Arthrobotrys oligospora

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Arthrobotrys oligospora
20100828 005957 Fungus.jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Orbiliomycetes
Order: Orbiliales
Family: Orbiliaceae
Genus: Arthrobotrys
Species:
A. oligospora
Binomial name
Arthrobotrys oligospora
Fresen. (1850)
Synonyms
  • Orbilia auricolor (A. Bloxam) Sacc. (1889)
  • Arthrobotrys superba var. oligospora (Fresen.) Coemans (1863)
  • Didymozoophaga oligospora (Fresen.) Soprunov & Galiulina (1951)

Arthrobotrys oligospora was discovered in Europe in 1850 by Georg Fresenius. [1] [2] A. oligospora is the model organism for interactions between fungi and nematodes. [2] It is the most common nematode-capturing fungus, [3] [4] [5] and most widespread nematode-trapping fungus in nature. [2] [6] It was the first species of fungi documented to actively capture nematodes. [2] [6]

Contents

Growth and morphology

This fungus reproduces by means of two-celled, pear-shaped conidia, in which the cells are of unequal size with the smaller cell nearer to the attachment point on the conidiophore. [4] [7] During germination, the germ tube typically erupts from the smaller cell. [7] In environments rich with nematodes, the spores range from 22-32 by 12-20 μm, [4] [7] though the spores are smaller in environments devoid of nematodes. [4] [7] Conidium germination has a success rate of 100% but the formation of trapping organs are not always observed. [6] Conidia have been found to disintegrate both in the air and on impact with an agar plate. [8] Conidiophores and conidia grow from hyphae sprouted outside of a trapped dead nematode, [2] and conidiophores have been found to change and grow into part of the adhesive net. [2] Under ideal conditions, a colony can reach 65 mm in diameter after seven days incubation, [6] with colourless, pale pink or yellow mycelium. [6] The optimal growth temperature for the fungus in nematode-free and nematode-infested environments is 20 °C (68 °F) and 25 °C (77 °F), respectively. [6] The growth rate of colonies is greater in the presence of light than in darkness. [6]

Physiology

Arthrobotrys oligospora is considered a saprobe and is more saprotrophic than other nematode capturing fungi. [2] [6] At first the fungus was considered largely saprophytic in nature but this interpretation was later questioned. [4] Saprophytic growth uses D-xylose, D-mannose, and cellobiose. [6] The fungus uses nitrite, nitrate, and ammonium for its nitrogen sources and uses pectin, cellulose, and chitin for its carbon sources. [6] When predating on nematodes, the fungus uses cellobiose, L-asparagine, L-arginine, DL glutamic acid for its carbon and nitrogen sources. [6]

Nematode capturing

Predation of nematodes occurs in low nitrogen environments, [9] as the nematode becomes the main nitrogen source for the fungi. [2] It has been found that the presence of ammonium causes a higher decrease of predation when compared to presence of nitrate or nitrite. [3] Adding green manure or carbohydrates has been found to increase nematode trapping behaviors. [6] A complex 3-dimensional net of hyphae is formed to trap the nematodes under conditions of pH 4.9-8.1 and a temperature less than 37 °C (99 °F). [5] [6] [8] [9] Nematodes, and specifically "nemin" (an extract derived from nematodes) were found to stimulate net formation. [2] [6] Nematodes are not as attracted to A. oligospora colonies that have not manifested traps, suggesting that these structures serve an additional attractant role possibly through the expression of pheromones. [9] [10] It is possible some of these pheromones, such as methyl 3-methyl-2-butenoate, evolved as olfactory mimicry. They may mimic and interfere with sex pheromones of some nematode species (in the above case, the pheromone interferes with Caenorhabditis elegans ). [11]

A full net is not needed to catch nematodes as smaller nematodes can be caught with a single loop. [2] Lectins are used in attaching nematode to fungi [9] The entire surface of net is covered in adhesive material. [2] [8] Strong adhesion keeps the nematode trapped and when the nematode struggles, it often results in multiple points of adhesion of the nematode to the net. [8] [10] It was even found that the adhesion of the nematode to the fungus remained under washing of agar plate with water. [8] The net is flexible which results in 'hyphal drag' tiring the nematode. [8] Multiple points of adhesion and 'hyphal drag' allow the net to be capable of catching both large and small nematodes easily. [8] In vitro, bait nematodes are consumed often leaving Bunonema nematodes. [8]

A substance found in paralyzed nematodes was found to be capable of paralyzing healthy nematodes, [6] [8] and it was later determined that a paralyzing substance, Subtilisin (A serine protease), [12] is excreted into nematodes. [2] [8] An unstable toxin was thought to be made by the fungus, [6] [8] and it was later found that toxic levels of linoleic acid for nematodes (lethal dose of linoleic acid for C. elegans is 5–10 μg/ml) [13] were found in the fungus. [5] [13] Enzymatic hyphal invasion, likely using collagenases which are found in 'Arthrobotrys', [2] of a trapped nematode is followed by the digestion of contents of the nematode. [8] [9] Shortly after hyphal invasion, a hyphal bulb appears where hyphae grow outwards from the bulb along the entire body of the nematode. [8]

Not all nematodes are caught by the net as the nematode needs to be in contact with the net for a short period of time in order for adhesion to occur. [8] Nematodes were found to quickly move away from any net followed by curling if instantaneous contact occurs. [8] [14] The nematode then proceeds to move forward until out of the area of the net and unless prolonged contact is made the nematode is safe. [8] This means one or several instantaneous contacts are not enough for adhesion between the nematode and net to occur. [8]

No competing fungi or bacteria are found in nematodes which are being consumed by the fungus which means it is possible an antibiotic is released inside the nematode. [8] In 1993, secondary metabolites (oligosporon, oligosporol A, and oligosporal B) which can act as antibiotics were found in the fungus. [2] [13] Oligosporon, oligosporol A, oligosporal B have hemolytic effects and are cytotoxic to nematodes, however they are not toxic to the C. elegans. [13] Other oligosporon-type secondary metabolites also found in A. oligospora include (4S,5R,6R)-4′,5′- dihydrooligosporon, (4S,5R,6R)-hydroxyoligosporon, and (4S,5R,6R)-10′11 ′-epoxyoligosporon. [13]

Net formation

A branch of hyphae grows out of a vegetative hyphae eventually arching back to the parent hyphae and fuses with it to make a loop. [3] [7] [8] This process repeats from any hyphae along any existing branches or a new parent hyphae. [3] [8] The nets are immediately adhesive, [8] and hyphae in the loop have different organelles to trap nematodes which are not found in vegetative cells. [2]

Habitat and ecology

Arthrobotrys oligospora has been found in many different geographical regions which include Asia, Africa, North America and South America and Australasia. [2] Some countries it has been found in include Turkmenistan, Azerbaijan, Poland, Canada, New Zealand, and India. [6] The presence of insects infected by nematodes increased presence of A. oligospora but not other nematode capturing fungi. [2]

The fungus can be found in soil in grassland, shrubland, plantations, sheep and cattle yards, [6] and domesticated and non-domesticated animal feces. [2] It colonizes forest steppe soil, mixed forest soil, and Mediterranean brown soil (pH 6.9-8.0) where the pH can be as low as 4.5, but is typically above 5.5. [6] The fungus has also been found in aquatic environments, [2] and heavily polluted areas, specifically heavy metal poisoned mines, fungicide, or nematicide infested soil, [2] [5] decayed plant material, leaves, roots, moss, [6] and in the rhizosphere of various bean plants, barley, [2] [6] and the tomato plant. [2] Larger populations of the fungus can be found in late spring and summer. [5]

Industrial uses

The fungus is a biological indicator of nematodes. [2] The annual global cost of plant-parasitic nematodes is approximately 100 billion USD. [13] Nematode capturing fungi such as the A. oligospora can be used to control growth of nematodes. [5] [6] This means that they can be potentially used as a bio-control agent to protect crops against nematode infestations. [2] This may not be feasible since the nematodes occasionally eat the fungi. [6]

References

  1. ↑ Fresenius, Georg (1850). Beiträge zur mykologie. p. 18.
  2. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Niu, Xue-Mei; Zhang, Ke-Qin (2011). "Arthrobotrys oligospora a model organism for understanding the interaction between fungi and nematodes". Mycology. 2 (2): 59–78. doi: 10.1080/21501203.2011.562559 .
  3. 1 2 3 4 Duddington, C; Wyborn, C (1972). "Recent Research on the Nematophagous Hyphomycetes". Botanical Review. 38 (4): 545–562. Bibcode:1972BotRv..38..545D. doi:10.1007/bf02859251. S2CID   29933497.
  4. 1 2 3 4 5 Dreschler, Charles (1937). "Some Hyphomycetes That Prey on Free-Living Terricolous Nematodes". Mycologia. 29 (4): 447–552. doi:10.2307/3754331. JSTOR   3754331.
  5. 1 2 3 4 5 6 Zhang, Ke-Qin; Hyde, Kevin; Zhang, Ying; Yang, Jinkui; Li, Guo-Hang (2014). Nematode-trapping Fungi. New York: Dordrecht: Springer. pp. 213, 215, 222, 316.{{cite book}}: CS1 maint: publisher location (link)
  6. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 Domsch, Klaus; Gams, Walter; Traute-Heidi, Anderson (1980). Compendium of soil fungi. New York: Academic Press (London) LTD. pp. 60–63.
  7. 1 2 3 4 5 Duddington, C (1955). "Fungi That Attack Microscopic Animals". Botanical Review. 21 (7): 377–439. Bibcode:1955BotRv..21..377D. doi:10.1007/bf02872434. S2CID   37392081.
  8. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 Barron, George (1977). The Nematode-Destroying Fungi. Guelph: Canadian Biological Publications Ltd. pp. 27–37, 93–95, 106, 111.
  9. 1 2 3 4 5 Alexopoulos, Constantine; Mims, Charles; Blackwell, Meredith (1996). Introductory Mycology (4th ed.). Toronto: John Wiley & Sons, Inc. p. 235.
  10. 1 2 Nordbring-Hertz, Birgit; Jansson, Hans-Börje; Stålhammar-Carlemalm, Margaretha (1977). "Interactions Between Nematophagous Fungi and Nematodes". Ecological Bulletins. 25: 483–484.
  11. ↑ Hsueh, Yen-Ping; Gronquist, Matthew R; Schwarz, Erich M; Nath, Ravi David; Lee, Ching-Han; Gharib, Shalha; Schroeder, Frank C; Sternberg, Paul W (2017-01-18). Hobert, Oliver (ed.). "Nematophagous fungus Arthrobotrys oligospora mimics olfactory cues of sex and food to lure its nematode prey". eLife. 6: e20023. doi: 10.7554/eLife.20023 . ISSN   2050-084X. PMC   5243009 . PMID   28098555.
  12. ↑ Nordbring-Hertz, Birgit (2004). "Morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora – an extensive plasticity of infection structures". Mycologist. 18 (3): 125–133. doi:10.1017/s0269915x04003052. S2CID   55590507.
  13. 1 2 3 4 5 6 Degenkolb, Thomas; Vilcinskas, Andreas (2016). "Metabolites from nematophagus fungi and nematicidal natural products from fungi as an alternative for biological control. Part 1: metabolites from nematophagous ascomycetes". Applied Microbiology and Biotechnology. 100 (9): 3799–3812. doi:10.1007/s00253-015-7233-6. PMC   4824826 . PMID   26715220.
  14. ↑ Dreschler, Charles (1934). "Organs of Capture in Some Fungi Preying on Nematodes". Mycologia. 26 (2): 135–144. doi:10.2307/3754035. JSTOR   3754035.
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