Abstract
The genus Wallemia comprises xerophilic species. Based on parenthesome ultrastructure it has been linked to the Filobasidiales (basidiomycetes). Species show a unique type of conidiogenesis, including basauxic development of fertile hyphae, segregation of conidial units more or less basipetally, and disarticulation of conidial units into mostly four arthrospore-like conidia. Wallemia is known from air, soil, dried food (causing spoilage), and salt. It can be isolated from hypersaline water of man-made salterns on different continents. Based on analyses of the nuclear small subunit ribosomal DNA (SSU rDNA) Wallemia has been placed into a highly supported clade together with Ustilaginomycetes and Hymenomycetes (Basidiomycota). Within this clade, it possesses an isolated position distantly related to the Filobasidiales and was characterized by numerous nucleotide substitutions not shared by any other fungus. Tests on xerotolerance indicated that Wallemia presents one of the most xerophilic fungal taxa. Xerotolerance is otherwise rare in the Basidiomycota. To acknowledge its unique morphology, evolution, and xerotolerance, a new basidiomycetous class Wallemiomycetes covering an order Wallemiales, is proposed. Based on differences in conidial size, xerotolerance, and sequence data of the rDNA internal transcribed spacer regions (ITS rDNA), at least three Wallemia species are segregated, identified as Wallemia ichthyophaga, Wallemia sebi, and Torula epizoa var. muriae, for which the combination Wallemia muriae is proposed. The three species are neotypified. Wallemia ichthyophaga differs from W. sebi and W. muriae in numerous nucleotides of the SSU and ITS rDNA. This high variation within Wallemia indicates existence of at least two cryptic genera not distinguishable by morphological characters.
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References
S.F. Altschul W. Gish W. Miller E.W. Myers D.J. Lipman (1990) ArticleTitleBasic local alignment search tool J. Mol. Biol. 215 403–410 Occurrence Handle10.1006/jmbi.1990.9999 Occurrence Handle1:CAS:528:DyaK3MXitVGmsA%3D%3D Occurrence Handle2231712
G.L. Barron (1968) The Genera of Hyphomycetes from Soil The Williams and Wilkins Co. Baltimore
D. Begerow R. Bauer T. Boekhout (2000) ArticleTitlePhylogenetic placements of ustilaginomycetous anamorphs as deduced from nuclear rDNA sequences Mycol. Res. 104 53–60 Occurrence Handle10.1017/S0953756299001161 Occurrence Handle1:CAS:528:DC%2BD3cXhsFartLY%3D
M.L. Berbee J.W. Taylor (1993) ArticleTitleDating the evolutionary radiations of the true fungi Can. J. Bot. 71 1114–1127
P. Blanz H. Döring (1995) ArticleTitleTaxonomic relationships in the genus Exobasidium (Basidiomycetes) based on ribosomal DNA analysis Stud. Mycol. 38 119–127
T. Boekhout R.J. Bandoni J.W. Fell K.J. Kwon-Chung (1998) Discussion of teleomorphic and anamorphic genera of heterobasidiomycetous yeasts C.F. Kurtzman J.W. Fell (Eds) The Yeasts, a Taxonomic Study Elsevier Science New York 609–625
P.F. Cannon (1990) ArticleTitleName changes in fungi of microbiological, industrial and medical importance. Part 4 Mycopathologia 111 75–83 Occurrence Handle1:STN:280:By6D3MrivFc%3D Occurrence Handle2215633
R.F. Castaňeda Ruiz D. Garcia J. Guarro (1998) ArticleTitleArthrowallemiaa new genus of hyphomycetes from tropical litter Mycol. Res. 102 16–18 Occurrence Handle10.1017/S0953756297004395
R. Ciferri (1958) ArticleTitleMauginiella a synonym of Sporendonema Atti Int. Bot. Univ. Pavia Lab. Crittog., Ser. 5 IssueID15 126–133
R. Ciferri P. Redaelli (1934) ArticleTitleSporendonema epizoum (Corda) Cif. et Red., an entity including Hemispora stellataOospora d’ Agatae J. Trop. Med. Hyg. 37 167–170
G.T. Cole R.A. Samson (1979) Patterns of Development in Conidial Fungi Pitman Publ. Co. London, San FranciscoMelbourne
G.S. de Hoog (1979) ArticleTitleThe black yeasts, II: Moniliellaallied genera Stud. Mycol. 19 1–90
G.S. de Hoog H. Beguin W.H. de Vegte (1997) ArticleTitlePhaeotheca triangularisa new meristematic black yeast from a humidifier Anton. Leeuw. 71 289–295 Occurrence Handle10.1023/A:1000156820793 Occurrence Handle1:STN:280:ByiB28nht1Y%3D
G.S. de Hoog A.H.G. Gerrits van den Ende (1998) ArticleTitleMolecular diagnostics of clinical strains of filamentous Basidiomycetes Mycoses. 41 183–189 Occurrence Handle1:CAS:528:DyaK1cXls1Wrtb4%3D Occurrence Handle9715630
de Hoog G.S., Göttlich E., Platas G., Genilloud O., Leotta G. and van Brummelen J. 2004. Evolution and ecology of the genus Thelebolus in Antarctica. Stud. Mycol, in press.
G.S. de Hoog J. Guarro J. Gené M.J. Figueras (2000) Atlas of Clinical Fungi2nd ed Centraalbureau voor Schimmelcultures/Universitat Rovira i Virgili Utrecht/Reus
K.H. Domsch W. Gams T.H. Anderson (1980) Compendium of Soil Fungi Academic Press London
O.E. Eriksson K. Winka (1997) ArticleTitleSupraordinal taxa of Ascomycota Myconet 1 IssueID1 1–16
M. Frank E. Hess (1941) ArticleTitleHalophilic brown molds of the genus Sporendonema emend. Ciferri et Redaelli J. Fish. Res. Board Can. 5 287–292
J.M. Frank E. Kingston J.C. Jeffery M.O. Moss M. Murray T.J. Simpson A. Sutherland (1999) ArticleTitleWalleminol and walleminonenovel caryophyllenes from the toxigenic fungus Wallemia sebi Tetrahedron Lett. 40 133–136 Occurrence Handle10.1016/S0040-4039(98)80039-7 Occurrence Handle1:CAS:528:DyaK1MXotlWrsg%3D%3D
Fries E.M. 1832. Systema mycologicumGreifswald.
W. Gams E.S. Hoekstra A. Aptroot (1998) CBS Course of Mycology, 4th ed Centraalbureau voor Schimmelcultures Baarn
A. Gargas J.W. Taylor (1992) ArticleTitlePolymerase chain reaction (PCR) for amplifying and sequencing nuclear 18S rDNA from lychenized fungi Mycologia 84 589–592 Occurrence Handle1:CAS:528:DyaK3sXitVKisrg%3D
A.H.G. Gerrits van den Ende G.S. de Hoog (1999) ArticleTitleVariability and molecular diagnostics of the neurotropic species Cladophialophora bantiana Stud. Mycol. 43 151–162
N. Gunde-Cimerman P. Zalar G.S. de Hoog A. Plemenitaš (2000) ArticleTitleHypersaline water in salterns – natural ecological niches for halophilic black yeasts FEMS Microbiol. Ecol. 32 235–240 Occurrence Handle10.1016/S0168-6496(00)00032-5 Occurrence Handle1:CAS:528:DC%2BD3cXktVSgu7s%3D Occurrence Handle10858582
T.A. Hall (1999) ArticleTitleBioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucl. Acids Symp. Ser. 41 95–98 Occurrence Handle1:CAS:528:DC%2BD3cXhtVyjs7Y%3D
M.H. Hashmi G. Morgan-Jones (1973) ArticleTitleConidium ontogeny in hyphomycetes. The meristem arthrospores of Wallemia sebi Can. J. Bot. 51 1669–1671
L. Hendriks A. Goris J.-M. Neefs Y. van de Peer G. Hennebert R. de Wachter (1989) ArticleTitleThe nucleotide sequence of the small ribosomal subunit RNA of the yeast Candida albicansthe evolutionary position of the fungi amongst the Eukaryotes Syst. Appl. Microbiol. 12 223–229 Occurrence Handle1:CAS:528:DyaK3cXksFensb4%3D
K. Høye (1902) ArticleTitleUndersøgelser op klipfiskesoppen Bergen Mus. Aarbog. 7 1–39
F. Jeannmougin J.D. Thompson M. Gouy D.G. Higgins T.J. Gibson (1998) ArticleTitleMultiple sequence alignment with Clustal X Trends Biochem. Sci. 23 403–405 Occurrence Handle10.1016/S0968-0004(98)01285-7 Occurrence Handle9810230
O. Johan-Olsen (1887) ArticleTitleOp sop på klipfisk den såkaldte mid Christiania Videnkabs-Selskab Forhandl. 12 5
S. Lappalainen A.L. Pasanen M. Reiman P. Kalliokoski (1998) ArticleTitleSerum IgG antibodies against Wallemia sebiFusarium species in Finnish farmers Ann. Alergy, Astma Immunol. 81 589–592
M.F. Madelin S. Dorabjee (1974) ArticleTitleConidium ontogeny in Wallemia sebi Trans. Br. Mycol. Soc. 63 121–130
F. Masclaux H. Guého G.S. de Hoog R. Christen (1995) ArticleTitlePhylogenetic relationships of human-pathogenic Cladosporium (Xylohypha) species inferred from partial LS rRNA sequences J. Med. Vet. Mycol. 33 327–338 Occurrence Handle1:STN:280:BymC383kvFM%3D Occurrence Handle8544086
R.T. Moore (1986) ArticleTitleA note on Wallemia sebi Anton. Leeuw. 52 183–187 Occurrence Handle10.1007/BF00429322 Occurrence Handle1:STN:280:BimB28jmsFE%3D
R.T. Moore (1996) The dolipore/parenthesome septum in modern taxonomy B. Sneh S. Jabaji-Hare S. Neate G. Dijst (Eds) Rhizoctonia Species: Taxonomy, Molecular Biology, Ecology, Pathology and Disease Control Kluwer Acad. Publ. DordrechtThe Netherlands 13–35
H. Nishida K. Ando Y. Ando A. Hirata J. Sugiyama (1995) ArticleTitleMixia osmundae: transfer from the Ascomycota to the Basidiomycota based on evidence from molecules and morphology Can. J. Bot. 73 S660–S666
H. Nishida Y. Tajiri J. Sugiyama (1998) ArticleTitleMultiple origins of fungal group I introns located in the same position of nuclear SSU rRNA gene J. Mol. Evol. 46 IssueID4 442–448 Occurrence Handle1:CAS:528:DyaK1cXitlSntLo%3D Occurrence Handle9541539
Y. Niwata M. Takashima J. Tornai-Lehoczki T. Deak T. Nakase (2002) ArticleTitleUdeniomyces pannonicus sp. nov., a ballistoconidium-forming yeast isolated from leaves of plants in Hungary Int. J. Syst. Evol. Microbiol. 52 1887–1892 Occurrence Handle10.1099/ijs.0.02209-0 Occurrence Handle1:CAS:528:DC%2BD38XnvFyhsLc%3D Occurrence Handle12361301
J.I. Pitt A.D. Hocking (1977) ArticleTitleInfluence of solute and hydrogen ion concentration on the water relations of some xerophilic fungi J. Gen. Microbiol. 101 35–40 Occurrence Handle1:STN:280:CSiB2M7kvVI%3D Occurrence Handle19558
J.I. Pitt A.D. Hocking (1997) Fungi and Food Spoilage2nd ed Blackie Academic & Professional London
K. Raper C. Thom (1949) A Manual of Penicillia The Williams and Wilkins Co. BaltimoreMaryland
S. Roussel G. Reboux J.-C. Dalphin K. Bardonnet L. Millon R. Piarroux (2004) ArticleTitleMicrobiological evolution of hay and relapse in patients with farmer’s lung Occup. Environ. Med. 61 3e
R.A. Samson E.S. Hoekstra J.C. Frisvad O. Filtenborg (2002) Introduction to Food- and Airborne Fungi6th ed Centraalbureau voor Schimmelcultures Utrecht
G. Schoop (1937) ArticleTitleSalzpilz (Torula epizoa) auf Lebensmitteln Deutsche Tierärztl. Wschr. 45 621–624
G. Scorzetti J.W. Fell A. Fonseca A. Statzell-Tallman (2002) ArticleTitleSystematics of basidiomycetous yeasts: a comparison of large subunit D1/D2 and internal transcribed spacer rDNA regions FEMS Yeast Res. 2 IssueID4 495–517 Occurrence Handle10.1016/S1567-1356(02)00128-9 Occurrence Handle1:CAS:528:DC%2BD38XovFGgsbw%3D Occurrence Handle12702266
J.S. Shah W. Pieciak J. Liu A. Buharin D.J. Lane (1996) ArticleTitleDiversity of host species and strains of Pneumocystis carinii is based on rRNA sequences Clin. Diagn. Lab. Immunol. 3 IssueID1 119–127 Occurrence Handle1:CAS:528:DyaK28XhtVajtrY%3D Occurrence Handle8770515
W. Sjamsuridzal Y. Tajiri H. Nishida T. Thuan H. Kawasaki A. Hirata A. Yokota J. Sugiyama (1997) ArticleTitleEvolutionary relationships of members of the genera TaphrinaProtomycesSchizosaccharomycesrelated taxa within the archiascomycetes: integrated analysis of genotypic and phenotypic characters Mycoscience 38 267–280
J.A. Stalpers (1978) ArticleTitleIdentification of wood-inhabiting Aphyllophorales in pure culture Stud. Mycol. 16 1–248
M. Stoll M. Piepenbring D. Begerow F. Oberwinkler (2003) ArticleTitleMolecular phylogeny of UstilagoSporisorium species (BasidiomycotaUstilaginales) based on internal transcribed spacer (ITS) sequences Can. J. Bot. 81 IssueID9 976–984 Occurrence Handle10.1139/b03-094 Occurrence Handle1:CAS:528:DC%2BD3sXpvVOms70%3D
T. Sugita T. Nakase (1998a) ArticleTitleMolecular phylogenetic study of the basidiomycetous anamorphic yeast genus Trichosporonrelated taxa based on small subunit ribosomal DNA sequences Mycoscience 39 7–13 Occurrence Handle1:CAS:528:DyaK1cXjvVelt7s%3D
T. Sugita T. Nakase (1998b) ArticleTitleTrichosporon japonicum sp. nov. isolated from the air Int. J. Syst. Bacteriol. 48 IssueIDPt 4 1425–1429
T. Sugita M. Takashima R. Ikeda T. Nakase T. Shinoda (2000) ArticleTitlePhylogenetic and taxonomic heterogeneity of Cryptococcus humicolus by analysis of the sequences of the internal transcribed spacer regions and 18S rDNAand the phylogenetic relationships of C. humicolusC. curvatusthe genus Trichosporon Microbiol. Immunol. 44 IssueID6 455–461 Occurrence Handle1:CAS:528:DC%2BD3cXkvFGhu70%3D Occurrence Handle10941928
J. Sugiyama T. Inamura G. Okada W. Sjamsuridzal H. Kawasaki A. Hirata (1995) Divergence and molecular evolution among basidiomycetous yeasts with the tropical and subtropical genus Graphiola Progress in Microbial Ecology: Proceedings of Seventh International Symposium on Microbial Ecology Santos Sao PauloBrazil 173–180
S.O. Suh T. Nakase (1995) ArticleTitlePhylogenetic analysis of the ballistosporous anamorphic genera UdeniomycesBullerarelated basidiomycetous yeasts, based on 18S rDNA sequence Microbiology 141 IssueIDPt 4 901–906 Occurrence Handle1:CAS:528:DyaK2MXltF2kurg%3D Occurrence Handle7773393
S.O. Suh J. Sugiyama (1993) ArticleTitlePhylogeny among the basidiomycetous yeasts inferred from small subunit ribosomal DNA sequence J. Gen. Microbiol. 139 IssueIDPt 7 1595–1598 Occurrence Handle1:CAS:528:DyaK2cXislamtQ%3D%3D Occurrence Handle8371119
S.O. Suh J. Sugiyama (1994) ArticleTitlePhylogenetic placement of the basidiomycetous yeasts Kondoa malvinellaRhodosporidium dacryoidumthe anamorphic yeast Sympodiomycepsis paphiopedili by means of 18S rRNA gene sequence analysis Mycoscience 35 367–375 Occurrence Handle1:CAS:528:DyaK2MXkvFyrtLg%3D
S. Suh M. Takashima M. Hamamoto T. Nakase (1996a) ArticleTitleMolecular phylogeny of the ballistoconidium-forming anamorphic yeast genus Bullerarelated taxa based on small subunit ribosomal DNA sequences J. Gen. Appl. Microbiol. 42 501–509 Occurrence Handle1:CAS:528:DyaK2sXht1Sitbw%3D
S. Suh A. Takematsu M. Takashima T. Nakase (1996b) ArticleTitleMolecular phylogenetic study on stalked conidium-forming yeasts and related basidiomycetous yeast taxa based on 18S rDNA sequences Microbiol. Cult. Coll. 12 79–86
E.C. Swann J.W. Taylor (1993) ArticleTitleHigher taxa of basidiomycetes: an 18S rRNA gene perspective Mycologia 85 IssueID6 923–936 Occurrence Handle1:CAS:528:DyaK2cXktVCqurs%3D
D.L. Swofford (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4.0b.4a Sinauer Associates Massachusetts, Sunderland
T. Takahashi (1997) ArticleTitleAirborne fungal colony-forming units in outdoor and indoor environments in YokohamaJapan Mycopathologia 139 23–33 Occurrence Handle10.1023/A:1006831111595 Occurrence Handle1:STN:280:DyaK1c7nt1ahtg%3D%3D Occurrence Handle9511234
M. Takashima T. Nakase (1996) ArticleTitleA phylogenetic study of the genus TilletiopsisTilletiaria anomalarelated taxa based on the small subunit ribosomal DNA sequences J. Gen. Appl. Microbiol. 42 421–429 Occurrence Handle1:CAS:528:DyaK2sXhvFCgtg%3D%3D
M. Takashima T. Nakase (1999) ArticleTitleMolecular phylogeny of the genus Cryptococcusrelated species based on the sequences of 18S rDNA and internal transcribed spacer regions Microbiol. Cult. Coll. 15 35–47
M. Takashima T. Nakase (2001) ArticleTitleTilletiopsis derxiiTilletiopsis oryzicolaTilletiopsis pennisetithree new species of the ustilagionomycetous anamorphic genus Tilletiopsis isolated from leaves in Thailand Anton. Leeuw. 80 43–56 Occurrence Handle10.1023/A:1012218108640 Occurrence Handle1:STN:280:DC%2BD38%2FjtVyqtw%3D%3D
F.C. Terracina (1974) ArticleTitleFine structure of the septum in Wallemia sebi Can. J. Bot. 52 2587–2590
K. Ueda-Nishimura K. Mikata (2000) ArticleTitleTwo distinct 18S rRNA secondary structures in Dipodascus (Hemiascomycetes) Microbiology 146 1045–1051 Occurrence Handle1:CAS:528:DC%2BD3cXjsFersbk%3D Occurrence Handle10832631
E.B. Vaisey (1955) ArticleTitleOsmophilism of Sporendonema epizoum J. Fish. Res. Board Can. 2 901–903
Y. van de Peer L. Hendriks A. Goris A. Neefs M. Vancanneyet K. Kersters J.F. Berny G.L. Hennebert R. De Wachter (1992) ArticleTitleEvolution of basidiomycetous yeasts as deduced from small ribosomal subunit RNA sequences Syst. Appl. Microbiol. 15 250–258 Occurrence Handle1:CAS:528:DyaK3sXpsl2gug%3D%3D
K. Voigt E. Cigelnik K. O’ Donnell (1999) ArticleTitlePhylogeny and PCR identification of clinically important Zygomycetes based on nuclear ribosomal. DNA sequence data J. Clin. Microbiol. 37 3957–3964 Occurrence Handle1:CAS:528:DyaK1MXotV2nu78%3D Occurrence Handle10565914
J.A. von Arx (1970) The Genera of Fungi Sporulating in Pure Culture Cramer Verlag Lehre
P. Vuillemin (1931) Hemisporees et thallosporees Les Champignons parasites et les mycoses de l’ homme Lechevalier Paris 74–81
Walther S., Garnica M. and Weiss M. 2004. The systematic relevance of conidiogenesis modes in the gilled Agaricales. Mycol. Res., in press.
C.J.K. Wang (1965) Fungi of Pulp and Paper in New York State Univ. Coll. Forestry Tech. Publ. No
K.A. Wheeler A.D. Hocking J.I. Pitt (1988) ArticleTitleEffects of T and aw on germination and growth of W. sebi Trans. Br. Mycol. Soc. 90 365–368
T.J. White T. Burns S. Lee J. Taylor (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenies M.A. Innis D.H. Gelfand J.J. Sninsky T.J. White (Eds) PCR Protocols. A Guide to Methods and Amplifications Academic San Diego 315–322
G.M. Wood P.J. Mann D.F. Lewis W.J. Reid M.O. Moss (1990) ArticleTitleStudies on a toxic metabolite from the mould Wallemia Food Addit. Contam. 7–1 69–77
Z. Wu Y. Tsumura G. Blomquist X.-R. Wang (2003) ArticleTitle18S rRNA gene variation among common airborne fungiand development of specific oligonucleotide probes for the detection of fungal isolates Appl. Environ. Microbiol. 69 5389–5397 Occurrence Handle10.1128/AEM.69.9.5389-5397.2003 Occurrence Handle1:CAS:528:DC%2BD3sXntlSju70%3D Occurrence Handle12957927
P. Zalar G.S. de Hoog N. Gunde-Cimerman (1999a) ArticleTitleTrimmatostroma salinuma new species from hypersaline water Stud. Mycol. 43 61–67
P. Zalar G.S. de Hoog N. Gunde-Cimerman (1999b) ArticleTitleTaxonomy of the endoconidial black yeast genera PhaeothecaHyphospora Stud. Mycol. 43 38–48
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Zalar, P., Sybren de Hoog, G., Schroers, HJ. et al. Taxonomy and phylogeny of the xerophilic genus Wallemia (Wallemiomycetes and Wallemiales, cl. et ord. nov.). Antonie Van Leeuwenhoek 87, 311–328 (2005). https://doi.org/10.1007/s10482-004-6783-x
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DOI: https://doi.org/10.1007/s10482-004-6783-x