Nematophagous fungus

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A dead nematode with Harposporium anguillulae growing out of it. Numbered ticks are 122 mm apart. 20100814 175958 FungusOnDeadnematode HarposporiumAnguillulae.jpg
A dead nematode with Harposporium anguillulae growing out of it. Numbered ticks are 122 μm apart.
A closer look at H. anguillulae from the previous image. Numbered ticks are 20 mm apart. 20100814 180201 FungusOnDeadnematode HarposporiumAnguillulae.jpg
A closer look at H. anguillulae from the previous image. Numbered ticks are 20 μm apart.
A fungus of the genus Arthrobotrys, showing adhesive nets which it uses to trap nematodes.  Numbered ticks are 122 mm apart. 20100828 005957 Fungus.jpg
A fungus of the genus Arthrobotrys , showing adhesive nets which it uses to trap nematodes.  Numbered ticks are 122 μm apart.

Nematophagous fungi are carnivorous fungi specialized in trapping and digesting nematodes. Around 160 species are known. Species exist that live inside the nematodes from the beginning and others that catch them, mostly with glue traps or in rings, some of which constrict on contact. Some species possess both types of traps. Another technique is to stun the nematodes using toxins, a method employed by Coprinus comatus , Stropharia rugosoannulata , and the family Pleurotaceae. [1] The habit of feeding on nematodes has arisen many times among fungi, as is demonstrated by the fact that nematophagous species are found in all major fungal groups. [2] Nematophagous fungi can be useful in controlling those nematodes that eat crops. Purpureocillium , for example, can be used as a bio-nematicide.

Contents

Types

Fungi that feed on nematodes (as the most abundant and convenient prey species) mostly live in nitrogen-deficient habitats. [3] These fungi can be divided into four main groups according to the methods they use to catch their prey. Some use a mechanical means, an adhesive or a mechanical hyphal trap. Some produce a toxin and use it to immobilise the nematode. Some are parasitic, using their spores to gain entry into their prey, and some are egg parasites, inserting their hyphal tips into the eggs or cysts, or into females before the eggs are deposited. [4]

Diversity

Nematophagous fungi have been found throughout the world in a wide range of habitats and climates, but few from extreme environments. Most studied have been the species that attack the nematodes of interest to farmers, horticulturists and foresters, but there are large numbers of species as yet undescribed. The sexual stage of Orbilia occurs on rotting wood on land or in fresh water, while the asexual stage occurs in marine, fresh water and terrestrial habitats. Arthrobotrys dactyloides was the first species to be discovered in brackish water, and other species have been found on mangroves. [4]

Ecology

Nematode-trapping fungi are mostly concentrated in the upper part of the soil, in pastures, leaf litter, mangroves and certain shallow aquatic habitats. They employ techniques such as adhesive hyphal strands, adhesive knobs, adhesive nets formed from hyphal threads, loops of hyphae which tighten round any ensnared nematodes and non-constricting loops. When the nematode has been restrained, the hyphae penetrate the cuticle and the internal tissues of the nematode are devoured. [5]

Arthrobotrys oligospora , a net-building species of fungus, can detect the presence of nematodes nearby in the soil and only builds its snares when they are present. This is presumably because building the net is a highly energy-consuming process; the fungus is alerted to the presence of the nematode by detecting the pheromones, such as ascarosides, with which the worms communicate. The fungus takes active steps to attract its prey by producing olfactory cues that mimic those used by the worm to find food and attract mates. [3] Arthrobotrys dactyloides is a species that employs a loop of hypha to catch nematodes; when one tries to pass through the ring, the loop constricts with great rapidity, trapping the prey. [6]

The hyphae of shaggy ink caps attack nematodes Schopftintling-Coprinus-comatus.jpg
The hyphae of shaggy ink caps attack nematodes
Juvenile root-knot nematode (Meloidogyne incognita) penetrating a tomato root A juvenile root-knot nematode (Meloidogyne incognita) penetrates a tomato root - USDA-ARS.jpg
Juvenile root-knot nematode ( Meloidogyne incognita ) penetrating a tomato root

Some nematophagous fungi produce toxic substances which immobilise nematodes. For example, the hypha of the shaggy ink cap (Coprinus comatus) attacks the free-living soil nematode Panagrellus redivivus with a structure known as a spiny ball; this is used to damage the nematode cuticle to enable immobilisation, after which the hypha pierces the skin and digests the contents. [7]

Most endoparasitic fungi have spores that are attracted to soil nematodes and tend to congregate in the mouth region. Having penetrated the cuticle, the hyphae grow throughout the nematode, absorbing its tissues. Escape tubes emerge from these and grow through the cuticle, and in due course, further motile spores exit through these, ready to infect other nematodes. In other species of fungi, it is conidia rather than spores which are encountered by the nematode and infect it in a similar way. [8] In the case of Harposporium anguillulae , the sickle-shaped conidia are ingested by the nematode and lodge in the oesophagus or gut from where they invade the tissues. [9]

In ovoparasitic species, the hypha flattens itself against an egg, appressoria indicating that infection is imminent or underway. It then pierces the choroid and devours the embryonic nematode before producing conidiophores and moving on to nearby eggs. [10]

Biological control

Some species of nematophagous fungi are being investigated for use in biological pest control. Purpureocillium lilacinum , for example, infests the plant-parasitic Meloidogyne incognita , which attacks the roots of many cultivated plants. Trials have provided varying results, with some strains being aggressive and others less pathogenic, and some strains that appeared promising in the lab proved ineffective in the field. [11] Arthrobotrys dactyloides shows promise at controlling the cosmopolitan plant-parasitic root-knot nematode Meloidogyne javanica . [6]

Related Research Articles

<span class="mw-page-title-main">Ascomycota</span> Division or phylum of fungi

Ascomycota is a phylum of the kingdom Fungi that, together with the Basidiomycota, forms the subkingdom Dikarya. Its members are commonly known as the sac fungi or ascomycetes. It is the largest phylum of Fungi, with over 64,000 species. The defining feature of this fungal group is the "ascus", a microscopic sexual structure in which nonmotile spores, called ascospores, are formed. However, some species of Ascomycota are asexual and thus do not form asci or ascospores. Familiar examples of sac fungi include morels, truffles, brewers' and bakers' yeast, dead man's fingers, and cup fungi. The fungal symbionts in the majority of lichens such as Cladonia belong to the Ascomycota.

<span class="mw-page-title-main">Hypha</span> Long, filamentous structure in fungi and Actinobacteria

A hypha is a long, branching, filamentous structure of a fungus, oomycete, or actinobacterium. In most fungi, hyphae are the main mode of vegetative growth, and are collectively called a mycelium.

<i>Coprinus comatus</i> Species of fungus

Coprinus comatus, commonly known as the shaggy ink cap, lawyer's wig, or shaggy mane, is a common fungus often seen growing on lawns, along gravel roads and waste areas. The young fruit bodies first appear as white cylinders emerging from the ground, then the bell-shaped caps open out. The caps are white, and covered with scales—this is the origin of the common names of the fungus. The gills beneath the cap are white, then pink, then turn black and deliquesce ('melt') into a black liquid filled with spores. This mushroom is unusual because it will turn black and dissolve itself in a matter of hours after being picked or depositing spores.

This is a glossary of some of the terms used in phytopathology.

Hyphomycetes are a form classification of fungi, part of what has often been referred to as fungi imperfecti, Deuteromycota, or anamorphic fungi. Hyphomycetes lack closed fruit bodies, and are often referred to as moulds. Most hyphomycetes are now assigned to the Ascomycota, on the basis of genetic connections made by life-cycle studies or by phylogenetic analysis of DNA sequences; many remain unassigned phylogenetically.

<span class="mw-page-title-main">Pleurotaceae</span> Family of mushrooms

The Pleurotaceae are a family of small to medium-sized mushrooms which have white spores. The family contains 13 genera over 412 species. Members of Pleurotaceae can be mistaken for members of Marasmiaceae. Perhaps the best known member is the oyster mushroom, Pleurotus ostreatus.

<span class="mw-page-title-main">Orbiliaceae</span> Family of fungi

The Orbiliaceae are a family of saprobic sac fungi. It is the only family in the monotypic class Orbiliomycetes and the monotypic order Orbiliales. The family was first described by John Axel Nannfeldt in 1932 and now contains 288 species in 12 genera. Members of this family have a widespread distribution, but are more prevalent in temperate regions. Some species in the Orbiliaceae are carnivorous fungi, and have evolved a number of specialized mechanisms to trap nematodes.

<i>Arthrobotrys</i> Genus of fungi

Arthrobotrys is a genus of mitosporic fungi in the family Orbiliaceae. There are 71 species. They are predatory fungi that capture and feed on nematode worms. Rings that form on the hyphae constrict and entrap the worms, then hyphae grow into the worm and digest it.

<i>Purpureocillium lilacinum</i> Species of fungus

Purpureocillium lilacinum is a species of filamentous fungus in the family Ophiocordycipitaceae. It has been isolated from a wide range of habitats, including cultivated and uncultivated soils, forests, grassland, deserts, estuarine sediments and sewage sludge, and insects. It has also been found in nematode eggs, and occasionally from females of root-knot and cyst nematodes. In addition, it has frequently been detected in the rhizosphere of many crops. The species can grow at a wide range of temperatures – from 8 to 38 °C for a few isolates, with optimal growth in the range 26 to 30 °C. It also has a wide pH tolerance and can grow on a variety of substrates. P. lilacinum has shown promising results for use as a biocontrol agent to control the growth of destructive root-knot nematodes.

<i>Zoophagus</i> Genus of fungi

Zoophagus is a genus of zygomycete fungi that preys on rotifers and nematodes. It was established in 1911 by Sommerstorff, who originally considered it to be an oomycete. It is common in a variety of freshwater habitats, such as ponds and sewage treatment plants.

Charles Drechsler was an American mycologist with 45 years of research with the United States Department of Agriculture. He spent considerable time working with cereal fungal diseases, and the genus Drechslera was named after him. Drechsler also worked extensively on oomycete fungi and their interactions with vegetable plants. Drechsler was recognized as a leading authority on helminthosporia, oomycetes, and other parasitic fungi.

<i>Harposporium anguillulae</i> Species of fungus

Harposporium anguillulae is a member of the genus Harposporium. It is an endoparasitic nematophagous fungus that attacks nematodes and eelworms and is isolated commonly from field and agricultural soils as well as used as an experimental organism in the laboratory.

<i>Arthrobotrys oligospora</i> Species of fungus

Arthrobotrys oligospora was discovered in Europe in 1850 by Georg Fresenius. A. oligospora is the model organism for interactions between fungi and nematodes. It is the most common nematode-capturing fungus, and most widespread nematode-trapping fungus in nature. It was the first species of fungi documented to actively capture nematodes.

Dactylellina haptotyla is a common soil-living fungus that develops structures to capture nematodes as nutrient source. In the presence of nematodes, spores can germinate into sticky knobs or non-constricting loops. The fungus traps nematodes with sticky knobs and non-constricting loops, then breakdown the cuticle, and penetrates the body of nematodes to obtain nutrients. For its predatory nature, Dactylellina haptotyla is also considered as nematode-trapping fungus or carnivorous fungus.

Arthrobotrys dactyloides is a species of fungus in the family Orbiliaceae. It is nematophagous, forming loops of hypha to trap nematodes, on which it then feeds.

Stylopage is a polytypic genus of predacious fungus in the order Zoopagales, within the subphylum Zoopagomycotina. All known species of Stylopage subsist on various species of amoebae or nematodes by trapping their prey, typically using an adhesive substance that coats their vegetative hyphae, and absorbing nutrients through the projection of a haustorium. 17 extant Stylopage species have been described thus far.

Birgit Ann-Marie Margareta Nordbring-Hertz, was a Swedish scientist at Lund University known for her work on the interactions between fungi and nematodes.

<i>Funneliformis mosseae</i> Species of fungus

Funneliformis mosseae is a species of fungus in the family Glomeraceae, which is an arbuscular mycorrhizal (AM) fungi that forms symbiotic relationships with plant roots. Funneliformis mosseae has a wide distribution worldwide, and can be found in North America, South America, Europe, Africa, Asia and Australia. Funneliformis are characterized by having an easily visible septum in the area of the spore base and are often cylindrical or funnel-shaped. Funneliformis mosseae similarly resembles Glomus caledonium, however the spore wall of Funneliformis mosseae contains three layers, whereas Gl. caledonium spore walls are composed of four layers. Funneliformis is an easily cultivated species which multiplies well in trap culture, along with its high distribution, F. mosseae is not considered endangered and is often used for experimental purposes when combined with another host.

Meristacrum is a fungal genus in the monotypic family Meristacraceae, of the order Entomophthorales. They are parasites of soil invertebrates, they typically infect nematodes, and tardigrades.

Arthrobotrys musiformis is a species of nematode catching fungi, genus Arthrobotrys. This, like other Arthrobotrys species, captures and feeds on nematodes. It is widespread, with its initial discovery being in Norfolk, Virginia. This species demonstrates promising anti-helminth potential, and is hypothesized to reduce the number of parasitic nematodes in plants and livestock as either a biocontrol or through isolating metabolites.

References

  1. Thorn, R. Greg; Moncalvo, Jean-Marc; Reddy, C. A.; Vilgalys, Rytas (2000). "Phylogenetic Analyses and the Distribution of Nematophagy Support a Monophyletic Pleurotaceae within the Polyphyletic Pleurotoid-Lentinoid Fungi". Mycologia. 92 (2): 241–252. doi:10.2307/3761557. JSTOR   3761557.
  2. Nordbring-Hertz, Birgit; Jansson, Hans-Börje; Tunlid, Anders (2011). "Nematophagous fungi". eLS. doi:10.1002/9780470015902.a0000374.pub3. ISBN   9780470016176.
  3. 1 2 Hsueh, Yen-Ping; Gronquist, Matthew R.; Schwarz, Erich M.; Nath, Ravi David; Lee, Ching-Han; Gharib, Shalha; Schroeder, Frank C.; Sternberg, Paul W. (2017). "Nematophagous fungus Arthrobotrys oligospora mimics olfactory cues of sex and food to lure its nematode prey". eLife. 6. doi: 10.7554/eLife.20023 . PMC   5243009 . PMID   28098555.
  4. 1 2 Zhang & Hyde 2014, pp. 2–8.
  5. Zhang & Hyde 2014, pp. 212–214.
  6. 1 2 Zhang & Hyde 2014, pp. 173–175.
  7. Luo, H.; Liu, Y.; Fang, L.; Li, X.; Tang, N.; Zhang, K. (2007). "Coprinus comatus Damages Nematode Cuticles Mechanically with Spiny Balls and Produces Potent Toxins to Immobilize Nematodes". Applied and Environmental Microbiology. 73 (12): 3916–3923. Bibcode:2007ApEnM..73.3916L. doi:10.1128/AEM.02770-06. PMC   1932715 . PMID   17449690.
  8. "Nematophagous fungi: part 1". World News. 13 March 2011. Retrieved 30 September 2017.
  9. Aschner, M.; Kohn, S. (1958). "The Biology of Harposporium anguillulae". Microbiology. 19 (1): 182–189. doi: 10.1099/00221287-19-1-182 . PMID   13575766.
  10. Money, N.P. (1998). "Mechanics of invasive fungal growth and the significance of turgor in plant infection". Molecular genetics of host-specific toxins in plant disease. Kluwer Academic Publishers. pp. 261–71.
  11. Jatala, P. (1986). "Biological control of plant-parasitic nematodes". Annual Review of Phytopathology. 24: 453–89. doi:10.1146/annurev.py.24.090186.002321.

Bibliography