Name Changes for Fungi of Medical Importance, 2016–2017

This article lists proposed new or revised species names and classification changes associated with fungi of medical importance that were published in the years 2016 and 2017. While many of the revised names listed have been widely adopted without further discussion, some may take longer to achieve more general usage.

ABSTRACT

This article lists proposed new or revised species names and classification changes associated with fungi of medical importance that were published in the years 2016 and 2017. 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 detailed phylogenetic analysis has enabled more accurate delineation of taxonomic boundaries and has resulted in ongoing revisions to the classification and naming of existing pathogens. Molecular analysis has also revealed the presence of genetically distinct populations that deserve species status. These newly recognized cryptic or sibling species lack distinct morphological characteristics and have been found within many medically important species. In most cases, it remains unclear whether detection of these molecular siblings contributes to patient management. However, this may change, and there are instances where cryptic or sibling species have been found to possess distinct phenotypic characteristics of clinical or epidemiological relevance.

Additional taxonomic changes are also resulting from the adoption of the Amsterdam Declaration (1). This proposed a major modification to the code of nomenclature for fungi (http://www.iapt-taxon.org/nomen/main.php). From 1 January 2013, the practice of assigning separate names to the anamorph (asexual) and teleomorph (sexual) states of fungi was no longer permitted, and mycologists began the process of choosing one name from several existing names for many fungal species. By allowing all legitimate names proposed for a species, whether for the sexual or the asexual form, to serve as the correct name for that species, the new code of nomenclature ends the previous precedence of teleomorph over anamorph. 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 retained (protected) 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 International Code of Nomenclature for algae, fungi, and plants (ICN) requires that all new fungal names should be registered in one or more of 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 update to a previous list of proposed new species names and revised names of existing species associated with fungi of clinical significance (2). It lists names published between 2016 and 2017. While some of the revised names listed have been widely adopted without further discussion, others 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 2016 and December 2017. The date of last access was 30 June 2018. To identify studies describing new fungal species and genera of medical importance published between January 2016 and December 2017, a systematic literature search of the PubMed database (https://www.ncbi.nlm.nih.gov/pubmed) using “new species,” “new genus,” “sp. nov.” (i.e., species novum or new species), and “gen. nov.” (i.e., genus novum or new genus) as the search terms was conducted. The date of last access was 30 June 2018.

The names listed in the tables 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 only valid 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. The tables 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 only been proven to cause infection in animals have been omitted. The tables also exclude existing species of soil, plant, or other environmental fungi newly recognized as etiologic agents of human disease.

RESULTS AND DISCUSSION

Table 1 lists validly described new fungal genera and species associated with human samples that were published in 2016 and 2017, and Table 2 lists proposals for revisions to names associated with fungi of medical importance that were published between the same dates.

TABLE 1.

List of new fungal taxa recovered from human clinical material reported from January 2016 through December 2017

Species name	Order	Source(s)	Clinical relevance	Reference
Aspergillus hongkongensis	Eurotiales	Nail	Infection	36
Aspergillus pseudosclerotiorum	Eurotiales	Bronchoalveolar lavage fluid, lung tissue, sputum	Infection	37
Blastomyces percursus	Onygenales	Granulomatous lesion on lip	Disseminated infection	3
Cladosporium angulosum	Capnodiales	Bronchoalveolar lavage fluid	Infection	38
Cladosporium anthropophilum	Capnodiales	Bronchoalveolar lavage fluid, CSF, pleural fluid	Infection	38
Cladosporium crousii	Capnodiales	Bronchoalveolar lavage fluid	Infection	38
Cladosporium flavovirens	Capnodiales	Nail	Infection	38
Cladosporium floccosum	Capnodiales	Ethmoid sinus	Infection	38
Cladosporium subcinereum	Capnodiales	Sputum	Not established	38
Cladosporium tuberosum	Capnodiales	Nasal biosy, foot	Infection	38
Cladosporium xantochromaticum	Capnodiales	Bronchoalveolar lavage fluid	Infection	38
Cyphellophora ludoviensis	Chaetothyriales	Lesion on leg	Chromoblastomycosis	39
Emarellia grisea	Pleosporales	Not stated	Mycetoma	32
Emarellia paragrisea	Pleosporales	Not stated	Mycetoma	32
Emergomyces africanus	Onygenales	Biopsy of skin lesion	Infection	3
Emergomyces canadensis	Onygenales	Skin lesion	Infection	4
Emergomyces europaeus	Onygenales	Biopsy of chronic granulomatous lung lesion	Infection	4
Emergomyces orientalis	Onygenales	Sputum	Disseminated infection	13
Exophiala campbellii	Chaetothyriales	Lesion on foot	Infection	40
Histoplasma mississippiense	Onygenales	Not stated	Disseminated histoplasmosis	6
Histoplasma ohiense	Onygenales	Not stated	Histoplasmosis	6
Histoplasma suramericanum	Onygenales	Not stated	Histoplasmosis	6
Malassezia arunalokei	Malasseziales	Scalp	Infection	41
Microascus alveolaris	Microascales	Bronchoalveolar lavage fluid, lung tissue, sputum	Infection	42
Microascus brunneosporus	Microascales	Bronchoalveolar lavage fluid	Infection	42
Microascus campaniformis	Microascales	Bronchoalveolar lavage fluid	Infection	42
Microascus chinensis	Microascales	Nail	Infection	43
Microascus expansus	Microascales	Pleural fluid, sputum	Not established	42
Microascus intricatus	Microascales	Bronchoalveolar fluid	Infection	42
Microascus onychoides	Microascales	Nail	Infection	43
Microascus pseudolongirostris	Microascales	Nail	Infection	43
Microascus verrucosus	Microascales	Bronchoalveolar lavage fluid	Infection	42
Paracoccidioides americana	Onygenales	Not stated	Chronic paracoccidioidomycosis	23
Paracoccidioidomyces restrepiensis	Onygenales	Not stated	Chronic paracoccidioidomycosis	23
Paracoccidioides venezuelensis	Onygenales	Soil	Not established	23
Phialophora chinensis	Chaetothyriales	Skin lesion	Chromoblastomycosis	44
Phialophora ellipsoidea	Chaetothyriales	Human tissue	Chromoblastomycosis	44
Phialophora expanda	Chaetothyriales	Skin lesion	Chromoblastomycosis	44
Phialophora tarda	Chaetothyriales	Tissue	Chromoblastomycosis	44
Pithoascus lunatus	Microascales	Lesion on foot	Infection	43
Rhinocladiella tropicalis	Chaetothyriales	Lesion on leg	Chromoblastomycosis	39
Scopulariopsis cordiae	Microascales	Finger	Infection	42
Spiromastigoides albida	Onygenales	Lung biopsy	Infection	45
Sporothrix chilensis	Ophiostomatales	Nail	Infection	29
Talaromyces alveolaris	Eurotiales	Bronchoalveolar lavage fluid	Infection	46
Talaromyces minnesotensis	Eurotiales	Ear	Not established	46
Talaromyces rapidus	Eurotiales	Bronchoalveolar lavage fluid	Infection	46
Tintelnotia destructans	Pleosporales	Cornea, nail	Infection	47

TABLE 2.

List of revised fungal taxa from January 2016 through December 2017

Current name	Revised name	Order	Reference
Emmonsia helica	Blastomyces helicus	Onygenales	4
Emmonsia parva	Blastomyces parvus	Onygenales	4
Emmonsia pasteuriana	Emergomyces pasteurianus	Onygenales	3
Microsporum cookei	Paraphyton cookei	Onygenales	25
Microsporum gallinae	Lophophyton gallinae	Onygenales	25
Microsporum gypseum	Nannizzia gypsea	Onygenales	25
Microsporum nanum	Nannizzia nana	Onygenales	25
Microsporum persicolor	Nannizzia persicolor	Onygenales	25
Pleurostomophora ochracea	Pleurostoma ochraceum	Calosphaeriales	48
Pleurostomophora repens	Pleurostoma repens	Calosphaeriales	48
Pleurostomophora richardsiae	Pleurostoma richardsiae	Calosphaeriales	48

Table 1 is notable for the number of new species detected among the dimorphic, endemic pathogens belonging to the family Ajellomycetaceae of the order Onygenales. The Ajellomycetaceae contains the teleomorph species Ajellomyces dermatitidis, Ajellomyces capsulatum, and Ajellomyces duboisii, the anamorphs of which are the genera Blastomyces and Histoplasma. The Ajellomycetaceae also contains some genera that have no known teleomorphs, including Paracoccidioides and the newly described genus Emergomyces (3, 4).

Historically, all populations of the genus Histoplasma have been classified as Histoplasma capsulatum. The following three distinct varieties, determined by geographic distribution, morphological characteristics, and nature of disease caused, are recognized: H. capsulatum var. capsulatum (North and South America, human pathogen), H. capsulatum var. duboisii (Africa, human pathogen), and H. capsulatum var. farciminosum (northern Africa and the Middle East, horse pathogen). Initial genetic studies, based on a few loci, revealed that H. capsulatum is composed of at least seven genetically distinct populations (5).

Using whole-genome sequencing, Sepulveda et al. (6) have demonstrated that H. capsulatum is composed of several monophyletic and identifiable cryptic species. These authors have proposed that the use of the name Histoplasma capsulatum sensu stricto should be restricted to a single monophyletic group, the Panama or H81 lineage, as Panama was where the organism was first discovered and described. Three other genetic groups, all endemic to the Americas, have also been elevated to species status. The three new species, Histoplasma mississippiense (formerly known as NAm 1), Histoplasma ohiense (NAm 2), and Histoplasma suramericanum (LAm A) are prevalent in the Mississippi and Ohio river valleys and in South America, respectively (Table 1). Although these molecular siblings differ in their geographic distribution, they lack distinguishing morphological characteristics that allow them to be differentiated during routine diagnostic laboratory testing. Sepulveda et al. (6) noted that a fifth group, the African clade of H. capsulatum var. duboisii, is likely a separate species, but refrained from modifying its taxonomic status until more information is obtained.

Multilocus phylogenetic analysis has revealed that the genus Blastomyces is composed of five monophyletic subgroups (3, 4). One of these clades contains the etiologic agents of blastomycosis in North America, Blastomyces dermatitidis, and its sibling species, Blastomyces gilchristii (7). A second clade contains a novel species, named Blastomyces percursus, which has been recovered from immunocompetent and immunocompromised individuals in Israel and South Africa and had previously been identified as Blastomyces dermatitidis (3, 4). The third clade comprised a strain, isolated in 1970, from a patient from Alberta, Canada, with what was described as an unusual case of blastomycosis (8). In 2015, Sigler (9) determined that the isolate from this case represented a novel species of Emmonsia, named Emmonsia helica. In 2017, it was first proposed that Emmonsia helica should be renamed as Blastomyces helicus (10), but this taxon was not validated until 2018 (4). To date, all strains of this species have originated from North America. The two remaining monophyletic clades of Blastomyces comprised strains previously identified as Emmonsia parva. Dukik et al. (3) proposed that E. parva should be renamed Blastomyces parvus, but this taxon was not validated until 2018 (4).

The various molecular siblings of Blastomyces dermatitidis show few distinguishing morphological characteristics. In culture at 37°C, Blastomyces dermatitidis and Blastomyces percursus produce large yeast cells with broad-based budding, while Blastomyces parvus mainly produces giant cells, as well as occasional large yeast cells with broad-based budding. Blastomyces helicus does not produce conidia in culture, but it forms variably shaped yeast-like cells in short chains at temperatures between 33°C and 40°C (4).

Historically, the genus Emmonsia comprised two species, Emmonsia parva and Emmonsia crescens, both associated with pulmonary disease (adiaspiromycosis) in small mammals. Reports of human infection are rare. The pathogenic form consists of large, thick-walled spherical structures, termed adiaspores. With the recent transfer of the type species, Emmonsia parva, to Blastomyces (4), the taxonomic status of Emmonsia crescens now needs to be resolved. Multilocus phylogenetic analysis has revealed that it is not closely related to Blastomyces (3, 4). Therefore, the taxon will either require transfer to a new genus or conservation of the genus Emmonsia, with Emmonsia crescens as the type species (4).

A new genus, Emergomyces, within the family Ajellomycetaceae has recently been created (3) to accommodate a number of novel human pathogens that had previously been described as “Emmonsia sp.” or “Emmonsia-like” fungi (11). This genus contains Emergomyces pasteurianus (formerly Emmonsia pasteuriana [12]) as the type species, and four newly introduced taxa, Emergomyces africanus (3), Emergomyces orientalis (13), Emergomyces canadensis, and Emergomyces europaeus (4). In vivo, these organisms produce small yeast cells that bud on a narrow base rather than adiaspores, enabling them to be distinguished from Emmonsia.

Almost all reported cases of Emergomyces infection, or “emergomycosis,” have occurred in HIV-infected individuals, often presenting as disseminated disease with cutaneous lesions. First isolated in Europe in 1994 (12), Emergomyces pasteurianus has since been found in India, China, and South Africa (14). Emergomyces africanus was described as an Emmonsia species when it was first isolated in 1995 (15). By 2017, over 80 cases had been diagnosed in South Africa (16), where it is now considered to be the most common endemic mycosis (14). Only one case each of Emergomyces europaeus and Emergomyces orientalis infections have so far been reported (13, 17), while Emergomyces canadensis has recently been described from four cases of invasive disease among immunocompromised individuals in western Canada and the United States (18).

The genus Paracoccidioides contains the etiologic agents of paracoccidioidomycosis, a disease endemic to Central and South America. Molecular analysis first led to the identification of three phylogenetic groups within Paracoccidioides brasiliensis, with different levels of divergence (19). One of these groups (PS3) was thought to be restricted to Colombia, while the other two (S1 and PS2) were distributed across most of South America. Subsequent work identified a fourth monophyletic group (Pb01), which showed significant morphological and sequence divergence from the other three groups (20). This group has been named Paracoccidioides lutzii (21). More recently, analysis of molecular variation led to the identification of a fifth group restricted to Venezuela (PS4) (22). Turissini et al. (23) have proposed that the use of the name Paracoccidioides brasiliensis sensu stricto should be restricted to the monophyletic group, formerly known as S1. These authors have also proposed that the three other phylogenetic groups within the Paracoccidioides brasiliensis species complex, namely Paracoccidioides americana (PS2), Paracoccidioides restrepiensis (PS3), and Paracoccidioides venezuelensis (PS4), should be elevated to species status (23). Paracoccidioides americana and Paracoccidioides venezuelensis have both been found in Venezuela, and while Paracoccidioides restrepiensis was thought to be confined to Colombia, it has also been found in Venezuela. Although these molecular siblings differ in their geographic distribution, they lack distinguishing morphological characteristics that allow them to be differentiated during routine diagnostic laboratory testing.

The etiologic agents of dermatophytosis, together with many of their nonpathogenic relatives, have long been classified in three genera, Trichophyton, Microsporum, and Epidermophyton, in the family Arthrodermataceae of the order Onygenales. These familiar anamorph names were associated with the historic teleomorph genera Arthroderma and Nannizzia (24). Multilocus phylogenetic analysis has demonstrated that Trichophyton is polyphyletic, and this has resulted in the recognition of seven genera of dermatophytes and dermatophyte relatives (25). Under this proposal, almost all anthropophilic dermatophytes are retained in the genera Trichophyton and Epidermophyton, together with several zoophilic species that regularly infect humans. The genus Microsporum is now restricted to Microsporum canis and some closely related species. Most geophilic species and those zoophilic species that are rare causes of human disease are now divided among Arthroderma, Lophophyton, Paraphyton, and Nannizzia (25).

Molecular analysis has demonstrated that Sporothrix schenckii, the etiologic agent of sporotrichosis in humans and animals, is a complex of numerous phylogenetic species that tend to cluster in distinct geographic regions (26, 27). Species associated with human infection include Sporothrix brasiliensis, Sporothrix globosa, Sporothrix luriei, and Sporothrix schenckii sensu stricto (28). Other members of the Sporothrix schenckii complex that have seldom been reported to cause infection include Sporothrix pallida and a new species, Sporothrix chilensis, which has recently been reported from a case of onychomycosis (29).

Historically, the most common fungal etiologic agents of black-grain mycetoma were classified in the genus Madurella in the order Sordariales. These fungi often fail to sporulate in culture or required prolonged incubation to induce sporulation. With the advent of molecular methods, it became possible to resolve the phylogenetic and taxonomic relationships among these fungi, and it was demonstrated that Madurella mycetomatis and “Madurella grisea” were unrelated. Furthermore, isolates previously misidentified as Madurella mycetomatis have been found to belong to the sibling species, Madurella pseudomycetomatis, Madurella fahalii, and Madurella tropicana (30). Based on sequence analysis, the taxonomic position of Madurella grisea was changed to the order Pleosporales, and it was renamed Trematosphaeria grisea (31). More recently, Borman et al. (32) have studied isolates deposited in the National Collection of Pathogenic Fungi (NCPF; Bristol, UK) or the Institut Pasteur Culture Collection (UMIP; Paris, France) that fulfilled the historical characteristics of Madurella grisea. Phylogenetic analysis using up to five loci identified two new species in a novel pleosporalean genus, Emarellia grisea and Emarellia paragrisea (32).

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 reported in the years 2016 and 2017. 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, molecular analysis enabled multiple monophyletic clades of novel cryptic or sibling species to be detected within large collections of existing well-established taxa of pathogens. In the absence of biological or significant morphological differences between clades and no consensus about the degree of DNA sequence concordance required for two fungal isolates to be considered the same or different species, it seems reasonable for clinical and public health laboratories to follow expert recommendations (33) to group these cryptic or sibling species together as a “species complex.”

To illustrate this point, consider the recent proposal that Cryptococcus neoformans be divided into two species and Cryptococcus gattii into five species. This resulted from a multilocus sequence typing (MLST)-based phylogenetic analysis of 115 strains (34). As Kwon-Chung et al. (35) have pointed out, other studies have revealed more genetic variation than can be encompassed in only seven species; the proposal for seven species is therefore premature. These authors have recommended using the terms “Cryptococcus neoformans species complex” and “Cryptococcus gattii species complex” as a practical intermediate step, rather than creating more species, thus recognizing genetic variation without creating confusion (35).

Together with recent developments in molecular phylogenetic analysis, the application of the “one fungus = one name” concept 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 for the manufacturers of commercial identification systems, to be aware of these changes and to update their databases as required. The impact of these changes on medical practice has received less attention, but clinician education will be essential for their acceptance. To this end, periodic updates of the lists provided here will be needed.