Cunninghamellaceae

Overview

Limits of the Cunninghamellaceae were a topic of controversy regarding not only which genera should be included in the family but also the number of valid species of Cunninghamella. Lendner (1908) was the first to include Cunninghamella in a taxonomic scheme when he placed it in the Chaetocladiaceae, along with Choanephora and Chaetocladium. Many later workers (Fitzpatrick, 1930; Zycha et al., 1969) classified Cunninghamella in the Choanephoraceae along with other taxa not thought by present-day students of Mucorales to be closely related to the genus: Blakeslea, Choanephora, Radiomyces (all Mucorales), and Rhopalomyces (Zoopagales). Naumov (1935) first proposed the family Cunninghamellaceae (without a Latin diagnosis; validated by R.K. Benjamin, 1959) for Cunninghamella, Sigmoideomyces and Thamnocephalis. The latter genus has often been treated as a member of the Deuteromycetes (Hesseltine, 1955; Kendrick and Carmichael, 1973; Carmichael et al., 1980). Several other genera including Chaetocladium, Mycotypha and Phascolomyces also have been placed in the family by various students of Mucorales (Hesseltine, 1955; Benjamin, 1959; Pidoplichko and Mil’ko, 1971; Hesseltine and Ellis, 1973; Mil’ko, 1974). Most unusual of the several schemes of classification is that of Mil’ko and coworkers whose Cunninghamellaceae included unispored taxa (Benjaminia, Chaetocladium, Cunninghamella, Mycotypha, Phascolomyces, Radiomycopsis), which have been placed in four separate mucoralean families: Chaetocladiaceae, Cunninghamellaceae, Mycotyphaceae and Radiomycetaceae.

A data set consisting of six taxa from the Mortierellales and 75 spp. containing at least one species all of the genera in culture of the Mucorales (tef-1a, 18S rDNA, 28S rDNA, morphology) of O’Donnell et al. (2001) showed that the Cunninghamella echinulata was the basal taxon of a clade containing three genera (Absidia s.s., Chlamydoabsidia, Halteromyces) that is considered the Absidiaceae here. The Absidiaceae clade, 94% bootstrap support (BP), is distinguished from C. echinulata by 75% BP (O’Donnell et al, 2001). Voigt and Olsson (2008) analyzed a data set (act, tef-1a, 18S rRNA, 28S rRNA) containing selected species of 50 genera of the Mucorales that contained two species of Cunninghamella (C. bertholletiae, C. echinulata). These two species of Cunninghamella form a clade (Cunninghamellaceae here) by neighbor-joining (> 50% BP) and strict consensus (100% BP).

Cunninghamella bertolletiae is a causative agent of mucormycosis in humans (Darrisaw et al., 2000; Righi et al., 2008) and a model of mucormycosis has been deeveloped with C. bertholletiae in mice (Honda et al. 1999). Several species of Cunninghamella have been used to study the metabolism of a drug in horses (meloxican by C. elegans; Åberg et al., 2009), tomato waste hydrolysate to improve glucose uptake and hyphal lipids (C. echinulata; Fakas et al., 2008), methoxychlor metabolism (C. elegans; Keum et al., 2009), and transformation of meloxicam and theobromine (C. blakesleeana — Prasad et al., 2009; C. echinulata — Pekala et al., 2008).

Cunninghamellaceae, as circumscribed here, contains only one genus Cunninghamella. Cunninghamella has been object of many monographs (Alcorn and Yeager, 1938; Cutter, 1946; Mil’ko and Beljakova, 1967; Samson, 1969; Baijal and Mehrotra, 1980; Lunn and Shipton, 1983) but the most recent may be the best (Zheng and Chen, 2001). These fungi can be readily isolated from dung, soil, and other organic materials. Cunninghamellaceae is recognized by Cannon and Kirk (2007) and Kirk et al (2008). The only significant genus for this family is Cunninghamella according to Cannon and Kirk (2007) but the Encyclopedia of Life (http://www.eol.org/) on 1 November 2009 listed Chlamydoabsidia, Cunninghamella, Gongronella, Halteromyces and Hesseltinella as belonging in the Cunninghamellaceae.

Cunninghamellaceae Naumov ex R. K. Benjamin, 1959 (Aliso 4: 415).
= Cunninghamellaceae Naumov, 1935 [Opredelitel Mukorovykh (Mucorales), Ed. 2, p. 16; nomen nudum, without a Latin diagnosis, Art. 36.1 of the ICBN (McNeill et al., 2006)].

Mycelium branched, coenocytic, often septate in age. Sporophores branched, coenocytic and terminating in fertile vesicles. Fertile vesicles globose to obovoid or obpiriform, bearing pedicellate sporangiola. Sporangiola unispored, acolumellate, smooth or spinose. Zygospores, where known, with a rough, pigmented, zygosporangial wall; suspensors opposed, nearly equal, lacking appendages.
Type genus: Cunninghamella

Synopsis of Genera

CUNNINGHAMELLA Matruchot, 1903 (Ann. Mycol. 1: 47); 5 spp. [10 spp. + 2 varieties to 3 spp. + 1 var. recognized] (O’Donnell, 1979 — illus.; Baijal and Mehrotra, 1980 – ILLUS. and KEY TO SPP; Weitzman, 1984; Liu et al., 2001—phylogeny; Zheng and Chen, 2001 – monograph).
= Actinocephalum Saito, 1905 [Bot. Mag. (Tokyo) 19: 36].
= Saitomyces Ricker, 1906 (J. Mycology 12: 61).
= Muratella Bainier & Sartory, 1913 (Bull. Soc. Mycol. France 29: 129).

Genera Not Accepted Here but Included in Cunninghaqmellaceae by Some Authors

[Benjaminia — a synonym of Benjaminiella: see Synopsis of Genera of Unknown Affinities (Mucorales)].

[Blakeslea— see Choanephoraceae (Mucorales)].

[Chaetocladium — see Chaetocladiaceae (Mucorales)].

[Chlamydoabsidia — see Absidiaceae (Mucorales)].

[Choanephora — see Choanephoraceae (Mucorales)].

[Gongronella — see Synopsis of Genera of Unknown Affinities (Mucorales)]

[Halteromyces — see Absidiaceae (Mucorales)].

[Hesseltinella — see Synopsis of Genera of Unknown Affinities (Mucorales)]

[Mycotypha — see Mycotyphaceae (Mucorales)].

[Phascolomyces — genus of uncertain affinity (Mucorales)].

[Radiomyces — see Radiomycetaceae (Mucorales)].

[Radiomycopsis — a synonym of Radiomyces: see Radiomycetaceae (Mucorales)].

[Rhopalomyces — see Helicocephalidaceae (Zoopagales)]..

[Sigmoideomyces — see Sigmoideomycetaceae (Zoopagales)].

[Thamnocephalis — see Sigmoideomycetaceae (Zoopagales)].

Bibliography

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Alcorn, G.D., and C.C. Yeager. 1938. A monograph of the genus Cunninghamella with additional descriptions of several common species. Mycologia 30:653-658.

Baijal, U., and B.S. Mehrotra. 1980. The genus Cunninghamella – a reassessment. Sydowia 33:1-13.

Benjamin, R.K. 1959. The merosporangiferous Mucorales. Aliso 4: 321-433.

Cannon, P.F., and P.M. Kirk. 2007. Fungal families of the World. Wallingford, United Kingdom, CAB International. 456 p.

Carmichael, J.W., W.B. Kendrick, I.L. Conners, and L. Sigler. 1980. Genera of Hyphomycetes. The University of Alberta Press, Edmonton, Alberta, Canada. 386 p.

Cutter, V.M., Jr. 1946. The genus Cunninghamella (Mucorales). Farlowia 2:321-343.

Darrisaw, L., G. Hanson, D.H. Vesole, and S.C. Kehl. 2000. Cunninghamella infection post bone marrow transplant: case report and review of the lieterature. Bone Marrow Transplantation 25:1213-1216.

Fakas, S., S. Papanikolaou, M. Galiotou-Panayotou, and G. Anngelis. 2008. Organic nitrogen of tomato waste hydrolysate enhances glocose uptake and lipid accumulation in Cunninghamella echinulata. Journal of Applied Microbiology 105: 1062-1070.

Fitzpatrick, H.M. 1930. The Lower Fungi. Phycomycetes. McGraw-Hill Book Co., Inc., New York. U.S.A. 331 p.

Hesseltine, C.W. 1955. Genera of Mucorales with notes on their synonymy. Mycologia 47:344-363.

Hesseltine, C.W., and J.J. Ellis. 1973. Mucorales, pp. 187-217, In G. C. Ainsworth, F. K. Sparrow, and A. S. Sussman (Eds.). The Fungi. Vol. 4b. Academic Press, New York. 504 p

Honda, A., H. Kamei, K. Unno, K. Hiroshima, T. Kurijama, and M. Mijaji. 1999. A murine model of zygomycosis by Cunninghamella bertholletiae. Mycopatholoia 144: 141-146.

Kendrick, W.B., and J.W. Carmichael. 1973. Hyphomycetes, pp. 323-509. In G. C. Ainsworth, F. K. Sparrow, and A. S. Sussman (Eds.). The Fungi. Vol. IVA. Academic Press, New York. 621 p.

Keum, Y.S., Y.H. Lee, and J.-H. Kim. 2009. Metabolium of methoxychlor by Cunninghamella elegans ATCC 36112. Journal of Agricultural and Food Chemistry 57: 7931-7937.

Kirk, P.M., P.F. Cannon, D.W. Minter, and J.A. Stalpers. 2008. Ainsworth & Bisby’s Dictionary of the Fungi. 10th Ed. Wallingford, United Kingdom, CAB International. 771 p.

Lendner, A. 1908. Les Mucorinées de la Suisse. Beiträge zur Kryptogamenflora der Schweiz. III. K.-J. Wyss, Bern, Switzerland. 180 p.

Liu, X.-y., H. Huang, and R.-y. Zheng. 2001. Relationships within Cunninghamella based on sequence analysis of ITS rDNA. Mycotaxon 80:77-95.

Lunn, J.A., and W.A. Shipton. 1983. Re-evaluation of taxonomic criteria in Cunninghamella. Transactions of the British Mycological Society 81: 303-312.

McNeill, J., F.R. Barrie, H.M. Burdet, V. Demoulin, D.L. Hawksworth, K. Marhold, D.H. Nicolson, J. Prado, P.C. Silva, J.E. Skog, J.H. Wiersema and N.J. Turland. [eds.]. 2006. International Code of Botanical Nomenclature (Vienna Code). [Regnum Vegetabile Vol. 126]. A.R.G. Gantner Verlag KG, Ruggell, Liechtenstein. 568 p.

Mil’ko, A.A. 1974. Opredeltiel’ mukoral’nykh gribov Key to the identification of Mucorales. ‘Naukova Dumka’ , Kiev, Ukraine. 303 p.

Mil’ko, A.A., and L.A. Beljakova. 1967. Rod Cunninghamella Matruchot I taxonomie Cunninghamellaceae [Genus Cunninghamella Matruchot and taxonomy of the Cunninghamellaceae]. Mikrobiologiya 36:684-690 [English translation available in Microbiology 36 (4):573-578, 1967]

Naumov, N.A. 1935. Opredelitel Mukorovykh (Mucorales). Ed. 2. Bot. Inst. Acad. Sci. U.S.S.R. Moscow and Leningrad. 136 p.

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O’Donnell, K., F.M. Lutzoni, T.J. Ward, and G.L. Benny. 2001. Evolutionary relationships among mucoralean fungi (Zygomycota): Evidence for family polyphyly on a large scale. Mycologia 93:286-296.

Pekala, E., M. Kochan, and A.J. Carnell. 2009. Microbial metabolism of hydroxy metabolites of 1-oxohexyl derivatives of theobromine by Cunninghamella echinulata NRRL 1384. Letters in Applied Microbiology 48:19-24.

Pidoplichko, N.M., and A.A. Mil’ko. 1971. Atlas mukoral’vykh gribov Atlas of the Mucorales. Izdat. ‘Naukova Dumka,’ Kiev, Ukraine. 115p.

Prasad, G.S., S. Girisham, and S.M. Reddy. 2009. Studies on microbial trnaformation of meloxicam by Fungi. Journal of Microbiology and Biotechnology 19:922-931.

Righi, E., C.G. Giacomazzi, V. Lindstrom, A. Albarello, O. Soro, M. Miglino, M. Perotti, O.E. Varnier, M. Gobbi, C. Viscoli, and M. Bassetti. 2008. A case of Cunninghamella bertolettii rhino-cerebral infection in a leukaemic patient and review of recent published studies. Mycopthologia 165: 407-410.

Samson, R.A. 1969. Revision of the genus Cunninghamella (Fungi, Mucorales). Proceedings Koninkl. Nederl. Akademie van Wetenschappen-Amsterdam, Series C, 72:322-335.

Voigt, K. and I. Olsson. 2008. Molecular phylogenetic and scanning electron microscopical analysis places the Choanephoraceae and the Gilbertellaceae in a monophyletic group within the Mucorales (Zygomycetes, Fungi). Acta Biologica Hungarica 59:365-383.

Weitzman, I. 1984. The case for Cunninghamella elegans, C. bertholletiae, and C. echinulata as separate species. Trans. Brit. Mycol. Soc. 83: 527-529.

Zheng, R.-y., and G.-q. Chen. 2001. A monograph of Cunninghamella. Mycotaxon 80:1-75.

Zycha, H., R. Siepmann, and G. Linnemann. 1969. Mucorales eine Beschreibung aller Gattungen und Arten dieser Pilzgruppe. Lehre, J. Cramer. 355 p.

Updated Jun 08, 2010