Arthrobotrys musiformis

Arthrobotrys musiformis (/aɹ.θɹoʊ'ba.tɹıs mju.sı'foɹ.mıs/) is a species of nematode catching fungi, genus Arthrobotrys (from Greek, meaning "jointed bunch of grapes"[1][2]). 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.[3][4][5]

Arthrobotrys musiformis
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Orbiliomycetes
Order: Orbiliales
Family: Orbiliaceae
Genus: Arthrobotrys
Species:
A. musiformis
Binomial name
Arthrobotrys musiformis
Synonyms
Synonymy
  • Candelabralla musiformis
  • Trichothesium musiformis

Taxonomy

Arthrobotrys musiformis is a fungus belonging to Orbiliomycetes within Ascomycota[6] that was described by Charles Drechsler in 1937.[7] The first samples came from rotting spinach plants in Norfolk, Virginia; with additional samples from Florida and Hawaii.[7] Synonyms for the fungi are Candelabralla musiformis and Trichothesium musiformis.[8][9]

Morphological taxonomy of Arthrobotrys places A. musiformis as most closely related to A. anchonia and A. dactyloids on the basis of their unbranched, non-nodular conidiophores. However, A. musiformis is unique from these species due to its 2 dimensional predatory structures while A. anchonia and A. dactyloids both produce constricting rings.[9]

Morphology

A drawing of conidia of Arthrobotrys musiformis based on the work of N.F. Gray and Karen Haard.[9][10]

A. musiformis has septate hyphae less than 5 µm in diameter that form branching[9] mycelium that may become very dense to catch nematodes with.[7][10] When kept as a colony, the colony is white and radial[9]

A drawing of adhesive nets of Arthrobotrys musiformis based on the work of N.F. Gray and Karen Haard.[9][10]

This fungi produces spores on curved, obvoid conidia that are 32 to 42 µm in length and 10 to 12 µm in width.[7] The conidia are developed in 1 to 2 weeks[9] on conidiophores that range between 250 and 375 µm long.[10] Following germination of conidia or production of nets, A. musiformis may produce chlamdospores 10-20 µm in diameter.[10] A. musiformis may be identified using its conidiaphores as they form a globalar, 'head' structure containing 5 to 15 conidia.[9]

To catch nematodes, the fungi produces 3 dimensional adhesive nets.[11] These adhesive nets can be used to identify A. musiformis from its close relatives, as many Arthrobotrys produce identifying, horseshoe like 2 dimensional rings.[9] The fungi forms nets with 2 to 7 loops 18-20 µm in inside diameter that connect back to the mycelium near where the net branched off.[10] These nets may capture nematodes by entangling them, though some studies suggest they are captured using strong adhesives on the net instead.[10] Following capture, the fungi may develop assimilative hyphae that grow into the nematode and digest it.[10]

Ecology

A. musiformis obtains nutrients through breaking down organic debris or capturing nematodes, known as saprotrophy and nematophagy respectively.[11] These two modes require the fungus to switch in lifestyle, which is accompanied by differential regulation of gene expression.[5] Some studies find that nematophagous fungi have limited impact on large scale ecological systems in California, though they caution that it is difficult to confidently reject fungi's involvement in processes such as the distribution of nematodes.[12]

In China, studies indicate that A. musiformis may be a dominant nematophagous fungi species in livestock fields, able to survive in soil and feces while continuing predacious and reproductive activity. The success of A. musiformis in this environment is estimated to be a result of lower nutritional costs, higher growing rates and greater reproductive ability in feces. While capable of surviving temperatures as low as 1 degree Celsius, the fungi performs best in wet, warm environments, with the greatest population being recorded in the rainy season at the end of summer. Likewise, the fungus did poorly during dry and cold weather at the end of winter[13]

Habitat

While the first description of A. musiformis described it as being distributed along the East Coast of the United States,[7] additional studies describe the distribution as ranging into Ireland, Canada, Denmark,[10] and China.[14]

Despite A. musiformis' nematophagous niche, it is outcompeted by other nematophagous fungi and instead performs better in environments where it can rely on saprotrophy as well.[9] In addition, it is resistant to some heavy metals, allowing it to survive in environments with fewer available nematodes or greater environmental toxins than its close relatives. As such, A. musiformis performs well in agricultural areas, where it may outcompete purely saprotrophic by consuming nematodes but also resist heavy metals common to those areas so they may outcompete other nematophagous fungi.[9]

Uses

Anti-helminth Potential

Nematodes are harmful to agriculture, costing the industry an excess of $100 billion (globally) annually.[6] Approximately 100 known species of nematode are economically relevant crop pests, with soil-borne nematodes causing the greatest losses.[6] Anti-helminth medicines have successfully combated infections, though resistance to these drugs is increasing, limiting the effectiveness of current treatments.[13]

A. musiformis produces multiple metabolites with potential as nematocides; including linoleic alcohol and desferriferrichrome. Both linoleic alcohol and desferriferrichrome are produced in higher concentrations when A. musiformis transitions to its predatory stage. Linoleic alcohol has limited nematodacidal activity, but one study proposes that it kills nematodes by transforming into linoleic acid which may oxidize linoleic alcohol found in the nematode. Desferriferrichrome belongs to a family of chemicals called siderophores that is used to uptake iron and may be used to kill nematodes.[5]

One study found that culture filtrate of A. musiformis colonies decreased the number of viable adult nematodes in lamb feces after being given orally, though the study concluded that the difference was not statistically significant, but encourages further research due to the benefit of finding a biocontrol option given the risks of contamination that come with chemical nematocides. This study, unlike many other studies in biocontrol, looks for potential uses for Arthrobotrys in treating animals directly rather than controlling nematodes at the level of substrate or fecal treatments.[4]

Another study finds a reduction of 97% in M. hapla nematodes on tomato plants following introduction of A. musiformis. The authors report that A. musiformis can suppress nematode infection in crop roots, with less damage occurring in the roots in treated plants at all measured dates and with anti-helminth activity surpassing that of synthetic treatments on day 30. Additionally, they conclude that further research into A. musiformis as a biocontrol agent is recommended as a means to significantly improve plant health while avoiding the contamination and off target effects of current pesticides.[3]

References

  1. "Botry-". Merriam Webster. Retrieved 23 March 2023.
  2. "Arthro-". Merriam Webster. Retrieved 23 March 2023.
  3. Purba RT, Fauzi F, Sari RW, Naibaho DC, Putri QA, Maulana A, Hastuti LD, Punnapayak H (July 2022). "Arthrobotrys thaumasia and Arthrobotrys musiformis as biocontrol agents against Meloidogyne hapla on tomato plant". Biodiversitas Journal of Biological Diversity. 23 (7). doi:10.13057/biodiv/d230743. S2CID 251260396.
  4. Angeles-Hernández S, Torres-Hernández G, Alonso-Díaz MA, von Son-de-Fernex E, Aguilar-Marcelino L, González-Garduño R, et al. (April 2021). "Effect of an Arthrobotrys musiformis (Fungi: Orbiliales) culture filtrate on the population of gastrointestinal parasitic nematode eggs in faeces of grazing lambs". Veterinary Parasitology, Regional Studies and Reports. 24: 100565. doi:10.1016/j.vprsr.2021.100565. PMID 34024381. S2CID 233598218.
  5. Kuo TH, Yang CT, Chang HY, Hsueh YP, Hsu CC (March 2020). "Nematode-Trapping Fungi Produce Diverse Metabolites during Predator-Prey Interaction". Metabolites. 10 (3): 117. doi:10.3390/metabo10030117. PMC 7143726. PMID 32245081.
  6. Degenkolb T, Vilcinskas A (May 2016). "Metabolites from nematophagous fungi and nematicidal natural products from fungi as an alternative for biological control. Part I: metabolites from nematophagous ascomycetes". Applied Microbiology and Biotechnology. 100 (9): 3799–3812. doi:10.1007/s00253-015-7233-6. PMC 4824826. PMID 26715220.
  7. Drechsler C (1937). "Some Hyphomycetes that Prey on Free-Living Terricolous Nematodes". Mycologia. 29 (4): 447–552. doi:10.1080/00275514.1937.12017222 via Taylor & Francis Online.
  8. "Arthrobotrys musiformis Drechsler". NBN Atlas. Retrieved 23 March 2023.
  9. Haard K (1968). "Taxonomic Studies on the Genus Arthrobotrys Corda". Mycologia. 60 (6): 1140–1159. doi:10.2307/3757214. JSTOR 3757214.
  10. Gray NF (1983). "Ecology of Nematophagous Fungi: Arthrobotrys musiformis, a Nematode-Destroying Fungus New to Ireland". Irish Journal of Agricultural Research. 22 (1): 107–111 via JSTOR.
  11. Pérez-Anzúrez G, Olmedo-Juárez A, von-Son de Fernex E, Alonso-Díaz MÁ, Delgado-Núñez EJ, López-Arellano ME, et al. (September 2022). "Arthrobotrys musiformis (Orbiliales) Kills Haemonchus contortus Infective Larvae (Trichostronylidae) through Its Predatory Activity and Its Fungal Culture Filtrates". Pathogens. 11 (10): 1068. doi:10.3390/pathogens11101068. PMC 9609027. PMID 36297125.
  12. Jaffee BA, Strong DR, Muldoon AE (1996). "Nematode-Trapping Fungi of a Natural Shrubland: Tests for Food Chain Involvement". Mycologia. 88 (4): 554–564. doi:10.2307/3761149. JSTOR 3761149.
  13. Su H, Hao Y, Mo M, Zhang K (March 2007). "The ecology of nematode-trapping hyphomycetes in cattle dung from three plateau pastures". Veterinary Parasitology. 144 (3–4): 293–298. doi:10.1016/j.vetpar.2006.10.012. PMID 17113711.
  14. Hao Y, Mo M, Su H, Zhang K (September 6, 2005). "Ecology of aquatic nematode-trapping hyphomycetes in southwestern China". Aquatic Microbial Ecology. 40 (2): 175–181. doi:10.3354/ame040175 via int-res.com.
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