . PMC   3382423 . PMID   22731915.
  9. 1 2 Félix MA, Duveau F (2012). "Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C. briggsae". BMC Biol. 10: 59. doi: 10.1186/1741-7007-10-59 . PMC   3414772 . PMID   22731941.
  10. ↑ McGrath PT, Xu Y, Ailion M, Garrison JL, Butcher RA, Bargmann CI (2011). "Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes". Nature. 477 (7364): 321–325. Bibcode:2011Natur.477..321M. doi:10.1038/nature10378. PMC   3257054 . PMID   21849976.
  11. ↑ Weber KP, De S, Kozarewa I, Turner DJ, Babu MM, de Bono M (2010). "Whole Genome Sequencing Highlights Genetic Changes Associated with Laboratory Domestication of C. elegans". PLOS ONE. 5 (11): e13922. Bibcode:2010PLoSO...513922W. doi: 10.1371/journal.pone.0013922 . PMC   2978686 . PMID   21085631.
  12. ↑ Barrière, A.; Félix, M.-A. (2005). "Natural variation and population genetics of Caenorhabditis elegans (December 26, 2005), WormBook, ed. The C. elegans Research Community". WormBook: 1–19. doi:10.1895/wormbook.1.43.1. PMC   4781346 . PMID   18050391.
  13. ↑ Félix, M.-A.; Barrière, A. (2010). "The natural history of Caenorhabditis elegans". Current Biology. 20 (22): R965–9. doi: 10.1016/j.cub.2010.09.050 . PMID   21093785. S2CID   12869939.
  14. ↑ Fuhrmann, Jeffry J.; Zuberer, David A. (1998). Principles and Applications of Soil Microbiology. Prentice Hall. ISBN   978-0-13-459991-5.[ page needed ]
  15. ↑ Garigan D, Hsu AL, Fraser AG, Kamath RS, Ahringer J, Kenyon C (2002). "Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation". Genetics. 161 (3): 1101–1112. doi:10.1093/genetics/161.3.1101. PMC   1462187 . PMID   12136014.
  16. ↑ McGee MD, Weber D, Day N, Vitelli C, Crippen D, Herndon LA, Hall DH, Melov S (2011). "Loss of intestinal nuclei and intestinal integrity in aging C. elegans". Aging Cell. 10 (4): 699–710. doi:10.1111/j.1474-9726.2011.00713.x. PMC   3135675 . PMID   21501374.
  17. ↑ Brenner, S. (1974). "The genetics of Caenorhabditis elegans". Genetics. 77 (1): 71–94. doi:10.1093/genetics/77.1.71. PMC   1213120 . PMID   4366476.
  18. ↑ Frézal, Lise; Félix, Marie-Anne (30 March 2015). "C. elegans outside the Petri dish". eLife. 4: e05849. doi: 10.7554/eLife.05849 . PMC   4373675 . PMID   25822066.
  19. 1 2 Stiernagle, T. (February 11, 2006). The C. elegans Research Community (ed.). "Maintenance of C. elegans". WormBook: 1–11. doi:10.1895/wormbook.1.101.1. PMC   4781397 . PMID   18050451.
  20. ↑ Clark, L.C., Hodgkin, J. (2014). "Commensals, probiotics and pathogens in the C aenorhabditis elegans model". Cell Microbiol. 16 (1): 27–38. doi: 10.1111/cmi.12234 . PMID   24168639. S2CID   3520862.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  21. 1 2 3 4 Coolon, J.D., Jones, K.L., Todd, T.C., Carr, B.C., and Herman, M.A. (2009). "Caenorhabditis elegans Genomic Response to Soil Bacteria Predicts Environment-Specific Genetic Effects on Life History Traits". PLOS Genetics. 5 (6): e1000503. doi: 10.1371/journal.pgen.1000503 . PMC   2684633 . PMID   19503598.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  22. 1 2 3 Montalvo-Katz, Sirena; Huang, Hao; Appel, Michael David; Berg, Maureen; Shapira, Michael (2012). "Association with Soil Bacteria Enhances p38-Dependent Infection Resistance in Caenorhabditis elegans". Infection and Immunity. 81 (2): 514–520. doi:10.1128/IAI.00653-12. PMC   3553824 . PMID   23230286.
  23. ↑ Sekirov, Inna; Russell, Shannon L.; Antunes, L. Caetano M.; Finlay, B. Brett (July 2010). "Gut Microbiota in Health and Disease". Physiological Reviews. 90 (3): 859–904. doi:10.1152/physrev.00045.2009. PMID   20664075. S2CID   9281721.
  24. ↑ Stecher B, Hardt WD (2011). "Mechanisms controlling pathogen colonization of the gut". Curr. Opin. Microbiol. 14 (1): 82–91. doi:10.1016/j.mib.2010.10.003. PMID   21036098.
  25. ↑ Tan MW, Mahajan-Miklos S, Ausubel FM (1999). "Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis". Proc. Natl. Acad. Sci. U.S.A. 96 (2): 715–720. Bibcode:1999PNAS...96..715T. doi: 10.1073/pnas.96.2.715 . PMC   15202 . PMID   9892699.
  26. ↑ Avery L, Shtonda BB (2003). "Food transport in the C. elegans pharynx". J. Exp. Biol. 206 (14): 2441–2457. doi:10.1242/jeb.00433. PMC   3951750 . PMID   12796460.
  27. ↑ Pike, Victoria L.; Ford, Suzanne A.; King, Kayla C.; Rafaluk‐Mohr, Charlotte (October 2019). "Fecundity compensation is dependent on the generalized stress response in a nematode host". Ecology and Evolution. 9 (20): 11957–11961. doi:10.1002/ece3.5704. PMC   6822023 . PMID   31695900.
  28. 1 2 MacNeil, L.T., Watson, E., Arda, H.E., Zhu, L.J., and Walhout, A.J.M (2013). "Diet-induced developmental acceleration independent of TOR and insulin in C. elegans". Cell. 153 (1): 240–252. doi:10.1016/j.cell.2013.02.049. PMC   3821073 . PMID   23540701.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  29. ↑ Altun, Z.F.; Hall, D.H. "Introduction. In WormAtlas".{{cite journal}}: Cite journal requires |journal= (help)
  30. ↑ Go, Junhyeok (2014). "Extended longevity and robust early-stage development of Caenorhabditis elegans by a soil microbe, Lysinibacillus sphaericus". Environmental Microbiology Reports. 6 (6): 730–737. doi:10.1111/1758-2229.12196. PMID   25756126.
  31. 1 2 Schulenburg, H., Kurz, C.L., Ewbank, J.J. (2004). "Evolution of the innate immune system: the worm perspective". Immunological Reviews. 198: 36–58. doi:10.1111/j.0105-2896.2004.0125.x. PMID   15199953. S2CID   21541043.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  32. ↑ Hodgkin J, Partridge FA (2008). "Caenorhabditis elegans Meets Microsporidia: The Nematode Killers from Paris. PLoS Biol". PLOS Biology. 6 (12): 2634–7. doi: 10.1371/journal.pbio.1000005 . PMC   2605933 . PMID   19108611.
  33. ↑ Ewbank, Jonathan (2006). "Signaling in the immune response". WormBook: 1–12. doi:10.1895/wormbook.1.83.1. PMC   4781569 . PMID   18050470.
  34. ↑ Schulenburg, H., Ewbank, J.J (2007). "the genetics of pathogen avoidance in Caenorhabditis elegans". Molecular Microbiology. 66 (3): 563–570. doi: 10.1111/j.1365-2958.2007.05946.x . PMID   17877707. S2CID   20783253.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  35. ↑ Chan, Shepherd Yuen; Liu, Sylvia Yang; Seng, Zijing; Chua, Song Lin (January 2021). "Biofilm matrix disrupts nematode motility and predatory behavior". The ISME Journal. 15 (1): 260–269. doi: 10.1038/s41396-020-00779-9 . ISSN   1751-7370. PMC   7852553 . PMID   32958848.
  36. ↑ Li, Shaoyang; Liu, Sylvia Yang; Chan, Shepherd Yuen; Chua, Song Lin (May 2022). "Biofilm matrix cloaks bacterial quorum sensing chemoattractants from predator detection". The ISME Journal. 16 (5): 1388–1396. doi:10.1038/s41396-022-01190-2. ISSN   1751-7370. PMC   9038794 . PMID   35034106.
  37. ↑ Hu, Minqi; Ma, Yeping; Chua, Song Lin (2024-01-16). "Bacterivorous nematodes decipher microbial iron siderophores as prey cue in predator–prey interactions". Proceedings of the National Academy of Sciences. 121 (3). doi: 10.1073/pnas.2314077121 . ISSN   0027-8424.
  38. ↑ Luallen, Robert; Reinke, Aaron; Tong, Linda; Botts, Michael; Felix, Marie-Anne; Troemel, Emily (2016). "Discovery of a Natural Microsporidian Pathogen with a Broad Tissue Tropism in Caenorhabditis elegans". PLOS Pathogens. 12 (6): e1005724. bioRxiv   10.1101/047720 . doi: 10.1371/journal.ppat.1005724 . PMC   4928854 . PMID   27362540.
  39. ↑ Barron, George L (1977). The nematode-destroying fungi. Canadian Biological Publications. OCLC   742327534.
  40. ↑ Jansson, Hans-Börje (December 1994). "Adhesion of Conidia of Drechmeria coniospora to Caenorhabditis elegans WildType and Mutants". Journal of Nematology. 26 (4): 430–435. PMC   2619527 . PMID   19279912.
  41. ↑ Félix MA, Ashe A, Piffaretti J, Wu G, Nuez I (2011). "Natural and Experimental Infection of Caenorhabditis Nematodes by Novel Viruses Related to Nodaviruses". PLOS Biol. 9 (1): e1000586. doi: 10.1371/journal.pbio.1000586 . PMC   3026760 . PMID   21283608.
  42. ↑ Gammon, Don B. (2017-12-01). "Caenorhabditis elegans as an Emerging Model for Virus-Host Interactions". Journal of Virology. 91 (23). doi:10.1128/JVI.00509-17. ISSN   0022-538X. PMC   5686719 . PMID   28931683.
  43. ↑ Hodgkin, J., Félix, MA., Clark, L.C., Stroud, D., Gravato-Nobre, M.J. (2013). "Two Leucobacter Strains Exert Complementary Virulence on Caenorhabditis Including Death by Worm-Star Formation". Curr. Biol. 23 (21): 2157–2161. doi:10.1016/j.cub.2013.08.060. PMC   3898767 . PMID   24206844.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  44. ↑ Höfte, H., Whiteley, H.R. (1989). "Insecticidal crystal proteins of Bacillus thuringiensis". Microbiol. Rev. 53 (2): 242–255. doi:10.1128/MMBR.53.2.242-255.1989. PMC   372730 . PMID   2666844.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  45. 1 2 3 Schulenburg, H., Müller S. (2004). "Natural variation in the response of Caenorhabditis elegans towards Bacillus thuringiensis". Parasitology. 128 (4): 433–443. doi:10.1017/s003118200300461x. PMID   15151149. S2CID   41628475.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  46. ↑ Wei J.Z.; Hale K.; Carta L.; Platzer E.; Wong C.; Fang S-C.; Aroian R.V. (2003). "Bacillus thuringiensis crystal proteins that target nematodes". PNAS. 100 (5): 2760–2765. Bibcode:2003PNAS..100.2760W. doi: 10.1073/pnas.0538072100 . PMC   151414 . PMID   12598644.
  47. ↑ Borgonie G.; Van Driessche R.; Leyns F.; Arnaut G.; De Waele D.; Coomans A (1995). "Germination of Bacillus thuringiensis Spores in Bacteriophagous Nematodes (Nematoda: Rhabditida)". Journal of Invertebrate Pathology. 65 (1): 61–67. doi:10.1006/jipa.1995.1008. PMID   7876593.
  48. 1 2 3 Salamitou S.; Ramisse F.; Brehélin M.; Bourget D.; Gilois N.; Gominet M.; Hernandez E.; Lereclus D. (2000). "the plcR regulon is involved in the opportunistic properties of Bacillus thuringiensis and Bacillus cereus in mice and insects". Microbiology. 146 (11): 2825–2832. doi: 10.1099/00221287-146-11-2825 . PMID   11065361.

Further reading

This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.