Lycoperdon perlatum

Lycoperdon perlatum Scientific classification Kingdom: Fungi Division: Basidiomycota Class: Agaricomycetes Order: Agaricales Family: Agaricaceae Genus: Lycoperdon Species: L. perlatum Binomial name Lycoperdon perlatum Pers. (1796) Synonyms[1] Lycoperdon gemmatum Batsch (1783) Lycoperdon gemmatum var. perlatum (Pers.) Fr. (1829)

Lycoperdon perlatum, commonly known as the common puffball, warted puffball, gem-studded puffball or devil's snuff-box, is a species of puffball mushroom in the Agaricaceae family. A common species with a cosmopolitan distribution, it is a moderate-sized puffball with a round fruit body tapering to a wide stalk, and dimensions of 1.5 to 6 cm (0.6 to 2.4 in) wide by 3 to 7 cm (1.2 to 2.8 in) tall. It is off-white with a top covered in short spiny bumps or 'jewels', which are easily rubbed off. When mature they become brown and a hole in the top opens to release spores in a burst when the body is compressed by raindrops, a touch, falling nuts, etc. It grows in fields, gardens, and along roadsides, as well as in grassy clearings in woods. The puffball is edible when young and the internal flesh is completely white. Laboratory tests indicate that extracts of the puffball have antimicrobial and antifungal activities.

Taxonomy

The species was first described in the scientific literature in 1796 by mycologist Christian Hendrik Persoon.^[2] The variant Lycoperdon gemmatum var. perlatum, published by Elias Magnus Fries in 1829,^[3] is a synonym.^[1] Some authorities consider Lycoperdon gemmatum, described by August Batsch in 1783,^[4] to be a synonym.^[5][6]

The specific epithet perlatum is Latin for "widespread".^[7] It is commonly known as the common puffball, the gem-studded puffball^[8] (or gemmed puffball^[9]), the warted puffball,^[7] or the devil's snuff-box.^[10]

Description

Closeup of the surface, showing the characteristic spines

The fruit body ranges in shape from pear-like with a flattened top, to nearly spherical, and reaches dimensions of 1.5 to 6 cm (0.6 to 2.4 in) wide by 3 to 7 cm (1.2 to 2.8 in) tall. It has a stem-like base. The outer surface of the fruit body (the exoperidium) is covered in short cone-shaped spines that are interspersed with granular warts. The spines, which are whitish, gray, or brown, can be easily rubbed off, and leave reticulate pock marks or scars after they are removed.^[9] The base of the puffball is thick, and has internal chambers. It is initially white, but turns yellow, olive, or brownish in age.^[9] The reticulate pattern resulting from the rubbed-off spines is less evident on the base.^[11] In maturity, the exoperidium at the top of the puffball sloughs away, revealing a pre-formed hole (ostiole) in the endoperidium, through which the spores can escape.^[12] In young puffballs, the internal contents, the gleba, is white and firm, but turns brown and powdery as the spores mature.^[9] The gleba contains minute chambers that are lined with hymenium (the fertile, spore-bearing tissue); the chambers collapse when the spores mature.^[12]

The spores are spherical, thick-walled, covered with minute spines, and measure 3.5–4.5 μm in diameter. The capillitia (threadlike filaments in the gleba in which spores are embedded) are yellow-brown to brownish in color, lack septae,^[6] and measure 3–7.5 μm in diameter.^[11] The basidia (spore-bearing cells) are club-shaped, four-spored, and measure 7–9 by 4–5 μm. The basidia bear four slender sterigmata of unequal length ranging from 5–10 μm long. The surface spines are made of chains of pseudoparenchymatous hyphae (resembling the parenchyma of higher plants), in which the individual hyphal cells are spherical to elliptical in shape, thick-walled (up to 1 μm), and measure 13–40 by 9–35 μm. These hyphae do not have clamp connections.^[13]

Edibility

Lycoperdon perlatum, dried^[14]

Nutritional value per 100 g (3.5 oz)
Energy	1,845.5 kJ (441.1 kcal)
Carbohydrates	42 g
Fat	10.6 g
Protein	44.9 g
Iron	5.5 mg (42%)
Manganese	0.6 mg (29%)
Zinc	0.5 mg (5%)
Percentages are relative to US recommendations for adults. Source: USDA Nutrient Database

Lycoperdon perlatum is considered to be a good edible mushroom when young, when the gleba is still homogeneous and white. They have been referred to as "poor man's sweetbread" due to their texture and flavor. The fruit bodies can be eaten by slicing and frying in batter or egg and breadcrumbs,^[10] or used in soups.^[15] The puffballs become inedible as they mature: the gleba becomes yellow-tinged then finally develops into a mass of powdery olive-green spores.

The immature 'buttons' or 'eggs' of deadly Amanita species can be confused with puffballs. For this reason puffballs being collected for the table should always be sliced vertically and inspected for the internal developing structures of a mushroom. Amanitas will generally not have 'jewels' or a bumpy external surface.^[16]

The spores are ornamented with many sharp microscopic spines and can cause severe irritation of the lung (lycoperdonosis) when deliberately inhaled.^[17][18] This condition has been reported to afflict dogs that play or run where puffballs are present.^[19][20]

Similar species

There are several other puffball species with which L. perlatum might be confused. L. nettyanum, found in the Pacific Northwest region of the United States, is covered in granular patches, but these granules adhere more strongly to the surface than those of L. perlatum.^[21] L. pyriforme lacks prominent spines on the surface, and grows on rotting wood—although if growing on buried wood, it may appear to be terrestrial. The widely distributed and common L. umbrinum has spines that do not leave scars when rubbed off, a gleba that varies in color from dark brown to purple-brown at maturity, and a purple-tinged base. The small and rare species L. muscorum grows in deep moss. L. peckii can be distinguished from L. pyriforme by the lavender-tinged spines it has when young. L. rimulatum has purplish spores, and an almost completely smooth exoperidium.^[9]

Habitat and distribution

Lycoperdon perlatum grows solitarily, scattered, or in groups or clusters on the ground. It can also grow in fairy rings.^[10] Typical habitats include woods, grassy areas, and along roads.^[9] It has been reported from Pinus patula plantations in Tamil Nadu, India.^[13] The puffball sometimes confuses golfers because of its resemblance to a golfball when viewed from a distance.^[10] It is widely distributed, and has been reported from Africa (Tanzania),^[22] Asia (Himalayas,^[23] Japan),^[24] Australia,^[10] and South America (Brazil).^[25] In North America, where it is considered the most common puffball species, it ranges from Alaska^[5] to Mexico.^[26]

The puffball bioaccumulates heavy metals present in the soil,^[27][28] and can be used as a bioindicator of soil pollution by heavy metals and selenium.^[29] In one 1977 study, samples collected from grassy areas near the side of an interstate highway in Connecticut were shown to have high concentrations of cadmium and lead.^[30]

Chemistry

Several steroid derivatives have been isolated and identified from fruit bodies of L. perlatum, including (S)-23-hydroxylanostrol, ergosterol α-endoperoxide, ergosterol 9,11-dehydroendoperoxide and (23E)-lanosta-8,23-dien-3β,25-diol. The compounds 3-octanone, 1-octen-3-ol, and (Z)-3-octen-1-ol are the predominant components of the volatile chemicals that give the puffball its odor and flavor.^[31] Extracts of the puffball contain relatively high levels of antimicrobial activity against the human pathogenic bacteria Bacillus subtilis, Staphylococcus aureus, Escherichia coli, and Pseudomonas aeruginosa, with an efficiency comparable to that of ampicillin.^[32] These results corroborate an earlier study that additionally reported antibacterial activity against Salmonella typhimurium, Streptococcus pyogenes, and Mycobacterium smegmatis.^[33] Extracts of the puffball have also been reported to have antifungal activity against Candida albicans, Candida tropicalis, Aspergillus fumigatus, Alternaria solani, Botrytis cinerea, and Verticillium dahliae.^[34] A 2009 study found L. perlatum puffballs to contain the phenolic compound cinnamic acid at a concentration of about 14 milligrams per kilogram of mushroom.^[35] The fruit bodies contain the pigment melanin.^[36]

The unusual amino acid lycoperdic acid 3-(5(S)-carboxy-2-oxotetrahydrofuran-5(S)-yl)-2(S)-alanine was isolated from the mushroom, and reported in a 1979 publication.^[37] Based on the structural similarity of the new amino acid with (S)-glutamic acid, (S)-(+)-lycoperdic acid is expected to have antagonistic or agonistic activity for the glutamate receptor in the mammalian central nervous system. Methods to synthesize the compounds were reported in 1992,^[38] 1995,^[39] and 2002.^[40]

The predominant fatty acids in the puffball are linoleic acid (37% of the total fatty acids), oleic acid (24%), palmitic acid (14.5%), and stearic acid (6.4%).^[41]

References

1. ^ ^{a b} "Lycoperdon perlatum Pers. 1796". MycoBank. International Mycological Association. http://www.mycobank.org/MycoTaxo.aspx?Link=T&Rec=220647. Retrieved 2011-09-12. 
2. ^ Persoon CH. (1796) (in Latin). Observationes Mycologicae. 1. p. 4. 
3. ^ Fries EM. (1829) (in Latin). Systema Mycologicum. 3. Greifswald, Germany: Ernesti Mauritii. p. 37. http://www.archive.org/stream/systemamycologi00friegoog#page/n48/mode/2up. 
4. ^ Batsch AJGK. (1783) (in Latin) (PDF). Elenchus fungorum. Halle an der Saale, Germany: apud J. J. Gebauer. p. 147. http://caliban.mpiz-koeln.mpg.de/batsch/elenchus1/batsch_elenchus_1.pdf. 
5. ^ ^{a b} Orr DB, Orr RT. (1979). Mushrooms of Western North America. Berkeley, California: University of California Press. p. 115. ISBN 0-520-03656-5. 
6. ^ ^{a b} Miller HR, Miller OK. (2006). North American Mushrooms: a Field Guide to Edible and Inedible Fungi. Guilford, Connecticut: Falcon Guide. p. 453. ISBN 0-7627-3109-5. 
7. ^ ^{a b} Schalkwijk-Barendsen HME. (1991). Mushrooms of Western Canada. Edmonton, Canada: Lone Pine Publishing. p. 346. ISBN 0-919433-47-2. 
8. ^ Ammirati JF, McKenny M, Stuntz DE. (1987). The New Savory Wild Mushroom. Seattle, Washington: University of Washington Press. p. 194. ISBN 0-295-96480-4. 
9. ^ ^{a b c d e f} Arora D. (1986). Mushrooms Demystified: a Comprehensive Guide to the Fleshy Fungi. Berkeley, California: Ten Speed Press. pp. 693–4. ISBN 0-89815-169-4. 
10. ^ ^{a b c d e} Dickinson C, Lucas J. (1982). VNR Color Dictionary of Mushrooms. Van Nostrand Reinhold. p. 29. ISBN 978-0442219987. 
11. ^ ^{a b} Laessoe T, Pegler DN, Spooner B. (1995). British Puffballs, Earthstars and Stinkhorns: an Account of the British Gasteroid Fungi. Kew, UK: Royal Botanic Gardens. p. 152. ISBN 0-947643-81-8. 
12. ^ ^{a b} Miller HR, Miller OK. (1988). Gasteromycetes: Morphological and Developmental Features, with Keys to the Orders, Families, and Genera. Eureka, California: Mad River Press. p. 40. ISBN 0-916422-74-7. 
13. ^ ^{a b} Natarajan K, Purushothama KB. (1987). "On the occurrence of Lycoperdon perlatum in Pinus patula plantations in Tamil Nadu" (PDF). Current Science 56 (21): 1117–8. http://www.ias.ac.in/j_archive/currsci/56/21/1117-1118/viewpage.html. 
14. ^ Nutritional values are based on chemical analysis of Turkish specimens, conducted by Colak and colleagues at the Department of Chemistry, Karadeniz Technical University. Source: Colak A, Faiz Ö, Sesli E. (2009). "Nutritional composition of some wild edible mushrooms" (PDF). Türk Biyokimya Dergisi [Turkish Journal of Biochemistry] 34 (1): 25–31. http://www.turkjbiochem.com/2009/025-031.pdf. 
15. ^ Kuo M. (2007). 100 edible mushrooms. Ann Arbor, Michigan: The University of Michigan Press. p. 192. ISBN 0-472-03126-0. 
16. ^ Marley G. (2010). Chanterelle Dreams, Amanita Nightmares: The Love, Lore, and Mystique of Mushrooms. White River Junction, Vermont: Chelsea Green Publishing. p. 49. ISBN 1-60358-214-2. http://books.google.com/books?id=KJybhI1yWucC&pg=PA49. 
17. ^ Taft TA, Cardillo RC, Letzer D, Kaufman CT, Kazmierczak JJ, Davis JP. (July 29, 1994). "Respiratory Illness Associated with Inhalation of Mushroom Spores – Wisconsin, 1994". Morbidity and Mortality Weekly Report (Centers for Disease Control and Prevention) 43 (29): 525–6. http://www.cdc.gov/mmwr/preview/mmwrhtml/00032029.htm. Retrieved 2011-09-11. 
18. ^ Strand RD, Neuhauser EBD, Somberger CF. (1967). "Lycoperdonosis". New England Journal of Medicine 277 (2): 89–91. doi:10.1056/NEJM196707132770209. PMID 6027138. 
19. ^ Rubensohn M. (2009). "Inhalation pneumonitis in a dog from spores of puffball mushrooms". Canadian Veterinary Journal 50 (1): 93. PMC 2603663. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=2603663. 
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21. ^ Ramsey RW. (1980). "Lycoperdon nettyana, a new puffball from western Washington State". Mycotaxon 11 (1): 185–8. http://www.cybertruffle.org.uk/cyberliber/59575/0011/001/0185.htm. 
22. ^ Maghembe JA, Redhead JF. (1984). "A survey of ectomycorrhizal fungi in pine plantations in Tanzania". East African Agricultural and Forestry Journal 45 (3): 203–6. ISSN 0012-8325. 
23. ^ Thind KS, Thind IPS. (1982). "Gasteromycetes of the Himalayas, India. 10". Research Bulletin of the Panjab University Science 33 (1–2): 139–50. ISSN 0555-7631. 
24. ^ Kasuya T. (2004). "Gasteromycetes of Chiba Prefecture, Central Honshu, Japan – I. The family Lycoperdaceae". Journal of the Natural History Museum and Institute Chiba 8 (1): 1–11. ISSN 0915-9452. 
25. ^ Baseia UG. (2005). "Some notes on the genera Bovista and Lycoperdon (Lycoperdaceae) in Brazil". Mycotaxon 91: 81–6. 
26. ^ Moreno G, Lizárraga M, Esqueda M, Coronado ML. (2010). "Contribution to the study of gasteroid and secotioid fungi of Chihuahua, Mexico". Mycotaxon 112: 291–315. 
27. ^ Ylmaz F, Isloglu M, Merdivan M. (2003). "Heavy metal levels in some macrofungi". Turkish Journal of Botany 27 (1): 45–56. ISSN 1300-008X. 
28. ^ Falandysz J, Lipka K, Kawano M, Brzostowski A, Dadej M, Jedrusiak A, Puzyn T. (2003). "Mercury content and its bioconcentration factors in wild mushrooms at Lukta and Morag, northeastern Poland". Journal of Agricultural and Food Chemistry 51 (9): 2832–6. doi:10.1021/jf026016l. 
29. ^ Quince J-P. (1990). "Lycoperdon perlatum a fungus accumulating heavy metals and selenium" (in French). Mycologia Helvetica 3 (4): 477–86. ISSN 0256-310X. 
30. ^ McCreight JD, Schroeder DB. (1977). "Cadmium, lead and nickel content of Lycoperdon perlatum Pers. in a roadside environment". Environmental Pollution 13 (3): 265–8. doi:10.1016/0013-9327(77)90045-3. 
31. ^ Szummy A, Adamski M, Winska K, Maczka W. (2010). "Identification of steroid compounds and essential oils from Lycoperdon perlatum". Przemysl Chemiczny 89 (4): 550–3. ISSN 0033-2496. 
32. ^ Ramesh C, Pattar MG. (2010). "Antimicrobial properties, antioxidant activity and bioactive compounds from six wild edible mushrooms of western ghats of Karnataka, India". Pharmacognosy Research 2 (2): 107–12. doi:10.4103/0974-8490.62953. PMC 3140106. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=3140106. 
33. ^ Dulgar B. (2005). "Antimicrobial activity of ten Lycoperdaceae". Fitoterapia 76 (3–4): 352–4. doi:10.1016/j.fitote.2005.02.004. 
34. ^ Pujol V, Seux V, Villard J. (1990). "Research of antifungal substances produced by higher fungi in culture". Annales Pharmaceutiques Francaises 48 (1): 17–22. ISSN 0003-4509. 
35. ^ Barros L, Duenas M, Ferreira ICFR, Baptista P, Santos-Buelga C. (2009). "Phenolic acids determination by HPLC-DAD-ESI/MS in sixteen different Portuguese wild mushrooms species". Food and Chemical Toxicology 47 (6): 1076–9. doi:10.1016/j.fct.2009.01.039. 
36. ^ Almendros G, Martín F, González-Vila FJ, Martínez AT. (1987). "Melanins and lipids in Lycoperdon perlatum fruit bodies". Transactions of the British Mycological Society 89 (4): 533–7. doi:10.1016/S0007-1536(87)80087-6. http://www.cybertruffle.org.uk/cyberliber/59351/0089/004/0533.htm. 
37. ^ Rhugenda-Banga N, Welter A, Jadot J, Casimir J. (1979). "Un nouvel acide amine isole de Lycoperdon perlatum [A new amino acid isolated from Lycoperdon perlatum]" (in French). Phytochemistry 18 (3): 482–4. doi:10.1016/S0031-9422(00)81892-0. 
38. ^ Kaname M, Yoshifuji S. (1992). "1st synthesis of lycoperdic acid". Tetrahedron Letters 33 (52): 8103–4. doi:10.1016/S0040-4039(00)74730-7. 
39. ^ Yoshifuji S, Kaname M. (1995). "Asymmetric synthesis of Lycoperdic acid". Chemical & Pharmaceutical Bulletin 43 (10): 1617–20. ISSN 0009-2363. 
40. ^ Makino K, Shintani K, Yamatake T, Hara O, Hatano K, Hamada Y. (2002). "Stereoselective synthesis of (S)-(+)-lycoperdic acid through an endo selective hydroxylation of the chiral bicyclic lactam enolate with MoOPH". Tetrahedron 58 (48): 9737–40. doi:10.1016/S0040-4020(02)01254-1. 
41. ^ Nedelcheva D, Antonova D, Tsvetkova S, Marekov I, Momchilova S, Nikolova-Damyanova B, Gyosheva M. (2007). "TLC and GC‐MS probes into the fatty acid composition of some Lycoperdaceae mushrooms". Journal of Liquid Chromatography & Related Technologies 30 (18): 2717–27. doi:10.1080/10826070701560629. 

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