Name Changes for Fungi of Medical Importance, 2020 to 2021

ABSTRACT

The current article summarizes recent changes in nomenclature for fungi of medical importance published in the years 2020 to 2021, including new species and revised names for existing ones. Many of the revised names have been widely adopted without further discussion. However, those that concern common pathogens of humans may take longer to achieve general usage, with new and current names reported together to engender increasing familiarity with the correct taxonomic classification.

INTRODUCTION

Conventional fungal identification methods based on examination of morphological and phenotypic features are complicated by the astonishing diversity of organisms capable of causing human infections, especially in immunocompromised hosts (1–5). The adoption of molecular methods for fungal identification has driven profound changes in fungal nomenclature and taxonomy as correct taxonomic relationships and affiliations are elucidated. Many phyla recently recognized as polyphyletic have been disbanded or substantially revised, cryptic species have been described in numerous classical morphospecies, long-extant species have been moved to new genera based on genotypic comparisons, and new taxa have been erected to accommodate novel organisms delineated by modern phylogenetic analyses.

Alongside upheavals driven by modern polyphasic approaches to the delineation of taxonomic boundaries, implementation of the Amsterdam Declaration (6) has precipitated further widespread nomenclatural changes. Since 1 January 2013, the employment of separate names for the teleomorph (sexual) and anamorph (asexual) states of fungi has been prohibited, forcing mycologists to choose a single name (often from numerous existing ones) for many thousands of species. This new nomenclatural code also abandoned the practice of assigning precedence to the teleomorph name over its anamorph alternative(s) by allowing any of the multiple published legitimate names for a given species to be chosen as the correct name. To lessen unnecessary and transient nomenclatural instability, working groups and committees established under the auspices of the International Commission on the Taxonomy of Fungi (ICTF) and the Nomenclature Committee for Fungi (NCF) will propose lists of retained (protected) and rejected names for key species/genera, with only definitive changes being ratified.

While unambiguous application of fungal names is clearly important, the traceability of nomenclatural changes and a stable taxonomic system are paramount for all users, including medical mycologists (7). The multiplicity of names given to fungi of medical importance has long been recognized as a major issue in medical mycology, as highlighted in a Medical Research Council memorandum on the nomenclature of fungi pathogenic to humans and animals as early as 1958 (8) (Fig. 1). Currently, there is no single source available to clinicians, microbiologists, and mycologists that captures all nomenclatural changes proposed for fungi of medical importance. Novel fungal taxa and proposals to reassign or rename existing taxa are published continually in an ever-expanding range of scientific journals. However, for new names and combinations to be accepted as validly published, the International Code of Nomenclature for algae, fungi, and plants (ICN) requires that all such taxa be registered in recognized online repositories. The principal repositories, MycoBank (https://mycobank.org/) and Index Fungorum (https://indexfungorum.org), are thus invaluable sources of up-to-date taxonomic information. However, given the speed of change, even they are not complete/correct across all genera of medically important fungi. The current article represents an update to three previous ones (9–11) which provided lists of novel taxa and revised names for existing taxa for fungi of medical importance published from 2012 to 2015 (9), 2016 to 2017 (10), and 2018 to 2019 (11, 12).

FIG 1.

Photographs of the front cover (left) and introductory paragraph (right) of the Medical Research Council memorandum no. 23 (revised edition 1958) entitled “Nomenclature of fungi pathogenic to man and animals: names recommended for use in Great Britain.”

EXPERIMENTAL METHODS

To capture new fungal taxa and nomenclatural revisions described between 2020 and 2021, a series of systematic literature searches were conducted in the PubMed database (https://pubmed.ncbi.nlm.nih.gov/) using the following search terms: “fungal sp. nov.,” “fungal gen. nov.,” “sp. nov. mycosis,” “fungal new species,” “fungal new genus,” “novel fungus,” “ascomycete sp. nov.,” “basidiomycete sp. nov,” “Mucorales sp. nov,” “fungal taxonomic revision,” and “fungal comb. nov.” In addition, MycoBank and Index Fungorum were extensively searched to find taxonomic changes and additions to the most common fungal genera associated with human disease. The last date of access to these resources was 5 November 2022.

The novel taxa retained for inclusion here were those that had been recovered from human specimens; in some cases a proven etiological role in human infection has been established, but in others the clinical significance of the organism remains unknown. New species/genera from veterinary sources were excluded from our lists, even if they were proven agents of infection and likely to be causes of human mycoses in the future. Such is the case with Arthroderma lilyanum sp. nov. and Arthroderma mcgillisianum sp. nov., which were isolated from multiple kittens with suspected dermatophytosis in a Californian animal shelter (13). Similarly, extant species which had been recognized as agents of human disease for the first time have been excluded here. As in previous iterations of this review (11), the names listed in Tables 1 and 2 of the current article are those that fulfill the ICN rules for valid publication in that they (i) are in Latin binomial form, (ii) are accompanied by a description in Latin or English, (iii) have a holotype deposited in a recognized culture collection, and (iv) have been registered in MycoBank and published with a MycoBank registration number.

TABLE 1.

List of new fungal taxa from clinical material for the period 2020 to 2021

Speciesc	Order	Source(s)	Clinical relevance	Reference	MBb accession no.
Arachnomyces bostrychodes	Arachnomycetales	Human scalp	Not established	30	MB 834921
Arthroderma melbournense	Onygenales	Toenail dust	Not established	14	MB 835313
Basidiobolus omanensis	Basidiobolales	Intestinal tissue	Mucoromycosis	19	MB 839872
Coniochaeta massiliensis	Coniochaetales	Hand abscess	Not established	27	MB 843839
Cunninghamella arunalokei	Mucorales	Sinus and skin	Mucoromycosis	17	MB 840808
Currahmyces sparsispora	Onygenales	Human sputum	Not established	30	MB 835692
Exophiala arunalokei	Chaetothyriales	Subcutaneous mass	Phaeohyphomycosis	22	Pending
Gloeostereum cimri	Agaricales	Sputum, biopsy sample	Pulmonary cyst	25	MB 834197
Meanderella rijsii	Pleosporales	Subcutaneous mass	Phaeohyphomycosis	20	MB 838115
Malbranchea gymnosacoides	Onygenales	Human bronchial washing	Not established	30	MB 835692
Malbranchea multiseptata	Onygenales	Human bronchial washing	Not established	30	MB 835213
Malbranchea stricta	Onygenales	Human nail	Not established	30	MB 835219
Montagnula cylindrospora	Pleosporales	Human skin	Not established	28	MB 834472
Mucor variicolumellatus	Mucorales	Tissue/blood	Mucoromycosis	18	MB 828292
Nannizzia polymorpha	Onygenales	Skin lesion	Dermatophytosis	15	MB 825465
Parengyodontium americanum	Hypocreales	Respiratory samples	From patients with CMa	29	MB 828553
Phialemoniopsis limonesiae	Incertae sedis	Pus, cutaneous tissue	Phaeohyphomycosis	23	MB 837525
Pleurostoma hongkongense	Calosphaeriales	Subhepatic abscess	Phaeohyphomycosis	24	MB 835850
Pseudoarthropsis crassispora	Onygenales	Human bronchial washing	Not established	30	MB 834930
Pseudocanariomyces americanus	Sordariales	Hip tissue	Prosthetic joint infection	21	MB 839083
Pseudomalbranchea gemmata	Onygenales	Human bronchial washing	Not established	30	MB 835221
Purpureocillium roseum	Hypocreales	Corneal tissue	Keratitis	26	MB 835774
Spiromastigoides geomycoides	Onygenales	Human foot skin	Not established	30	MB 835222
Trichophyton persicum	Onygenales	Skin scrapings	Tinea corporis	16	MB 839323
Trichophyton spiraliforme	Onygenales	Skin scrapings	Tinea corporis	16	MB 839324

^aCoisolated from patients with confirmed coccidioidomycosis (CM).

^bMB, MycoBank.

^cBoldface indicates gen. nov.

TABLE 2.

List of revised fungal taxa from 2020 through 2021

Previous species name(s)	Revised species namea	Order	Reference	MB accession no.
Aspergillus amoenus	Aspergillus versicolor	Eurotiales	31	MB 172159
Aspergillus austroafricanus	Aspergillus versicolor	Eurotiales	31	MB 172159
Aspergillus cvetkovicii	Aspergillus creber	Eurotiales	31	MB 800598
Aspergillus fructus	Aspergillus versicolor	Eurotiales	31	MB 172159
Aspergillus griseoaurantiacus	Aspergillus versicolor	Eurotiales	31	MB 172159
Aspergillus hongkongensis	Aspergillus versicolor	Eurotiales	31	MB 172159
Aspergillus jensenii	Aspergillus creber	Eurotiales	31	MB 800598
Aspergillus pepii	Aspergillus versicolor	Eurotiales	31	MB 172159
Aspergillus protuberus	Aspergillus versicolor	Eurotiales	31	MB 172159
Aspergillus puulaauensis	Aspergillus creber	Eurotiales	31	MB 800598
Aspergillus tabacinus	Aspergillus versicolor	Eurotiales	31	MB 172159
Aspergillus tennesseensis	Aspergillus creber	Eurotiales	31	MB 800598
Aspergillus venenatus	Aspergillus creber	Eurotiales	31	MB 800598
Ozonium auricomum	Coprinellus domesticus*	Agaricales	36	MB 474257
Phoma versabilis, Ascochyta versabilis	Sclerotiophoma versabilis	Pleosporales	35	MB 833530
Polyporus adustus, Geotrichopsis mycoparasitica	Bjerkandera adusta	Polyporales	36	MB 100902
Trichophyton benhamiae (African “race”)	Trichophyton africanum	Onygenales	33	MB 835890
Trichophyton benhamiae (European “race”; guinea pigs)	Trichophyton europaeum	Onygenales	33	MB 835888
Trichophyton benhamiae (East Asia; rabbits and guinea pigs)	Trichophyton japonicum	Onygenales	33	MB 835889
Trichophyton terrestre	Arthroderma terrestre	Onygenales	14	MB 835317
Proposed names for protection
Sporotrichum pruinosum, Phanerodontia chrysosporium	Phanerochaete chrysosporium*	Polyporales	36	MB 319705

^aAsterisks indicate names that will require protection from the Nomenclatural Committee for Fungi as older, legitimate names exist.

FINDINGS AND IMPLICATIONS

The novel fungal taxa from human samples described between 2020 and 2021 are presented in Table 1 and include new (often cryptic) species in several established human-pathogenic fungal genera including Arthroderma, Exophiala, Nannizzia, Pleurostoma, and Trichophyton. As in previous versions of this article, members of the Onygenales are overrepresented in this list, with a total of four new dermatophyte relatives: Arthroderma melbournense (14), Nannizzia polymorpha (15), Trichophyton persicum (16), and Trichophyton spiraliforme (16). N. polymorpha, T. spiraliforme, and A. melbournense were reported from a skin lesion, a case of tinea corporis, and toenail material, respectively, from single patients, and thus their wider clinical significance remains unproven. Conversely, T. persicum was reported from 36 Iranian cases of highly inflammatory human dermatophytosis and 1 case of feline infection (16). For both T. persicum (16) and T. spiraliforme, a zoonotic source of infection was postulated. The presence of several novel dermatophyte relatives in Table 1 of this article and the equivalent tables of the previous incarnations (9–11) once again reflects the fact that fungi isolated from visible superficial fungal infections are overrepresented compared to environmental saprobes that might be associated with pulmonary or other deep organ infections.

A similar picture is seen with novel fungi associated with deeper, subcutaneous infection and ocular infections where diagnosis and isolation of the causative agents are also less problematic. A third of the novel taxa (9/27) listed in Table 1 were isolated from various (often chronic) subcutaneous infections, from keratitis, or from other rapidly progressive infections. The novel fungi from proven cases of human infection include the following: (i) three novel species reported as agents of mucoromycosis (“mucoromycosis” rather than “mucormycosis” to reflect that the agents belong to the phylum Mucoromycota), two in Mucorales (Cunninghamella arunalokei [17] and Mucor variicolumellatus, a newly delineated member of the Mucor circinelloides complex [18]) and one in Basidiobolales, Basidiobolus omanensis (19); (ii) novel genera in Pleosporales (Meanderella rijsii, from a case of phaeohyphomycosis [20]) and Sordariales (Pseudocanariomyces americanus, from a prosthetic hip infection [21]); (iii) three additional novel species reported from isolated cases of phaeohyphomycosis, Exophiala arunalokei (Chaetothyriales, subcutaneous mass [22]), Phialemoniopsis limonesiae (incertae sedis, cutaneous tissue [23]), and Pleurostoma hongkongense (Calosphaeriales, abscess [24]); (iv) a single novel basidiomycete species, Gloeostereum cimri (Agaricales) from a patient with a pulmonary cyst (25); and (v) Purpureocillium roseum (Hypocreales) from corneal tissue in a case of keratitis (26). Additional novel species listed in Table 1 include single reports of Coniochaeta massiliensis (Coniochaetales, from a hand abscess [27]) and Montagnula cylindrospora (Pleosporales, human skin [28]), for both of which evidence of causation of human infection was lacking, and Parengyodontium americanum (Hypocreales), which was isolated from respiratory sample cultures from five patients with confirmed coccidioidomycosis (29). Whether P. americanum represented an opportunistic or coinfecting pathogen in that series of patients or rather was a repeated culture contaminant remains to be determined (29).

Finally, the number of novel Onygenales and close relatives listed in Table 1 is further swelled by the description of two additional new genera (Pseudoarthropsis and Pseudomalbranchea) and 8 new species (Currahmyces sparsispora, Malbranchea gymnosacoides, Malbranchea multiseptata, Malbranchea stricta, Pseudoarthropsis crassispora, Pseudomalbranchea gemmata, Spiromastigoides geomycoides [all Onygenales], and Arachnomyces bostrychodes [Arachnomycetales]) from an extensive revision of Malbranchea-like fungi from clinical specimens in the United States (30). It should be noted, however, that the majority of these novel taxa once again represented single isolations (from either human respiratory samples or dermatological specimens), and their clinical significance thus remains to be elucidated.

The number of existing fungal taxa with proposed nomenclatural changes during the period 2020 to 2021 (Table 2) is similar in length to the lists presented in previous updates. Previous lists were bolstered by genus- or family-wide taxonomic reappraisals of clinically important fungi, including the dermatophytes, yeasts with anamorphs in Candida, species in the Fusarium solani complex, and several genera within Ajellomycetaceae and Cryptococcus spp. in the neoformans and gattii complex (9–11). Here, the majority of the proposed changes concern fungi in Aspergillus series Versicolores following a detailed reassessment of the species boundaries within this hitherto-diverse clade comprising the medically important Aspergillus versicolor (31). The taxonomy of this series had previously undergone multiple rearrangements over the last decades, with a reduction of section Versicolores to series rank and its inclusion in the wider section Nidulantes (32) and parallel expansions in the numbers of species recognized, resulting in a total of 17 recognized species within series Versicolores (reviewed in reference 31). Despite multiple previous revisions involving multilocus and polyphasic approaches, identification to species level remained problematic even when genomic or proteomic approaches were employed, highlighting potential issues with the precise definitions of species boundaries. In this most recent revision, which combined phylogenetic analyses involving 5 loci and multispecies coalescence model-based methods, series Versicolores is reduced to four species (A. versicolor, Aspergillus creber, Aspergillus sydowii, and Aspergillus subversicolor) with the remaining 13 cryptic species subsumed into these four broadly defined species (Table 2) (31). Notably, the four retained species could all be robustly identified by any of the five genes employed for the phylogenetic analyses. Since similar issues surrounding accurate species-level identification have been noted in other common Aspergillus species (and indeed other medically important fungal genera), the authors of the latest revision predict that application of similar methodologies coupled with extensive taxon sampling might also lead to a similar reduction in the number of accepted cryptic species in other Aspergillus species complexes (31). It is also worth highlighting here that the 9 gene sequence data set analyses that led to the reduction of section Versicolores to series rank, while not directly precipitating name changes for fungi of medical importance, also resulted in widespread reevaluation of the genera and families across the Eurotiales, with updated subgeneric, sectional, and series classifications for both Aspergillus and Penicillium (32).

Table 2 is further bolstered by taxonomic revisions affecting the Onygenales, with the geophile Trichophyton terrestre transferred to Arthroderma (14) and the African, European, and East Asian “races” of the zoophilic Trichophyton benhamiae complex erected to species level as Trichophyton africanum, Trichophyton europaeum, and Trichophyton japonicum, respectively (33). Members of the former T. terrestre complex, which are among the most frequently isolated Arthroderma species from dermatological specimens and are usually considered geophilic contaminants or opportunistic colonizers/rare pathogens in humans, include several sexual states (Arthroderma insingulare, Arthroderma lenticulare, and Arthroderma quadrifidum) that are distinct from each other and from the original strain of T. terrestre based on both phylogenetic analyses and sexual incompatibility (14, 34). For the T. benhamiae complex, phylogenetic analyses based on four genes, coupled with population-genetic, ecological, and physiological data and mating type gene characterization, led to the erection of three novel species and one novel variety (33). Trichophyton benhamiae var. luteum var. nov. (MB 835887) was proposed for the strains of T. benhamiae with intense yellow coloration, predominantly of guinea pig origin, which are a major cause of tinea corporis and capitis in Europe. Isolates of the white phenotype segregated into three taxa: Trichophyton benhamiae var. benhamiae, which is predominantly found from dogs in North America; T. japonicum sp. nov., which affects rabbits and guinea pigs and predominates in East Asia but is also found in Europe; and T. europaeum sp. nov., which is mainly found in Europe with guinea pigs as a natural host (33). T. africanum sp. nov. was proposed for the African “race” of T. benhamiae. However, the rapid spread of T. benhamiae clade members across Europe, which has in part been driven by the animal trade, has likely obscured both the original geographic origins of individual species and the identities of any natural, wild-living animal hosts.

The remaining nomenclatural revisions listed in Table 2 include the type species Sclerotiophoma versabilis (ex-Phoma versabilis) of a novel genus, Sclerotiophoma, erected following reevaluation of phylogenetic relations among over 1,000 strains of Didymellaceae from 92 countries (35). A strain of P. versabilis had previously been recovered from human toenail material, although clinical significance was never demonstrated. The revisions also include recommendations for use or protection of three generic names in Agaricomycotina (Basidiomycota). Following the change to one scientific name for all fungal taxa, Stalpers and colleagues (36) evaluated the generic names of a large number of Agaricomycotina to determine synonymy based on their type and identified 47 sets of congeneric sexually and asexually typified names. Among those organisms that were identified as being nomenclaturally problematic were three that are occasionally or regularly isolated from clinical specimens. For Bjerkandera adusta, which was previously described as one of the most common basidiomycete contaminants of clinical cultures (37), this name had priority by date and was recommended for usage over more recent synonyms, so no further action is required. Coprinellus domesticus and Phanerochaete chrysosporium (asterisks in Table 2) do not have nomenclatural priority as older legitimate synonyms exist, and both of these more recent preferred generic names will require protection from the Nomenclatural Committee for Fungi.

CONCLUSION

We hope that the current review has captured most, if not all, of the proposed new or revised species names and nomenclatural changes affecting fungi of medical importance during the period 2020 to 2021. As in previous editions, the list of novel species includes a mixture of newly recognized cryptic or sibling species in well-established taxa and genuinely novel agents of superficial, subcutaneous, and disseminated human infections. Since a number of these novel species have been described around a single isolate, understanding of their prevalence and wider clinical relevance and whether the initial isolates are representative of the species will require the isolation and examination of additional examples. As always, further work will also be required to determine the importance of new cryptic species reported during this period and to determine whether they possess clinically relevant differences in pathogenicity or antifungal susceptibility that justify their identification beyond “species complex” level (38).

Historically, many nomenclatural changes in medically important fungi were met with considerable resistance and often took decades to gain complete acceptance (38). Indeed, in the previous edition of this update, we chose to summarize attempts to address the polyphyletic nature of genus Candida, which contains in excess of 200 species encompassing at least 13 teleomorph genera (11), and listed the often historical, key nomenclatural changes to provide a more complete update on the taxonomic status of clinically relevant “Candida” species. Our rationale for addressing this contentious issue was that a revised taxonomy that reflects phylogenetic relationships correlates better with unusual antifungal resistance profiles observed with many of the less common species of pathogenic yeasts (4, 39). Despite that many of the taxonomic revisions to “Candida” summarized at that time were several decades old, the suggestion that they should be finally adopted generated sustained and heated debate on social media with dire predictions of patient harm and irreconcilable disruption to the mycological literature (summarized in reference 40). It was reassuring that several highly respected mycology reference laboratories worldwide lent voices of support during the ensuing Twitter maelstrom and confessed to having also chosen independently to implement those long-overdue changes in a manner very similar to that originally suggested by ourselves, by reporting novel names alongside the historical ones (39–41). It was even more rewarding to recently read that the overwhelming majority of laboratories and clinicians who responded to an Australasian survey concerning fungal nomenclature changes were aware of and indeed had implemented such changes (42). In the future it is almost inevitable that many more medically important fungi will be similarly affected, with the result that ongoing clinical education will be essential. We believe that unnecessary confusion can be alleviated in part by reporting of novel names alongside their previous incarnation(s) until they have gained widespread recognition, together with regular reviews providing updates of the type presented here and elsewhere (11, 40–42).