Podospora appendiculata

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Podospora appendiculata
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Sordariomycetes
Order: Sordariales
Family: Podosporaceae
Genus: Podospora
Species:
P. appendiculata
Binomial name
Podospora appendiculata
(Auerswald ex Niessl) Niessl (1883)
Synonyms
  • Sordaria appendiculataAuersw. ex Niessl (1872)
  • Podospora fimiseda var. appendiculata(Auersw. ex Niessl) G.Winter (1885)
  • Pleurage appendiculata(Auersw. ex Niessl) C.Moreau (1953)
  • Sordaria winteri P.Karst. (1873)
  • Sphaeria amphicornis Ellis (1876)

Podospora appendiculata is a coprophilous fungus that is most commonly found in the dung of lagomorphs, such as hares and rabbits, in temperate to warm climates. [1] [2] [3] A member of the division Ascomycota, P. appendiculata is characterized by ovoid, hair-studded perithecia which can bear a distinctive violaceous colouring and peridia which are coriaceous, or leathery, in texture. [1] [4] Podospora appendiculata has been shown to produce three compounds (Appenolide A, Appenolide B, and Appenolide C) with antimicrobial properties. [5]

Contents

History and taxonomy

The fungus was first collected by the German mycologist Bernhard Auerswald from hare dung found near the German city of Leipzig. [6] Auerswald sent a sample in a letter to Gustav Niessl von Mayendorf, who published a description of the species under the name Sordaria appendiculata in 1872 before reclassifying it under the genus Podospora in 1883. [6] [7]

Contesting Auerswald and Niessl's work, Heinrich Georg Winter later argued in 1885 that the fungus was merely a variant of the species Podospora fimiseda with smaller spores. [7] Winter's assessment was supported by George Edward Massee and Ernest Stanley Salmon, but, upon closer examination in 1934, the Canadian mycologist R. F. Cain agreed with Niessl and set Podospora appendiculata apart as its own species. [7] The cylindrical or conical appearance of the pedicel (an uncoloured, cytoplasm-filled appendage attached to each ascospore) in P. appendiculata allows it to be distinguished easily from P. fimiseda, whose pedicels are club-like in shape. [7]

Podospora appendiculata was also discovered independently slightly after Auerswald in 1873 by the Finnish mycologist Petter Adolf Karsten, who classified it as Sordaria winteri, and in 1876 by Job Bicknell Ellis who classified it under the name Sphaeria amphicornis. [8]

Habitat and ecology

Podospora appendiculata is a coprophilous fungus that grows on the dung of many herbivorous animals but is most strongly associated with the dung of lagomorphs, a group which includes hares and rabbits. [2] [3] [4] While it has been recovered from the dung of horses and cows, Podospora appendiculata tends only to appear in excrement found in forests. [4] In more domesticated settings, such as pastures as fields, P. appendiculata is considerably more scarce. [4] The fungus grows widely in temperate to warm climates, and has been identified naturally in New Zealand, Israel, Japan, Brazil, and in areas throughout North America and Europe. [1] [9] [10]

Evidence also exists for an antagonistic relationship between P. appendiculata and certain other coprophilous species. Analysis of 137 global dung samples recovered from nations such as England, Scotland, Yugoslavia and New Zealand revealed a statistically significant negative association between the incidence of P. appendiculata and the occurrence of Ascobolus immersus, Lasiobolus ciliatus, and Podospora curvula. [2]

Morphology

Podospora appendiculata produces perithecia, necked fruiting bodies laden with sexual spores. [1] Unlike perithecia obtained from other ascomycota, however, perithecia from P. appendiculata lack very prominent necks. [1] Its perithecia are ovoid, appear blackish to purplish, have hyaline (uncolored) tips, and are covered evenly with short, stiff hairs. [1] [4] These hairs are wide and brown at the base, and, like the perithecia, have hyaline, uncoloured tips. [11]

The peridium, or outer covering, of each perithecium possesses a coriaceous (leathery) texture and can have a violaceous colouring. [1] Such colouring is very rare amongst coprophilous pyrenomycetes, and in this manner P. appendiculata is similar to two other fungal species both belonging to the genus Cercophora: Cercophora septentrionalis and Cercophora caerulea. [1] [4]

As with other members of the ascomycota, the perithecia of P. appendiculata are filled with asci (singular: ascus) that contain, in turn, the sexual ascospores. [1] Each ascus is clavate (club-like) in shape, [10] possesses a small apical ring, and contains 8 ascospores arranged in a biseriate (two-rowed) manner. [1] [9] [11] In contrast to other members of the genus Podospora, the ascospores of P. appendiculata bunch together in the middle of each ascus instead of spreading out through the entire enclosure evenly. [4]

While early on in development each ascospore is clavate and hyaline, they become dark in colouring and ellipsoid in shape as they mature. [11] Ascospores all have incredibly sticky, gelatinous, tail-like appendages called caudae, [1] a pedicel that is cylindrical to conical in shape, [7] and a singular germ pore through which future germination will occur. [9]

Growth

Growth of the fungus on corn meal agar is slow, with only 7-8 millimeters of growth observed after 1 month. [1] The hyphae, or filamentous strands, that characterize the vegetative phase of the fungus become funiculose, weaving together to form rope-like strands. [11] [12] Sparse white aerial hyphae can also develop as the fungus is cultured. [1] [11]

Ordinarily, the teleomorph, or sexual stage, of P. appendiculata can be difficult to obtain in vitro. However, perithecial development can be stimulated through the addition of steam-sterilized rabbit dung to the corn meal agar plate. [1] The developmental process is still slow, with 4 months needed for growth, but the perithecia obtained with steam-sterilized dung in vitro are identical morphologically to those obtained from the wild. [1]

While its violaceous colouring is already reminiscent of species belonging to the genus Cercophora, [1] Podospora appendiculata bears further similarity to Cercophora in that its spores are able to germinate in their hyaline, immature phase. [4] Although spores are never naturally released when immature, such a feature is still highly unusual among species belonging to the genus Podospora, with only the spores of P. fimiseda being similarly capable. [4]

Production of antimicrobial compounds

Coprophilous fungi have been known to competitively interfere with other fungi, producing chemical agents that impair the ability of rival species to access resources. [13] There is evidence to suggest that slower-growing fungi, such as Poronia punctata, employ antagonistic strategies more often in order to hamper the reproductive potential of quicker-growing fungi in dung. [13] Podospora appendiculata, itself a slow-growing fungus, has likewise been shown to produce three molecules with antimicrobial properties: Appenolide A, Appenolide B, and Appenolide C. [5] Each molecule is a 2(5H)-furanone. [5]

Appenolides A, B, and C display microbicidal activity against a variety of fungi, with 150 micrograms of each compound enough to produce 12-14  millimeter zones of inhibition against Candida albicans in standard disc assays. [5] Similar antifungal effects were noted with all Appenolides against the coprophilous fungi Sordaria fimicola and Ascobolus furfuraceous. [5]

Furthermore, Appenolides B and C exhibited additional antibacterial properties in disc assays against Bacillus subtilis . Zones of inhibition of 8 millimeters were noted at concentrations of 150 micrograms per disk. [5] The exact mechanisms of bacterial inhibition for Appenolides B and C remain unknown, but other 2(5H)-furanones appear to interfere with bacterial growth by blocking the activity of N-Acyl homoserine lactones and autoinducer 2 (AI-2), signalling molecules that help mediate quorum sensing. [14] [15]

Quorum sensing, a process which allows for differential gene expression in response to changes in cell density, can trigger bacterial biofilm formation when bacteria are present in sufficiently high concentrations. [15] Biofilm formation in turn drives resistance to a range of environmental and biological stressors, including antibiotics and human immune responses, and the 2(5H)-furanone-mediated disruption of quorum sensing has been shown to negatively impact the growth rate of Campylobacter jejuni , a clinically significant food-borne pathogen. [15] 2(5H)-furanone derivatives have also demonstrated in vitro bactericidal effects against Mycobacterium tuberculosis and methicillin-resistant Staphylococcus aureus, two species that have demonstrated increased resistance to more traditional antibiotics. [16] [17]

Related Research Articles

<span class="mw-page-title-main">Ascus</span> Spore-bearing cell in ascomycete fungi

An ascus is the sexual spore-bearing cell produced in ascomycete fungi. Each ascus usually contains eight ascospores, produced by meiosis followed, in most species, by a mitotic cell division. However, asci in some genera or species can occur in numbers of one, two, four, or multiples of four. In a few cases, the ascospores can bud off conidia that may fill the asci with hundreds of conidia, or the ascospores may fragment, e.g. some Cordyceps, also filling the asci with smaller cells. Ascospores are nonmotile, usually single celled, but not infrequently may be coenocytic, and in some cases coenocytic in multiple planes. Mitotic divisions within the developing spores populate each resulting cell in septate ascospores with nuclei. The term ocular chamber, or oculus, refers to the epiplasm that is surrounded by the "bourrelet".

<i>Sordaria fimicola</i> Species of fungus

Sordaria fimicola is a species of microscopic fungus. It is commonly found in the feces of herbivores. Sordaria fimicola is often used in introductory biology and mycology labs because it is easy to grow on nutrient agar in dish cultures. The genus Sordaria, closely related to Neurospora and Podospora, is a member of the large class Sordariomycetes, or flask-fungi. The natural habitat of the three species of Sordaria that have been the principal subjects in genetic studies is dung of herbivorous animals. The species S. fimicola is common and worldwide in distribution. The species of Sordaria are similar morphologically, producing black perithecia containing asci with eight dark ascospores in a linear arrangement. These species share a number of characteristics that are advantageous for genetic studies. They all have a short life cycle, usually 7–12 days, and are easily grown in culture. Most species are self-fertile and each strain is isogenic. All kinds of mutants are easily induced and readily obtainable with particular ascospore color mutants. These visual mutants aid in tetrad analysis, especially in analysis of intragenic recombination.

<span class="mw-page-title-main">Coprophilous fungi</span> Fungi that grow on animal dung

Coprophilous fungi are a type of saprobic fungi that grow on animal dung. The hardy spores of coprophilous species are unwittingly consumed by herbivores from vegetation, and are excreted along with the plant matter. The fungi then flourish in the feces, before releasing their spores to the surrounding area.

<i>Sporormiella</i> Genus of fungi

Sporormiella is a genus of fungi in the phylum Ascomycota whose species can be found worldwide, including the Arctic. It grows primarily on dung but also can be found in soil and plant debris. The exact number of species is debated and can range from 60 to 80 in total depending on the source. A majority of these species are coprophilous, however, there are a few that are endophytes and saprobic.

<i>Podospora</i> Genus of fungi on the family Podosporaceae

Podospora is a genus of fungi in the family Podosporaceae. Fossils of Podospora have been reported from 12 million year old rocks from central England.

Polytolypa is a monotypic genus of fungus containing the single species Polytolypa hystricis. First classified in the Onygenaceae family, as of 2008 it is considered to be in the Ajellomycetaceae, although there is still uncertainty as to its phylogenetic relationships with other similar genera. This species is only known from a single specimen derived in the laboratory from a specimen of dung of the North American porcupine, Erethizon dorsatum, collected in Ontario, Canada. Polytolypa hystricis contains bioactive compounds that have antifungal activity.

<i>Psilocybe hispanica</i> Species of fungus in the family Hymenogastraceae

Psilocybe hispanica is a species of fungus in the family Hymenogastraceae. It produces small brown mushrooms with conical to convex caps up to 10 mm (0.4 in) in diameter and stems 16 to 25 mm long by 0.5 to 1 mm thick. Reported as new to science in 2000, it is only known from the Pyrenees mountain range in northern Spain and southwestern France, where it grows on horse dung in grass fields at elevations of 1,700 to 2,300 m. The mushroom contains the psychoactive compound psilocybin. The possible depiction of this species in the 6,000-year-old Selva Pascuala rock art suggests that it might have been used in ancient religious rituals—the oldest evidence of such usage in prehistoric Europe.

Psilocybe tasmaniana is a species of coprophilous agaric fungus in the family Hymenogastraceae. It was described by Gastón Guzmán and Roy Watling in 1978 as a small tawny orange mushroom that grows on dung, with a slight blueing reaction to damage, known only from Tasmania and southeastern Australia. It was likened to Psilocybe subaeruginosa although characteristics, appearance, and the association with dung were not typical for that species. As a blueing member of the genus Psilocybe it contains the psychoactive compounds psilocin and psilocybin.

<i>Podospora anserina</i> Species of fungus

Podospora anserina is a filamentous ascomycete fungus from the order Sordariales. It is considered a model organism for the study of molecular biology of senescence (aging), prions, sexual reproduction, and meiotic drive. It has an obligate sexual and pseudohomothallic life cycle. It is a non-pathogenic coprophilous fungus that colonizes the dung of herbivorous animals such as horses, rabbits, cows and sheep.

Collariella bostrychodes is a fungal decomposer of lignin and carbohydrate in the family Chaetomiaceae commonly found in soil and dung. The fungus is distinguished by a darkened collar-like ostiole around the ostiolar pore, giving the fungus its name. The fungus is highly variable in shape and form, giving raise to the belief that there are two subclades in the species. The ascospores range from lemon-shaped to nearly spherical with slightly pointed ends. It can grow to be pale green and later turn pale bluish grey or olivaceous with age. The fungus produces the toxic secondary metabolite, chaetochromin.

Botryotrichum piluliferum is a fungal species first identified in 1885 by Saccardo and Marchal. It was discovered to be the asexual state of a member of the ascomycete genus, Chaetomium. The name B. piluliferum now applies to the fungus in all its states. B. piluliferum has been found worldwide in a wide range of habitats such as animal dung and vegetation. The colonies of this fungus start off white and grow rapidly to a brown colour. The conidia are smooth and white. B. piluliferum grows optimally at a temperature of 25–30 °C and a pH of 5.5.

<i>Myxotrichum chartarum</i> Species of fungus

Myxotrichum chartarum is a psychrophilic and cellulolytic fungus first discovered in Germany by Gustav Kunze in 1823. Its classification has changed many times over its history to better reflect the information available at the time. Currently, M. chartarum is known to be an ascomycete surrounded by a gymnothecium composed of ornate spines and releases asexual ascospores. The presence of cellulolytic processes are common in fungi within the family Myxotrichaceae. M. chartarum is one of many Myxotrichum species known to degrade paper and paper products. Evidence of M. chartarum "red spot" mold formation, especially on old books, can be found globally. As a result, this fungal species and other cellulolytic molds are endangering old works of art and books. Currently, there is no evidence that suggests that species within the family Myxotrichaceae are pathogenic.

Zopfiella ebriosa is an unharmful fungus discovered covering the corks of wine bottles in 1991 in Tarragona, Spain. A member of the division Ascomycota, Zopfiella ebriosa is characterized by small and asymmetrical asci, presence of ostioles, and possession of germ slits.

Triangularia setosa is a member of the Ascomycota, and of the genus Triangularia. This genus is notable for its widespread appearance on the excrement of herbivores, and is therefore seen as a coprophilous fungus. The fungus itself is characteristically dark in colour and produces sac-like perithecium with a covering of hair. Its dispersion involves the ingestion, passage, and projectile ejection of spores. It has preference for colonizing the dung of lagomorphs, such as hares and rabbits.

Ascodesmis nigricans is a coprophilous fungus that could be isolated from the dung of various animals. It was firstly introduced by Philippe Édouard Léon Van Tieghem, a French botanist, and was the type species of the genus Ascodesmis. It is an uncommon species but its development of the fruit body has been the subject of much laboratory study due to the easy nature of its cultivation. Ascodesmis nigricans is not pathogenic to human, animals or plants. This species has world-wide distribution.

Anopodium ampullaceum is a species of fungus first discovered by Nils Lundqvist in Sweden, in the year 1964. A. ampullaceum became one of the first few fungi along with Anopodium epile and Podospora dagonerii, to be placed in the new genus Anopodium due to their unique spores that did not suit the description of the spores of the Podospora genus, which P. dagonerii had previously belonged to. The genus Anopodium deviates from other members of the Sordariomycetes class by two spore characteristics; firstly the pedicels of its spore in the apical position, and secondly due to its immature spores having spherical bodies with cylindrical apical regions. As of 1998 all three of these species are now considered to be one species, using the name A. ampullaceum.

Cercophora areolata is a member of the Ascomycota division, and is grouped into the Lasiosphaeriaceae family based on morphology. C. areolata is a coprophilous fungus that has been most recently isolated from porcupine dung. Defining features of C. areolata include: 1) ovoid-conical, glabrous ascomata, 2) black, carbonaceous, areolate peridium and 3) clavate-shaped, single-walled asci. From studies on C. areolata, this fungus produces multiple antifungal compounds, which inhibit other competitor fungi.

Ostropomyces is a genus of fungi in the family Stictidaceae. It has two species, both of which are found in tropical forests in northern Thailand, where they grow as saprotrophs on bark.

Savoryella is a genus of freshwater and marine based fungi in the family Savoryellaceae and the order Savoryellales.

Zwackhiomacromyces is a genus of lichenicolous (lichen-dwelling) fungi in the family Xanthopyreniaceae. It has two species. The genus is distinguished by its black, pear-shaped fruiting bodies with large, nipple-shaped ostioles that have a granular surface, and a dark, multi-layered wall made up of hyphal cells forming a pseudoparenchymatous structure. The genus is closely related to the similarly named genus Zwackhiomyces.

References

  1. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Bell, A.; Mahoney, D. P. (November 1997). "Coprophilous Fungi in New Zealand. II. Podospora Species with Coriaceous Perithecia". Mycologia. 89 (6): 908. doi:10.2307/3761111. JSTOR   3761111.
  2. 1 2 3 Richardson, M.J. (January 1972). "Coprophilous ascomycetes on different dung types". Transactions of the British Mycological Society. 58 (1): 37–48. doi:10.1016/S0007-1536(72)80069-X.
  3. 1 2 Parker, Alan D. (11 June 1979). "Associations Between Coprophilous Ascomycetes and Fecal Substrates in Illinois". Mycologia. 71 (6): 1206–1214. doi:10.1080/00275514.1979.12021132.
  4. 1 2 3 4 5 6 7 8 9 Lundqvist, Nils (1972). Nordic Sordariaceae s. lat. Uppsala, Sweden: Almqvist & Wiksells Boktryckeri. pp. 26–27, 128–135.
  5. 1 2 3 4 5 6 Wang, Yong; Gloer, James B.; Scott, James A.; Malloch, David (March 1993). "Appenolides A-C: Three New Antifungal Furanones from the Coprophilous Fungus Podospora appendiculata". Journal of Natural Products. 56 (3): 341–344. doi:10.1021/np50093a005. PMID   8482945.
  6. 1 2 Niessl von Mayendorf, Gustav (1870). "Sordaria appendiculata". Verhandlungen des naturforschenden Vereines in Brünn. 10: 188–189.
  7. 1 2 3 4 5 Moreau, Claude (1953). Les Genres Sordaria et Pleurage. Paris: Paul Lechevalier. pp. 246–247.
  8. ↑ "Podospora appendiculata". www.mycobank.org. Retrieved 16 November 2019.
  9. 1 2 3 Mirza, J. H.; Cain, R. F. (December 1969). "Revision of the genus Podospora". Canadian Journal of Botany. 47 (12): 1999–2048. doi:10.1139/b69-293.
  10. 1 2 Melo, RFR; Miller, AN; Maia, LC (2015). "The genus Podospora (Lasiosphaeriaceae, Sordariales) in Brazil". Mycosphere. 6 (2): 201–215. doi: 10.5943/mycosphere/6/2/10 .
  11. 1 2 3 4 5 Furuya, Kouhei; Udagawa, Shun-Ichi (1972). "Coprophilous Pyrenomycetes From Japan I". The Journal of General and Applied Microbiology. 18 (6): 433–454. doi: 10.2323/jgam.18.433 .
  12. ↑ Uecker, F. A. (January 1976). "Development and Cytology of Sordaria humana". Mycologia. 68 (1): 30–46. doi:10.2307/3758895. JSTOR   3758895.
  13. 1 2 Wicklow, Donald T.; Hirschfield, B. J. (July 1979). "Evidence of a competitive hierarchy among coprophilous fungal populations". Canadian Journal of Microbiology. 25 (7): 855–858. doi:10.1139/m79-126. PMID   476559.
  14. ↑ Ponnusamy, K; Paul, D; Sam Kim, Y; Kweon, JH (January 2010). "2(5H)-Furanone: A Prospective strategy for biofouling-control in membrane biofilm bacteria by quorum sensing inhibition". Brazilian Journal of Microbiology. 41 (1): 227–34. doi:10.1590/S1517-83822010000100032. PMC   3768598 . PMID   24031485.
  15. 1 2 3 Castillo, Sandra; Heredia, Norma; García, Santos (18 September 2014). "2(5H)-Furanone, epigallocatechin gallate, and a citric-based disinfectant disturb quorum-sensing activity and reduce motility and biofilm formation of Campylobacter jejuni". Folia Microbiologica. 60 (1): 89–95. doi:10.1007/s12223-014-0344-0. PMID   25231135. S2CID   2415460.
  16. ↑ Ngwane, Andile H.; Panayides, Jenny-Lee; Chouteau, Franck; Macingwana, Lubabalo; Viljoen, Albertus; Baker, Bienyameen; Madikane, Eliya; de Kock, Carmen; Wiesner, Lubbe; Chibale, Kelly; Parkinson, Christopher J.; Mmutlane, Edwin M.; van Helden, Paul; Wiid, Ian (August 2016). "Design, synthesis, and In vitro antituberculosis activity of 2(5H)‐Furanone derivatives antituberculosis activity of 2(5 )-Furanone derivatives". IUBMB Life. 68 (8): 612–620. doi: 10.1002/iub.1526 . PMID   27346745.
  17. ↑ Sharafutdinov, Irshad S.; Trizna, Elena Y.; Baidamshina, Diana R.; Ryzhikova, Maria N.; Sibgatullina, Regina R.; Khabibrakhmanova, Alsu M.; Latypova, Liliya Z.; Kurbangalieva, Almira R.; Rozhina, Elvira V.; Klinger-Strobel, Mareike; Fakhrullin, Rawil F.; Pletz, Mathias W.; Bogachev, Mikhail I.; Kayumov, Airat R.; Makarewicz, Oliwia (20 November 2017). "Antimicrobial Effects of Sulfonyl Derivative of 2(5H)-Furanone against Planktonic and Biofilm Associated Methicillin-Resistant and -Susceptible Staphylococcus aureus". Frontiers in Microbiology. 8: 2246. doi: 10.3389/fmicb.2017.02246 . PMC   5701942 . PMID   29209288.
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