Name Changes for Fungi of Medical Importance, 2012 to 2015

ABSTRACT

This article lists proposed new or revised species names and classification changes associated with fungi of medical importance for the years 2012 through 2015. While many of the revised names listed have been widely adopted without further discussion, some may take longer to achieve more general usage.

INTRODUCTION

The shift from recognizing fungal species on the basis of their morphological and biochemical characteristics to defining them on the basis of nucleic acid variations has resulted in significant revisions to the classification and naming of existing pathogens. This is because DNA sequence comparisons have demonstrated that many of the phenotypic characteristics used to classify fungal genera and species do not necessarily predict phylogenetic relatedness. In addition, as methods of molecular analysis have become more sophisticated, they have revealed the presence of cryptic or sibling species that lack distinct morphological characteristics, within many existing phenotypic species (1).

It has long been recognized that fungi can occur in several different morphological forms arising from asexual, sexual, or vegetative reproduction (2). Because these forms often develop independently from each other, the anamorph (asexual form) and teleomorph (sexual form) of many fungi have been described and named at different times without the connection between them being recognized. With the widespread application of molecular methods, it is now possible to confirm that these separate forms constitute a single species. As a consequence, there are numerous instances where the different names that have been applied to the asexual and sexual forms of the same species are now redundant. This is reflected in the most recent set of rules guiding the naming of fungi, the International Code of Nomenclature for algae, fungi, and plants (ICN) that was adopted in 2011 (http://www.iapt-taxon.org/nomen/main.php). As of 1 January 2013, the dual-naming system is no longer permitted, and mycologists have begun the process of choosing one name from several existing names for many fungal species. It should be noted that all legitimate names proposed for a species, whether for the sexual or the asexual form, can in the future serve as the correct name for that species. In cases where a later teleomorph-typified name is not widely used, it is to be hoped that the earlier anamorph-typified name will be adopted. Working groups and committees have been established under the auspices of the International Commission on the Taxonomy of Fungi (ICTF) (http://www.fungaltaxonomy.org/subcommissions) and the Nomenclature Committee for Fungi (NCF), and these will propose lists of accepted and rejected names for ratification.

Many scientific journals publish descriptions of new fungal species or proposed classification changes, and there is no single source that clinical microbiologists can easily consult to be updated on proposals affecting species of medical importance. However, the new ICN requires that all new fungal names should be registered in one or more several recognized online repositories, including Index Fungorum (http://www.indexfungorum.org) and MycoBank (http://www.MycoBank.org), in order for the names to be regarded as validly published.

This article is an attempt to list the proposed new species names and revised names of existing species associated with fungi of clinical significance published between 2012 and 2015. While many of the revised names listed have been widely adopted without further discussion, some may take longer to achieve more general usage.

METHODS

A systematic search of the Index Fungorum and MycoBank databases was conducted to identify studies describing new fungal species or proposed name changes of existing species published between January 2012 and December 2015. As search terms, the list of approximately 600 fungal generic names included in the online species list of the Atlas of Clinical Fungi (http://www.clinicalfungi.org) was used. The date of last access was 31 March 2016. To identify studies describing new fungal genera of medical importance published between January 2012 and December 2015, a systematic literature search of the PubMed database (http://www.ncbi.nlm.nih.gov/pubmed) using “gen. nov.” (i.e., genus novum or new genus) as the search term was conducted. The date of last access was also 31 March 2016.

The names listed in Tables 1 and 2 in this article are those that fulfilled the requirements of the ICN for valid publication. Under the ICN rules, a new or revised name for a fungal species is valid only if it is in Latin binomial form, is accompanied by an English or Latin description, has a designated living culture (holotype) deposited in a recognized culture collection, has been registered with MycoBank, and has been assigned a MycoBank registration number. Tables 1 and 2 include all studies that described species recovered from human samples. They include taxa that have been verified to cause human infection, as well as taxa whose pathogenic role was not established but where, for instance, the fungus was described as a respiratory tract colonizer. Species that have been proven to cause infection only in animals have been omitted. Tables 1 and 2 also exclude species of soil, plant, or other environmental fungi newly recognized as etiologic agents of human disease.

TABLE 1.

List of new fungal taxa recovered from human clinical material reported from January 2012 through December 2015

Species name	Order	Source	Clinical relevance	Reference
Apophysomyces mexicanus	Mucorales	Necrotizing fasciitis	Infection	28
Aspergillus citrinoterreus	Eurotiales	Respiratory tract	Infection	29
Aspergillus novoparasiticus	Eurotiales	Sputum	Not established	30
Aspergillus pragensis	Eurotiales	Nail	Infection	31
Aspergillus tanneri	Eurotiales	Gastric abscess, lung	Infection	32
Auxarthron ostraviense	Onygenales	Nail	Infection	33
Blastomyces gilchristii	Onygenales	Various	Infection	3
Candida mesorugosa	Saccharomycetales	Blood	Infection	12
Candida neorugosa	Saccharomycetales	Leg wound	Infection	13
Candida tunisiensis	Saccharomycetales	Mouth	Infection	34
Coniochaeta polymorpha	Coniochaetales	Endotracheal aspirate	Not established	35
Curvularia americana	Pleosporales	Bone marrow, nasal sinus, other sites	Infection	36
Curvularia chlamydospora	Pleosporales	Nasal sinus, nail	Infection	36
Curvularia hominis	Pleosporales	Nasal sinus, eye, nail, other sites	Infection	36
Curvularia muehlenbeckiae	Pleosporales	Chest	Infection	36
Curvularia pseudolunata	Pleosporales	Nasal sinus	Infection	36
Exophiala hongkongensis	Chaetothyriales	Nail	Infection	37
Exophiala polymorpha	Chaetothyriales	Subcutaneous nodule	Infection	38
Fonsecaea pugnacius	Chaetothyriales	Skin, brain	Infection	39
Fusarium keratoplasticum	Hypocreales	Keratitis	Infection	40
Fusarium petroliphilum	Hypocreales	Keratitis	Infection	40
Hongkongmyces pedis	Pleosporales	Subcutaneous nodule	Infection	15
Lecythophora luteorubra	Coniochaetales	Leg wound	Infection	41
Madurella fahalii	Sordariales	Black-grain eumycetoma	Infection	42
Madurella pseudomycetomatis	Sordariales	Black-grain eumycetoma	Infection	42
Madurella tropicana	Sordariales	Black-grain eumycetoma	Infection	42
Microsporum aenigmaticum	Onygenales	Skin	Infection	43
Microsporum mirabile	Onygenales	Not established	Infection	44
Ochroconis olivacea	Venturiales	Bronchoalveolar lavage fluid	Infection	45
Ochroconis ramosa	Venturiales	Bronchoalveolar lavage fluid, nail, skin	Infection	45
Paracoccidioides lutzii	Onygenales	Various	Infection	4
Phialemoniopsis cornearis	Sordariales	Corneal fluid	Infection	41
Phialemoniopsis hongkongensis	Sordariales	Subcutaneous nodule	Infection	46
Phialemoniopsis pluriloculosa	Sordariales	Nail	Infection	41
Phialemonium globosum	Sordariales	Sinus	Infection	41
Pleurostomophora ochracea	Diaporthales	Yellow-grain eumycetoma	Infection	47
Pseudochaetosphaeronema martinelli	Pleosporales	Subcutaneous nodule	Infection	48
Purpureocillium lavendulum	Hypocreales	Bronchial wash	Not established	49
Rasamsonia aegroticola	Eurotiales	Bronchial secretions	Not establisheda	27
Rasamsonia piperina	Eurotiales	Bronchial secretions	Not establisheda	27
Trichophyton onychocola	Onygenales	Nail	Infection	50

^aIsolates were respiratory tract colonizers in cystic fibrosis patients.

TABLE 2.

List of revised fungal taxa from January 2012 through December 2015

Current name	Revised name	Order	Reference
Bipolaris australiensis	Curvularia australiensis	Pleosporales	24
Bipolaris hawaiiensis	Curvularia hawaiiensis	Pleosporales	24
Bipolaris spicifera	Curvularia spicifera	Pleosporales	24
Candida haemulonii group II	Candida duobushaemulonii	Saccharomycetales	51
Cryptococcus neoformans var. grubii (serotype A, molecular types VNI and VNII)	Cryptococcus neoformans	Filobasidiales	16
Cryptococcus neoformans var. neoformans (serotype D, molecular type VNIV)	Cryptococcus deneoformans	Filobasidiales	16
Cryptococcus gattii (serotype B, molecular type VGI)	Cryptococcus gattii	Filobasidiales	16
Cryptococcus gattii (serotype C, molecular type VGIII)	Cryptococcus bacillisporus	Filobasidiales	16
Cryptococcus gattii (serotype B, molecular type VGII)	Cryptococcus deuterogattii	Filobasidiales	16
Cryptococcus gattii (serotype C, molecular type VGIV)	Cryptococcus tetragattii	Filobasidiales	16
Cryptococcus gattii (serotype B, molecular types VGIV and VGIIIc)	Cryptococcus decagattii	Filobasidiales	16
Geosmithia argillacea	Rasamsonia argillacea	Eurotiales	26
Lecythophora hoffmannii	Coniochaeta hoffmannii	Coniochaetales	35
Lecythophora mutabilis	Coniochaeta mutabilis	Coniochaetales	35
Leptosphaeria senegalensis	Falciformispora senegalensis	Pleosporales	22
Leptosphaeria tomkinsii	Falciformispora tomkinsii	Pleosporales	22
Madurella grisea	Trematosphaeria grisea	Pleosporales	22
Nigrograna mackinnonii	Biatriospora mackinnonii	Pleosporales	22
Phialemonium curvatum	Phialemoniopsis curvata	Sordariales	41
Pyrenochaeta romeroi	Medicopsis romeroi	Pleosporales	23
Pyrenochaeta mackinnonii	Nigrograna mackinnonii	Pleosporales	23
Ochroconis gallopava	Verruconis gallopava	Venturiales	52
Sarcopodium oculorum	Phialemoniopsis ocularis	Sordariales	41

RESULTS AND DISCUSSION

Table 1 lists validly described new fungal genera and species associated with human samples published between 2012 and 2015. The list includes new species of Aspergillus, Fusarium, and other well-recognized pathogens, such as Curvularia, Exophiala, and Madurella. It is also notable for two new cryptic species detected among the dimorphic endemic pathogens Blastomyces dermatitidis and Paracoccidioides brasiliensis. Blastomyces gilchristii and Paracoccidioides lutzii are genetically distinct and taxonomically valid but lack distinct morphological characteristics that allow them to be distinguished during routine laboratory testing (3, 4). It is unclear at present whether detection of these particular cryptic species contributes to patient management. However, this may change, and there are examples where cryptic or sibling species have subsequently been found to possess distinct phenotypic characters of potential clinical relevance. For instance, Aspergillus lentulus, a sibling species of Aspergillus fumigatus, is less susceptible to azole and echinocandin antifungal agents (5).

Molecular analysis of Candida species has allowed for the identification of an increasing number of taxa that cannot be distinguished on the basis of their phenotypic characteristics. These include Candida albicans and Candida dubliniensis (6), the Candida parapsilosis species complex (C. parapsilosis sensu stricto, C. metapsilosis, and C. orthopsilosis) (7), and the Candida glabrata species complex (C. glabrata, C. bracarensis, and C. nivariensis) (8, 9). Candida rugosa is an uncommon yeast species that has emerged as a cause of invasive human infection, particularly in Latin America, where it has been associated with catheter use (10). In 2006, Li et al. (11) described Candida pseudorugosa, which could be distinguished from Candida rugosa on the basis of several biochemical tests. Molecular analysis has now expanded the C. rugosa species complex to include five taxa, all of which are human pathogens, and two of which are newly described cryptic species: C. rugosa, Candida mesorugosa (12), C. neorugosa (13), C. pararugosa, and C. pseudorugosa. These species are genetically distinct but cannot be distinguished by the commercial identification systems used in clinical laboratories. Matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) mass spectrometry may be used to distinguish the individual members of the C. rugosa species complex (14).

Only one new genus of medical importance, Hongkongmyces, was described during the period under review (15). Hongkongmyces pedis was isolated from a lesion on the foot of an immunocompromised patient with subcutaneous phaeohyphomycosis.

Table 2 lists proposals for revisions to names associated with fungi of medical importance published between 2012 and 2015. The most controversial of these is the proposal to reorganize the Cryptococcus gattii-C. neoformans species complex into seven new species, two derived from C. neoformans and five from within C. gattii (16). This proposal is based on data from numerous phylogenetic analyses (including whole-genome analyses) and genotyping studies that have revealed significant genetic diversity within the species complex. These newly delimited taxa differ in their clinical manifestations, in their prevalence among different patient groups, and in some biochemical and physiological aspects (16). Of note for clinical laboratories, MALDI-TOF mass spectrometry can be used to distinguish the seven new species (16, 17).

Hagen et al. (16) have proposed that C. neoformans var. grubii and C. neoformans var. neoformans be recognized as separate species, named C. neoformans (formerly serotype A, molecular types VNI and VNII) and C. deneoformans (serotype D, molecular type VNIV), respectively. C. neoformans serotype A accounts for most reported cases of cryptococcal meningitis and is found worldwide. In 1999, Franzot et al. (18) assigned this serotype separate varietal status as C. neoformans var. grubii, while naming the much less common serotype D C. neoformans var. neoformans. With this latest renaming, the most common pathogen is now more clearly linked with the major disease it causes.

Unlike C. neoformans, which has a global distribution and is a common opportunistic pathogen in HIV-infected or other immunocompromised individuals, C. gattii typically affects patients without HIV infection and is thought to have a more limited environmental distribution. C. gattii infection is considered more difficult to treat than C. neoformans infection and requires longer and more aggressive treatment (19). Before 1999, C. gattii infection was rare in North America. However, since then, an outbreak of C. gattii infections has been ongoing in British Columbia, Canada, and the U.S. Pacific Northwest states of Oregon and Washington.

Hagen et al. (16) proposed that C. gattii be recognized as five separate species, namely, C. gattii (formerly molecular type VGI), C. bacillisporus (molecular type VGIII), C. deuterogattii (molecular type VGII), Cryptococcus tetragatii (molecular type VGIV), and C. degattii (molecular types VGIV and VGIIIc). The U.S. Pacific Northwest outbreak is characterized by infection with three clonal C. gattii strains (molecular types VGIIa, VGIIb, and VGIIc), two of which are uncommon outside this region, and one (molecular type VGIIc) that is unique to the region (20). These strain types now comprise C. deuterogattii. Harris et al. (21) reported 25 cases of C. gattii infection from eight non-Pacific Northwest U.S. states, including California, Georgia, and New Mexico. Twenty-three of these cases were caused by nonoutbreak strains of C. gattii. These infections differed in their clinical and demographic characteristics from outbreak-associated C. deuterogattii infections and were largely caused by molecular types VGI (C. gattii) and VGIII (C. bacillisporus).

The etiologic agents of black-grain eumycetoma mostly belong to the orders Pleosporales and Sordariales. These fungi often fail to sporulate in culture or require prolonged incubation to induce sporulation. Application of phenotypic morphological characteristics has thus led to many misidentifications and also to the misclassification of this difficult group of fungi. With the advent of molecular methods, it is now possible to resolve the phylogenetic and taxonomic relationships among these fungi. As summarized in Table 2, several groups (22, 23) have proposed a major reclassification and renaming of species belonging to the Pleosporales, including Leptosphaeria senegalensis, Leptosphaeria tomkinsii, Madurella grisea, Pyrenochaeta mackinnonii, and Pyrenochaeta romeroi. The current names for these fungi are Falciformispora senegalensis, Falciformispora tomkinsii, Trematosphaeria grisea, Biatriospora mackinnonii, and Medicopsis romeroi, respectively.

The preponderant Bipolaris species in human infections are B. australiensis, B. hawaiiensis, and B. spicifera. There is no clear morphological separation between Bipolaris and Curvularia, and some species show intermediate morphological forms. Following a major phylogenetic reevaluation, Manamgoda et al. (24) transferred these species to the existing genus Curvularia.

Geosmithia argillacea is a common thermotolerant environmental mold that has recently been reported as a cause of invasive fungal infections in patients with chronic granulomatous disease (25) and as a chronic respiratory tract colonizer in patients with cystic fibrosis (53). Following a molecular analysis that showed that Geosmithia is polyphyletic, Houbraken et al. (26) created a new genus, Rasamsonia, to accommodate G. argillacea and a number of related species. Based on morphological characteristics and phylogenetic analysis, Houbraken et al. (27) subsequently showed that four species could be distinguished within the R. argillacea species complex: R. argillacea, R. eburnea, and two newly described species, R. piperina and R. aegroticola (see Table 1). Morphologically, Rasamsonia is similar to Paecilomyces.

CONCLUSION

This review lists most, if not all, of the proposed new or revised species names and classification changes associated with fungi of medical importance for the years 2012 through 2015. In some instances, the newly described species listed here were based on a single isolate, and their general prevalence and clinical or public health significance remain to be established. In other reports, sophisticated molecular analysis enabled multiple isolates of novel cryptic or sibling species to be detected within large collections of existing well-established taxa of pathogens. Until these newly recognized siblings are found to possess distinct phenotypic characteristics of potential clinical relevance, such as differing antifungal drug susceptibility profiles, it seems reasonable for clinical and public health laboratories to adhere to expert recommendations (1) to group these siblings together as a species complex. This can be defined as a cluster of species that are clinically similar or identical, and this approach has already been adopted for some closely related groups of Fusarium species and elsewhere. Only when further research identifies clinically relevant distinctions between siblings will it become more important and economically justifiable to be able to undertake their routine identification.

Nomenclatural changes in medically important fungi often take decades to gain widespread acceptance (1). While some of the revised names listed in this review have been widely adopted without further discussion, others, such as the proposal to reorganize the Cryptococcus gattii-C. neoformans species complex, may never achieve general usage. Together with recent developments in molecular phylogenetic analysis, the new ICN for fungi has led to dramatic changes in naming and classification and will continue to do so. In this process, it seems probable that the names of many medically important fungi will be affected, and it will be important for clinical and public health microbiologists, as well as the manufacturers of commercial identification systems, to be aware of these changes and to update their databases as required. To this end, periodic updates of the lists provided here will be needed.

Biography

David W. Warnock, Ph.D., is Honorary Professor, University of Manchester, UK. From 1999 through his retirement in 2012, he worked for the U.S. Centers for Disease Control and Prevention (CDC), Atlanta, GA, in various capacities (Chief, Mycotic Diseases Branch; Director, Division of Foodborne, Bacterial and Mycotic Diseases; and Senior Advisor for Laboratory Program Development, National Center for Emerging and Zoonotic Infectious Diseases). Between 1993 and 1999, he directed the Public Health Laboratory Service Mycology Reference Laboratory in Bristol, UK. Dr. Warnock graduated with honors from the University College of Wales, Aberystwyth in 1969. He received his Ph.D. from the University of Leeds in 1972 and then trained as a clinical mycologist with the National Health Service at the Bristol Royal Infirmary. He is a Fellow of the American Academy of Microbiology, Infectious Diseases Society of America, and the Royal College of Pathologists. Dr. Warnock has published extensively on the epidemiology, laboratory diagnosis, and therapy of fungal diseases. He is the coauthor of several books, including Fungal Infection: Diagnosis and Management and Identification of Pathogenic Fungi. He has served as a volume editor of the Manual of Clinical Microbiology since 2007 and an editor of the Journal of Clinical Microbiology since 2009. He is a past President of the International Society for Human and Animal Mycology.