Steinernema carpocapsae

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Steinernema carpocapsae
Steinernema carpocapsae SEM.tif
An activated Steinernema carpocapsae infective juvenile nematode.
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Nematoda
Class: Chromadorea
Order: Rhabditida
Family: Steinernematidae
Genus: Steinernema
Species:
S. carpocapsae
Binomial name
Steinernema carpocapsae
(Weiser, 1955)

Steinernema carpocapsae is an entomopathogenic nematode and a member of the family Steinernematidae. It is a parasitic roundworm that has evolved an insect-killing symbiosis with bacteria, and kills its hosts within a few days of infection. This parasite releases its bacterial symbiont along with a variety of proteins into the host after infection, and together the bacteria and nematode overcome host immunity and kill the host quickly. As a consequence, S. carpocapsae has been widely adapted for use as a biological control agent in agriculture and pest control. S. carpocapsae is considered a generalist parasite and has been effectively used to control a variety of insects including: Webworms, cutworms, armyworms, girdlers, some weevils, and wood-borers. This species is an example of an "ambush" forager, standing on its tail in an upright position near the soil surface and attaching to passing hosts, even capable of jumping. As an ambush forager, S. carpocapsae is thought to be especially effective when applied against highly mobile surface-adapted insects (though some below-ground insects are also controlled by this nematode). S. carpocapsae can sense carbon dioxide production, making the spiracles a key portal of entry into its insect hosts. It is most effective at temperatures ranging from 22–28 °C (72–82 °F) . [1]

Contents

Lifecycle

A general life cycle of entomopathogenic nematodes. EPN Lifecycle.tif
A general life cycle of entomopathogenic nematodes.

Steinernema carpocapsae is categorized as an entomopathogenic nematode, which is a specialized subgroup of insect-parasitic nematodes. [3] [4] The infective juvenile stage (IJ) is a modified third stage larva and is the only free-living stage of this nematode. It is a developmentally arrested, non-feeding stage, that seeks out an insect host to infect. All other life stages (L1, L2, L3, L4, and adult) occur within an insect host. The IJ enters the host through natural openings such as the spiracles, mouth, anus, or in some species through intersegmental membranes of the cuticle, and then enters into the hemocoel. [3] S. carpocapsae are mutualistically associated with the bacterium Xenorhabdus nematophila. [5] When the IJ stage enters the host, it initiates the actively parasitic part of its lifecycle. This process includes the resumption of development, and the release of their symbiotic bacteria and a variety of nematode-derived proteins into the hemocoel. [6] Though the X. nematophila bacteria is carried by the IJ in a specialized structure in the anterior gut called the receptacle, it is released into the host through defecation. [7] [8] The bacteria multiply in the insect hemolymph and the infected host usually dies within 24 to 48 hours. After the death of the host, nematodes continue to feed on the host tissue and the multiplying bacteria. They develop into males and females and reproduce. The progeny develop through four juvenile stages to the adult. Depending on the available resources, one or more generations may occur within the host cadaver and a large number of infective juveniles is eventually released into the environment to infect other hosts and continue their lifecycle. [3] [5]

Morphology

Morphological changes during the activation of a Steinernema carpocapsae infective juvenile. The IJ was imaged at 400X magnification and the black box is magnified in the image below. The arrow is pointing to the basal bulb of the pharynx, which expands during activation. Steinernema carpocapsae activation.tif
Morphological changes during the activation of a Steinernema carpocapsae infective juvenile. The IJ was imaged at 400X magnification and the black box is magnified in the image below. The arrow is pointing to the basal bulb of the pharynx, which expands during activation.

The IJ stage is the only free-living and therefore environmentally tolerant stage, thus S. carpocapsae nematodes are formulated and applied as infective juveniles. [9] S. carpocapsae IJs are between 0.44-0.65 mm in length, with males ranging from 1-1.7 mm and females ranging from 2.8-5.1 mm in length. [10] The IJs can be stored in tap water or buffer for several months, and can even be frozen for long term storage in liquid nitrogen. [11] When stored, the nematodes tend to display reduced movement, though disturbed nematodes move actively. S. carpocapsae and other ambush foragers, when stored in water soon revert to a characteristic J-shaped resting position, meaning that they have a straight body posture with a minor kink at the end of the tail. In short, lack of movement is not always a sign of mortality; nematodes may have to be stimulated (e.g., probes, acetic acid, gentle heat) to move before assessing viability. Living infective juveniles, that would still be useful in biological control, tend to possess high lipid levels that provide a dense appearance, whereas nearly transparent nematodes are often active but possess limited infection capabilities. [11]

Insects killed by most steinernematid nematodes, including S. carpocapsae, become brown or tan, distinctly different from insects killed by heterorhabditids, which become red and the tissues assume a gummy consistency. [11] Black cadavers with associated putrefaction indicate that the host was not killed by entomopathogenic species. Nematodes found within such cadavers tend to be free-living soil saprophages. [1]

The developmentally arrested IJ stage will activate upon exposure to insect tissue. The process of activation includes morphological changes, resumption of development, release of symbiotic bacteria, and release of a variety of proteins thought to be involved in active parasitism. [6] The morphological changes associated with activation include opening of the mouth and anus, opening of the oesophagus, expansion of the basal bulb of the pharynx, and the initiation of pumping of the pharynx. [6]

Mechanism

The immunomodulatory and pathogenic properties of parasitic nematodes are largely attributed to the excretory/secretory (ES) products they release during infection. The infective larvae also start spewing out a complex cocktail of proteins. When researchers isolated and examined this mixture more closely, they found that it was made up of 472 different proteins – many of them are proteases. For the average insect, a lethal dose of Xenorhabdus nematophilus consists of about 3500 bacterial cells. But, each S. carpocapsae only carries 20—200 cells of X. nematophilus – well below the lethal dose. The fact that a single worm is enough to kill an insect host with so few bacterial cells means that S. carpocapsae is not just relying on the bacteria to do all the work. [6]

Habitat

Steinernematid nematodes are exclusively soil organisms. They are ubiquitous, having been isolated from every inhabited continent from a wide range of ecologically diverse soil habitats including cultivated fields, forests, grasslands, deserts, and even ocean beaches. When surveyed, entomopathogenic nematodes are recovered from 2% to 45% of sites sample. [12]

Distribution

Asia, Africa, North, Central, South America and Caribbean, Oceania, and Europe. [13]

Related Research Articles

<i>Heterorhabditis</i> Genus of roundworms

Heterorhabditis is a genus of nematodes belonging to the order Rhabditida. All species of this genus are obligate parasites of insects, and some are used as biological control agents for the control of pest insects.

<span class="mw-page-title-main">Entomopathogenic nematode</span> Group of thread worms that attack insects

Entomopathogenic nematodes (EPN) are a group of nematodes, that cause death to insects. The term entomopathogenic has a Greek origin, with entomon, meaning insect, and pathogenic, which means causing disease. They are animals that occupy a bio control middle ground between microbial pathogens and predator/parasitoids. Although many other parasitic thread worms cause diseases in living organisms, entomopathogenic nematodes are specific in only infecting insects. Entomopathogenic nematodes (EPNs) live parasitically inside the infected insect host, and so they are termed as endoparasitic. They infect many different types of insects living in the soil like the larval forms of moths, butterflies, flies and beetles as well as adult forms of beetles, grasshoppers and crickets. EPNs have been found all over the world in a range of ecologically diverse habitats. They are highly diverse, complex and specialized. The most commonly studied entomopathogenic nematodes are those that can be used in the biological control of harmful insects, the members of Steinernematidae and Heterorhabditidae. They are the only insect-parasitic nematodes possessing an optimal balance of biological control attributes.

<i>Photorhabdus luminescens</i> Species of bacterium

Photorhabdus luminescens is a Gammaproteobacterium of the family Morganellaceae, and is a lethal pathogen of insects.

<i>Sphaerularia bombi</i> Species of roundworm

Sphaerularia bombi is an entomopathogenic nematode. It is parasite of bumblebees. It infects and sterilizes gynes or potential queens of bumblebees.

<i>Heterorhabditis bacteriophora</i> Species of roundworm

Heterorhabditis bacteriophora is a species of entomopathogenic nematode known commonly as beneficial nematodes. They are microscopic and are used in gardening as a form of biological pest control. They are used to control ants, fleas, moths, beetles, flies, weevils, and other pests.

Xenorhabdus is a genus of motile, gram-negative bacteria from the family of the Morganellaceae. All the species of the genus are only known to live in symbiosis with soil entomopathogenic nematodes from the genus Steinernema.

Photorhabdus is a genus of bioluminescent, gram-negative bacilli which lives symbiotically within entomopathogenic nematodes, hence the name photo and rhabdus. Photorhabdus is known to be pathogenic to a wide range of insects and has been used as biopesticide in agriculture.

<i>Heterorhabditis megidis</i> Species of roundworm

Heterorhabditis megidis is a species of nematodes in the genus Heterorhabditis. All species of this genus are obligate parasites of insects, and some are used as biological control agents for the control of pest insects.

Steinernema scapterisci, the mole cricket nematode, is a species of nematode in the order Rhabditida. It is a parasite of insects in the order Orthoptera, the grasshoppers, crickets and their allies. Native to southern South America, it was introduced into Florida in the United States in an effort to provide a biological control of pest (Neoscapteriscus) mole crickets.

Xenorhabdus ehlersii is a bacterium from the genus of Xenorhabdus which has been isolated from the nematode Steinernema serratum in China.

Xenorhabdus bovienii is a bacterium from the genus of Xenorhabdus which has been isolated from the nematodes Steinernema bibionis, Steinernema krsussei, Steinernema affine, Steinernema carpocapsae, Steinernema feltiae, Steinernema intermedium, Steinernema jollieti and Steinernema weiseri. Xenorhabdus bovienii produces N-Butanoylpyrrothine, N-(3-Methylbutanoyl)pyrrothine and Xenocyloins.

Xenorhabdus griffiniae is a bacterium from the genus of Xenorhabdus which has been isolated from the nematode Steinernema hermaphroditum in Indonesia.

Xenorhabdus indica is a bacterium from the genus of Xenorhabdus which has been isolated from the nematodes Steinernema thermophilum and Steinernema yirgalemense. Xenorhabdus indica produces the Taxlllaids A–G.

Xenorhabdus koppenhoeferi is a bacterium from the genus Xenorhabdus which has been isolated from the nematode Steinernema scarabaei in the United States.

Xenorhabdus japonica is a bacterium from the genus Xenorhabdus which has been isolated from the nematode Steinernema kushidai in Japan.

Xenorhabdus poinarii is a bacterium from the genus Xenorhabdus which has been isolated from the nematodes Steinernema glaseri and Steinernema cubanum.

The Steinernematidae are a family of nematodes in the order Rhabditida.

<i>Steinernema</i> Genus of roundworms

Steinernema is a genus of nematodes in the family of Steinernematidae. The genus Steinernema is named after the nematologist Gotthold Steiner.

<span class="mw-page-title-main">Morganellaceae</span> Family of bacteria

The Morganellaceae are a family of Gram-negative bacteria that include some important human pathogens formerly classified as Enterobacteriaceae. This family is a member of the order Enterobacterales in the class Gammaproteobacteria of the phylum Pseudomonadota. Genera in this family include the type genus Morganella, along with Arsenophonus, Cosenzaea, Moellerella, Photorhabdus, Proteus, Providencia and Xenorhabdus.

Necromeny is a symbiotic relationship where an animal infects a host and waits inside its body until its death, at which point it develops and completes its life-cycle on the cadaver, feeding on the decaying matter and the subsequent bacterial growth. As the necromenic animal benefits from the relationship while the host is unharmed, it is an example of commensalism.

References

  1. 1 2 Shapiro-Ilan, D. I. (n.d.). Rhabditida: Steinernematidae & Heterorhabditidae. Retrieved November 20, 2017, from https://biocontrol.entomology.cornell.edu/pathogens/nematodes.php
  2. ↑ Dillman, Adler R.; Chaston, John M.; Adams, Byron J.; Ciche, Todd A.; Goodrich-Blair, Heidi; Stock, S. Patricia; Sternberg, Paul W. (2012-03-01). Rall, Glenn F. (ed.). "An Entomopathogenic Nematode by Any Other Name". PLOS Pathogens. 8 (3): e1002527. doi: 10.1371/journal.ppat.1002527 . ISSN   1553-7374. PMC   3291613 . PMID   22396642.
  3. 1 2 3 Kaya, H K; Gaugler, R (1993). "Entomopathogenic Nematodes". Annual Review of Entomology. 38 (1): 181–206. doi:10.1146/annurev.en.38.010193.001145. ISSN   0066-4170.
  4. ↑ Dillman, Adler R.; Chaston, John M.; Adams, Byron J.; Ciche, Todd A.; Goodrich-Blair, Heidi; Stock, S. Patricia; Sternberg, Paul W. (2012-03-01). Rall, Glenn F. (ed.). "An Entomopathogenic Nematode by Any Other Name". PLOS Pathogens. 8 (3): e1002527. doi: 10.1371/journal.ppat.1002527 . ISSN   1553-7374. PMC   3291613 . PMID   22396642.
  5. 1 2 Akhurst, RJ; Dunphy, GB (1993). "Tripartite interactions between symbiotically associated entomopathogenic bacteria, nematodes, and their insect hosts". Parasites and Pathogens of Insects. Volume 2: Pathogens. Academic Press. ISBN   978-0120844425.
  6. 1 2 3 4 5 Lu, D., Macchietto, M., Chang, D., Barros, M. M., Baldwin, J., Mortazavi, A., & Dillman, A. R. (2017). Activated entomopathogenic nematode infective juveniles release lethal venom proteins. PLoS Pathogens, 13(4): e1006302.
  7. ↑ Martens, E. C.; Heungens, K.; Goodrich-Blair, H. (2003-05-15). "Early Colonization Events in the Mutualistic Association between Steinernema carpocapsae Nematodes and Xenorhabdus nematophila Bacteria". Journal of Bacteriology. 185 (10): 3147–3154. doi:10.1128/JB.185.10.3147-3154.2003. ISSN   0021-9193. PMC   154081 . PMID   12730175.
  8. ↑ Snyder, H.; Stock, S. P.; Kim, S.-K.; Flores-Lara, Y.; Forst, S. (2007-08-15). "New Insights into the Colonization and Release Processes of Xenorhabdus nematophila and the Morphology and Ultrastructure of the Bacterial Receptacle of Its Nematode Host, Steinernema carpocapsae". Applied and Environmental Microbiology. 73 (16): 5338–5346. Bibcode:2007ApEnM..73.5338S. doi:10.1128/AEM.02947-06. ISSN   0099-2240. PMC   1951000 . PMID   17526783.
  9. ↑ Lacey, Lawrence A.; Georgis, Ramon (2012). "Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production". Journal of Nematology. 44 (2): 218–225. ISSN   0022-300X. PMC   3578470 . PMID   23482993.
  10. ↑ Nguyen, Khuong B.; Hunt, David J.; Mracek, Zdenek (2007). "Chapter 4: Steinernematidae: Species descriptions". In Nguyen, Khuong B. (ed.). Entomopathogenic Nematodes: Systematics, Phylogeny and Bacterial Symbionts. Brill. pp. 218–225. ISBN   9789004152939.
  11. 1 2 3 Kaya, Harry K.; Stock, S. Patricia (1997). "Chapter VI: Techniques in insect nematology". Manual of Techniques in Insect Pathology. Academic Press Limited. pp. 281–324. ISBN   0124325556.
  12. ↑ Hominick, W. M. 2002. Biogeography. In: Gaugler, R. (Ed.), Entomopathogenic Nematology. CABI, New York, NY, pp. 115-143.
  13. ↑ "Steinernema carpocapsae".
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