Limnoperdon

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Limnoperdon
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Basidiomycota
Class: Agaricomycetes
Order: Agaricales
Family: Limnoperdaceae
G.A.Escobar (1976) [1]
Genus: Limnoperdon
G.A.Escobar (1976)
Type species
Limnoperdon incarnatum
G.A.Escobar (1976) [2]

Limnoperdon is a fungal genus in the monotypic family Limnoperdaceae. The genus is also monotypic, as it contains a single species, the aquatic fungus Limnoperdon incarnatum. The species, described as new to science in 1976, produces fruit bodies that lack specialized structures such as a stem, cap and gills common in mushrooms. Rather, the fruit bodies—described as aquatic or floating puffballs—are small balls (0.5–1 mm diameter) of loosely interwoven hyphae. The balls float on the surface of the water above submerged twigs. Experimental observations on the development of the fruit body, based on the growth on the fungus in pure culture, suggest that a thin strand of mycelium tethers the ball above water while it matures. Fruit bodies start out as a tuft of hyphae, then become cup-shaped, and eventually enclose around a single chamber that contains reddish spores. Initially discovered in a marsh in the state of Washington, the fungus has since been collected in Japan, South Africa, and Canada.

Contents

Taxonomy, classification and phylogeny

The family, genus and species were first described in a 1976 publication by graduate students Gustavo Escobar and Dennis McCabe, and undergraduate Craig Harpel who, in the fall of 1974, found the fungus as part of "a class project to find and isolate phycomycetes". [2] The holotype is located in the University of Washington Mycological Herbarium. An isotype (duplicate of the holotype specimen) is located in the Herbarium of the University of El Salvador in San Salvador. [2]

Pluteaceae

Pluteus petasatus

P. romellii

P. atromarginatus

Volvopluteus gloiocephalus

  Tricholomataceae  

Melanoleuca verrucipes

 Limnoperdaceae 

L. incarnatum

Cladogram indicating phylogeny of L. incarnatum and some related species in the Pluteoid clade, based on ribosomal DNA sequences; after Matheny et al., 2006: [3]

Limnoperdon incarnatum was originally thought to be associated with the Gasteromycetes, an artificial assemblage of species united by the fact that their spores mature inside the fruit bodies and are not forcibly discharged from the basidia. Other morphologically similar genera include the Gasterella of the family Gasterellaceae, and the Protogaster of the family Protogastraceae; however, it was excluded from these genera because of significant differences in spore color and structure, presence of clamp connections, and structure of the basidia. For these reasons the new family Limnoperdaceae was described to contain the new species, and it was classified along the Protogastraceae in the (now defunct) order Protogastrales. [2] More recently, molecular phylogenetics has been used to clarify the relationship Limnoperdon with other fungi. In 2001, David Hibbett and Manfred Binder established the membership of Limnoperdon incarnatum in the euagarics clade, a phylogenetically related group of species traditionally forming the order Agaricales. [4] Additional molecular studies have placed Limnoperdaceae in the pluteoid clade of the Agaricales, a grouping that includes the families Pluteaceae, Amanitaceae, and Pleurotaceae; [3] other studies that used comparisons of ribosomal DNA sequences placed Limnoperdon near the gilled genera Melanoleuca or Resupinatus , of the family Tricholomataceae. [5] [6] [7]

A 2007 field study that used molecular techniques to survey aquatic fungal taxa in a small springbrook in Valley Spring, Southern Ontario, Canada discovered many fungal taxa with high genetic affinity to Limnoperdon incarnatum, which suggests that a closely related species may also be common in streams. [8]

Description

Family description:

"Fructifications almost spherical, minute; peridium complex, with dendrophyses, indehiscent; gleba uniloculate, without invaginations; hymenium smooth; spores smooth."

Escobar, 1976 [2]

The genus description is similar to the family description, but further specifies that the fruit bodies float, are sometimes embedded in a loose subiculum (a woolly or net-like growth of hyphae), and that the spores are reddish. [2] The fungus has been described as an "aquatic puffball", [9] although a later review considered "floating puffball" to be a more apt descriptor. [10]

The fruit bodies of L. incarnatum are tiny, oval to roughly spherical, and measure 35–1250 by 200–450  μm. The floating balls are sometimes enclosed in a loose subiculum, with a whitish surface that is byssoid (consisting of fine threads). The peridium (the outer protective tissue layer) is 18–30 μm thick, byssoid, and made of clamped hyphae typically 2.5–4 μm in diameter intertwined with dendrophyses (irregularly branched cystidia) 1 μm in diameter. [2] The surface of the peridium is hydrophobic, a feature that helps keep water off the growing hymenium during its development, [11] and gives the fruit body buoyancy. [9]

The gleba is a single chamber, reddish in color, with a cavity that has an oblate spheroid shape. Initially empty, in maturity it is filled with spores that measure 330–1220 by 180–420 μm. The smooth inner surface of the chamber comprises the fertile spore-bearing tissue (the hymenium). The basidia (spore-bearing cells)—conspicuous when viewed under the microscope—are hyaline (translucent), more or less club-shaped, and usually have basal and apical swellings separated by a narrow strip of variable length. The basidia are four-spored, and have inflated sterigmata with a central constriction. The basidia measure 20–90 (typically 25–55) μm long by 8–10 μm thick. Reddish in mass, the spores are obovate (egg-shaped, with the broad extremity located away from the base), smooth, thick-walled, and measure 11–16 (typically 12–15) by 7–10 μm. They have a beaked pedicel that is 2–4 by 2–5 μm, and a basal germ pore. [2]

Habitat and distribution

The species was originally discovered floating in petri dishes that contained submerged hardwood twigs previously collected from a marsh next to a playground on the south shore of Lake Union in Seattle, Washington. After the initial 1976 publication, L. incarnatum was reported the following year when Keisuke Tubaki recovered it from wood blocks submerged in brackish water in Japan; [12] scientists Seiya Ito and T. Yokoyama later reported collecting it in Japanese rice paddy fields. [13] Later surveys uncovered the fungus in several localities in South Africa [14] and in freshwater ponds in Canada. [4] [15]

Development

Escobar grew cultures of the fungus by placing fresh fruit bodies on agar containing growth medium with an extract of horse dung. The tips of the hyphae were used to obtain axenic cultures; the fungus can grow on a variety of media commonly used to grow fungi in the laboratory. Depending on the composition of the growth media, fruit bodies were formed as early as eight days after initiating, when grown at 20 °C (68 °F) and under dim light. When minute agar blocks containing mycelium were submerged in distilled water, mycelial strands grew towards the water surface and eventually gave rise to floating fruit bodies connected to the parent agar block by strands of hyphae. [2]

Mycologist Dennis McCabe studied the development of the fruit body using specimens grown in pure culture. Starting out as a hyphal tuft, the fungus grows into a cup shape before eventually closing in completely to create the spherical structure of the mature fruit body. When the fungus is in the cup stage, the exposed hymenium is immature; typically, spores develop after the fruit body is fully closed. In some cases, the fruit body stops developing at the cup stage while the hymenium continues to mature. This results in a cup-shaped fungus with an exposed layer of basidia bearing normal and mature spores. Limnoperdon incarnatum is a structurally simple fungus, and relatively easy to grow in culture, suggesting it may have potential as a model organism for fruit body development in general. Under the experimental conditions used, fruit bodies matured to produce spores about 72 hours after the fungus started growing. [9] The aborted cups resemble the sporocarps of the cyphelloid fungi, but can be distinguished by their orthotrophic spore attachment and the lack of ballistospory (forceful spore discharge). McCabe and Escobar later suggested that the fungus may have evolved the loss of ballistospory by being compensated with the cup-shaped fruit body closing at maturity. [16] Halocyphina villosa is another small cup-shaped Basidiomycete fungus that has adapted to a marine environment; [17] in contrast to L. incarnatum, however, it starts out with a closed fruit body that later opens up to become cup-shaped. [11]

Although it is not known with certainty how the spores are dispersed, they may disperse passively in the water, or a mature spore-containing fruit body may float on the water surface for dispersal. L. incarnatum is homothallic, a mode of reproduction commonly employed by marine fungi that may confer a competitive advantage in marine environments. [11]

See also

Related Research Articles

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Phallaceae is a family of fungi, commonly known as stinkhorns, within the order Phallales. Stinkhorns have a worldwide distribution, but are especially prevalent in tropical regions. They are known for their foul-smelling, sticky spore masses, or gleba, borne on the end of a stalk called the receptaculum. The characteristic fruiting-body structure, a single, unbranched receptaculum with an externally attached gleba on the upper part, distinguishes the Phallaceae from other families in the Phallales. The spore mass typically smells of carrion or dung, and attracts flies, beetles and other insects to help disperse the spores. Although there is great diversity in body structure shape among the various genera, all species in the Phallaceae begin their development as oval or round structures known as "eggs". The appearance of Phallaceae is often sudden, as gleba can erupt from the underground egg and burst open within an hour. According to a 2008 estimate, the family contains 21 genera and 77 species.

The hymenium is the tissue layer on the hymenophore of a fungal fruiting body where the cells develop into basidia or asci, which produce spores. In some species all of the cells of the hymenium develop into basidia or asci, while in others some cells develop into sterile cells called cystidia (basidiomycetes) or paraphyses (ascomycetes). Cystidia are often important for microscopic identification. The subhymenium consists of the supportive hyphae from which the cells of the hymenium grow, beneath which is the hymenophoral trama, the hyphae that make up the mass of the hymenophore.

<i>Cyathus striatus</i> Species of fungus

Cyathus striatus, commonly known as the fluted bird's nest, is a common saprobic bird's nest fungus with a widespread distribution throughout temperate regions of the world. This fungus resembles a miniature bird's nest with numerous tiny "eggs"; the eggs, or peridioles, are actually lens-shaped bodies that contain spores. C. striatus can be distinguished from most other bird's nest fungi by its hairy exterior and grooved inner walls. Although most frequently found growing on dead wood in open forests, it also grows on wood chip mulch in urban areas. The fruiting bodies are encountered from summer until early winter. The color and size of this species can vary somewhat, but they are typically less than a centimeter wide and tall, and grey or brown in color. Another common name given to C. striatus, splash cups, alludes to the method of spore dispersal: the sides of the cup are angled such that falling drops of water can dislodge the peridioles and eject them from the cup. The specific epithet is derived from the Latin stria, meaning "with fine ridges or grooves".

<span class="mw-page-title-main">Auriculariales</span> Order of fungi

The Auriculariales are an order of fungi in the class Agaricomycetes. Species within the order were formerly referred to the "heterobasidiomycetes" or "jelly fungi", since many have gelatinous basidiocarps that produce spores on septate basidia. Around 200 species are known worldwide, placed in six or more families, though the status of these families is currently uncertain. All species in the Auriculariales are believed to be saprotrophic, most growing on dead wood. Fruit bodies of several Auricularia species are cultivated for food on a commercial scale, especially in China.

<i>Crucibulum</i> Genus of fungi

Crucibulum is a genus in the Nidulariaceae, a family of fungi whose fruiting bodies resemble tiny egg-filled bird's nests. Often called "splash cups", the fruiting bodies are adapted for spore dispersal by using the kinetic energy of falling drops of rain. The "eggs" inside the bird's nests are hard waxy shells containing spores, and tend to stick to whatever nearby herbage they land on, thus increasing the odds of being consumed and dispersed by herbivorous animals. Members of this genus are saprobic, obtaining nutrients from dead organic matter, and are typically found growing on decayed wood and wood debris. The three known Crucibulum species are distinguished from other genera of the Nidulariaceae by their relatively simple funiculus – a cord of hyphae that connects the peridiole to the exterior of the bird's nest.

<i>Nidula</i> Genus of fungi

Nidula is a genus of fungi in the family Agaricaceae. Their fruit bodies resemble tiny egg-filled birds' nests, from which they derive their common name "bird's nest fungi". Originally described in 1902, the genus differs from the related genera Cyathus and Crucibulum by the absence of a cord that attaches the eggs to the inside of the fruit body. The life cycle of this genus allows it to reproduce both sexually, with meiosis, and asexually via spores. Species in this genus produce a number of bioactive compounds, including 4-(p-hydroxyphenyl)-2-butanone, a major component of raspberry flavor and insect attractor used in pesticides.

<i>Cyathus olla</i> Species of fungus

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<i>Cyathus stercoreus</i> Species of fungus

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<i>Calbovista</i> Genus of fungi

Calbovista is a fungal genus containing the single species Calbovista subsculpta, commonly known as the sculptured puffball, sculptured giant puffball, and warted giant puffball. It is a common puffball of the Rocky Mountains and Pacific Coast ranges of western North America. The puffball is more or less round with a diameter of up to 15 cm (6 in), white becoming brownish in age, and covered with shallow pyramid-shaped plates or scales. It fruits singly or in groups along roads and in open woods at high elevations, from summer to autumn.

<i>Durianella</i> Genus of fungi

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<i>Panellus stipticus</i> Species of fungus in the family Mycenaceae found in Asia, Australia, Europe, and North America

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<i>Nia vibrissa</i> Species of fungus

Nia vibrissa is a species of fungus in the order Agaricales. The species is adapted to a marine environment and is a wood-rotting fungus, producing small, gasteroid basidiocarps on driftwood, submerged timber, mangrove wood, and similar substrates. The spores have long, hair-like projections and are widely dispersed in sea water, giving Nia vibrissa a cosmopolitan distribution.

<i>Podoserpula</i> Genus of fungi

Podoserpula is a genus of fungi in the family Amylocorticiaceae. The genus contains six species including the type species, P. pusio, commonly known as the pagoda fungus. Species of the genus Podoserpula produce fruit bodies consisting of up to a dozen caps arranged in overlapping shelves, attached to a central axis. Its unique shape is not known to exist in any other fungi. The genus is known to occur in Australia and New Zealand, Venezuela, Madagascar, and New Caledonia.

<i>Auriscalpium vulgare</i> Inedible European fungi

Auriscalpium vulgare, commonly known as the pinecone mushroom, the cone tooth, or the ear-pick fungus, is a species of fungus in the family Auriscalpiaceae of the order Russulales. It was first described in 1753 by Carl Linnaeus, who included it as a member of the tooth fungi genus Hydnum, but British mycologist Samuel Frederick Gray recognized its uniqueness and in 1821 transferred it to the genus Auriscalpium that he created to contain it. The fungus is widely distributed in Europe, Central America, North America, and temperate Asia. Although common, its small size and nondescript colors lead it to be easily overlooked in the pine woods where it grows. A. vulgare is not generally considered edible because of its tough texture, but some historical literature says it used to be consumed in France and Italy.

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<i>Xylobolus frustulatus</i> Species of fungus

Xylobolus frustulatus, commonly known as the ceramic fungus or ceramic parchment, is an inedible species of crust fungus in the Stereaceae family. The fruit body forms small, hard, flat crust-like aggregations that resemble broken pieces of ceramic tile. These pieces are initially whitish before turning yellow-brown to gray-brown in age. The spore-bearing cells cover the upper surfaces of the fruit body. A saprobic species, it grows on well-decayed oak wood in Asia, northern Europe, and North America.

<i>Pholiota nubigena</i> Species of fungus

Pholiota nubigena, commonly known as the gastroid pholiota or the bubble gum fungus, is a species of secotioid fungus in the family Strophariaceae. It is found in mountainous areas of the western United States, where it grows on rotting conifer wood, often fir logs. It fruits in spring, often under snow, and early summer toward the end of the snowmelt period in high mountain forests. Fruit bodies appear similar to unopened mushrooms, measuring 1–4 centimetres tall with 1–2.4 cm diameter caps that are whitish to brownish. They have a short but distinct whitish stipe that extend through the internal spore mass (gleba) of the fruit body into the cap. The gleba consists of irregular chambers made of contorted gills that are brownish in color. A whitish, cottony partial veil is present in young specimens, but it often disappears in age and does not leave a ring on the stipe.

<i>Crustomyces subabruptus</i> Species of fungus

Crustomyces subabruptus is a species of toothed crust fungus in the family Cystostereaceae.

References

  1. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008). Dictionary of the Fungi (10th ed.). Wallingford, UK: CABI. p.  383. ISBN   978-0-85199-826-8.
  2. 1 2 3 4 5 6 7 8 9 Escobar GA, McCabe DE, Harpel CW (1976). "Limnoperdon, a floating gasteromycete isolated from marshes". Mycologia. 68 (4): 874–80. doi:10.2307/3758803. JSTOR   3758803.
  3. 1 2 Matheny PB, Curtis JM, Hofstetter V, Aime MC, Moncalvo JM, Ge ZW, Slot JC, Ammirati JF, Baroni TJ, Bougher NL, Hughes KW, Lodge DJ, Kerrigan RW, Seidl MT, Aanen DK, DeNitis M, Daniele GM, Desjardin DE, Kropp BR, Norvell LL, Parker A, Vellinga EC, Vilgalys R, Hibbett DS (2006). "Major clades of Agaricales: a multilocus phylogenetic overview" (PDF). Mycologia. 98 (6): 982–95. doi:10.3852/mycologia.98.6.982. PMID   17486974.
  4. 1 2 Hibbett DS, Binder M (2001). "Evolution of marine mushrooms". Biological Bulletin. 201 (3): 319–22. doi:10.2307/1543610. JSTOR   1543610. PMID   11751244. S2CID   27779610.
  5. Bodensteiner P, Binder M, Moncalvo JM, Agerer R, Hibbett DS (2004). "Phylogenetic relationships of cyphelloid homobasidiomycetes". Molecular Phylogenetics and Evolution. 33 (2): 501–15. doi:10.1016/j.ympev.2004.06.007. PMID   15336682.
  6. Yamaguchi K, Degawa Y, Nakagiri A (2009). "An aero-aquatic fungus, Peyronelina glomerulata, is shown to have teleomorphic affinities with cyphelloid basidiomycetes". Mycoscience. 50 (3): 156–64. doi:10.1007/s10267-008-0467-8. S2CID   85034892.
  7. Justo A, Vizzini A, Minnis AM, Menolli N Jr, Capelari M, Rodríguez O, Malysheva E, Contu M, Ghignone S, Hibbett DS (2011). "Phylogeny of the Pluteaceae (Agaricales, Basidiomycota): taxonomy and character evolution" (PDF). Fungal Biology. 115 (1): 1–20. doi:10.1016/j.funbio.2010.09.012. hdl: 2318/74776 . PMID   21215950. Archived from the original (PDF) on 2012-09-16. Retrieved 2011-07-21.
  8. Bärlocher F, Seena S, Wilson KP, Williams DD (2007). "Raised water temperature lowers diversity of hyporheic aquatic hyphomycetes". Freshwater Biology. 53 (2): 368–79. doi:10.1111/j.1365-2427.2007.01899.x.
  9. 1 2 3 McCabe DE. (1979). "Synchronous production and developmental history of sporocarps of Limnoperdon incarnatum". Mycologia. 71 (5): 899–907. doi:10.2307/3759280. JSTOR   3759280.
  10. Donoghue MJ, Alverson WS (2000). "A new age of discovery". Annals of the Missouri Botanical Garden. 87 (1): 110–6. doi:10.2307/2666212. JSTOR   2666212. S2CID   84480189.
  11. 1 2 3 Nakagiri A, Ito T (1991). "Basidiocarp development of the cyphelloid gasteroid aquatic basidiomycetes Haloscyphina villosa and Limnoperdon incarnatum". Canadian Journal of Botany. 69 (10): 2320–7. doi:10.1139/b91-292.
  12. Tubaki K. (1977). "Brackishwater fungi and their relationships to marine fungi". In Bigelow HE, Simmons EG (eds.). Abstracts: IMC2, Second International Mycological Congress: University of South Florida, Tampa, Florida, U.S.A. : Saturday 27 August–Saturday 3 September 1977. Vol. 2. New York Botanical Garden. p. 681. OCLC   4931044.
  13. Ito T, Yokoyama T (1979). "Distribution of Limnoperdon incarnatum Escobar in rice paddy field soils". Proceedings of the 23rd Annual Meeting of the Mycological Society of Japan. The Mycological Society of Japan. p. 75.
  14. Webster J, Dekock AN, Eicker A (1993). "Limnoperdon incarnatum, a gasteromycete from submerged twigs in South Africa". South African Journal of Botany. 59 (5): 519–21. doi: 10.1016/S0254-6299(16)30698-6 .
  15. Michaelides J, Kendrick B (1982). "The bubble-trap propagules of Beverwykella, Helicoön and other aero-aquatic fungi". Mycotaxon. 14 (1): 247–60.
  16. Escobar GA, McCabe DE (1979). "Limnoperdon, a cyphellaceous fungus with gasteroid basidia?". Mycotaxon. 9 (1): 48–50.
  17. Ginns J, Malloch D (1977). "Halocyphina, a marine basidiomycete (Aphyllophorales)". Mycologia. 69 (1): 53–8. doi:10.2307/3758619. JSTOR   3758619.