The impact of changing nomenclatural rules
When in 2011 it was decided to abandon the dual names for fungi (Hawksworth 2011, Hawksworth et al. 2011), via the movement known as ‘One-Fungus-One Name’, we all expected that nomenclature would become more simple and stable, and that has been the case for many fungi. However, there are also cases where the opposite has happened. Particularly the recent proposal of ‘Nakaseomyces’ for Candida glabrata (Takashima & Sugita, 2022) has aroused irritation among clinicians. Nomenclature has become a fiercely debated topic (Borman & Johnson 2023, de Hoog et al. 2023, Denning 2023, Kidd et al. 2021, 2023), even though procedures to protect names have been put in place to avoid unfortunate consequences. How is that possible?
1F1N has been enabled by advances in molecular science. Asco- and basidiomycetous fungi are unique among the microbes by displaying separate sexual and asexual morphs, often displayed in different habitats: the sexual morph is mostly found under relatively harsh conditions, while rapid asexual reproduction is enhanced by the easy, nutrient-rich conditions in vitro. That is why after the times of Louis Pasteur, mycology has changed enormously: classification in the 19th century was by sexual morphology, while in the 20st century asexual morphology in culture became preponderant. Revealing the coherence between the two became a fundamental research focus. For the name of the fungus in all its morphs, the name given to the sexual one was preferred – until 2011, when the molecular approach took over.
The genome of the sexual and asexual morphs is identical. In 2011, it was recommended to use the oldest name, whether sexual or asexual, because this was apparently the easiest to discover. An old name also would have less risk of being replaced by younger synonyms. All of this marks a totally logical and understandable development. Almost the entire scientific community has welcomed 1F1N. However, when this was adopted, already tens of thousands species had been described, and these all had to be re-evaluated according to the new rules. The principle that has enabled 1F1N to be widely adopted, namely DNA sequencing, also determines the current phylogenetic method of classification. Fungi with similar morphology can be totally unrelated. When two species are remote, their behavior is likely to be very different, or the genetic background of similar behaviour is different, which are good reasons not to classify them in a single genus.
An example of morphological similarity of unrelated fungi is found in Madurella, a non-sporulating genus of fungi causing human mycetoma. The two classical species, M. mycetomatis and M. grisea, merely exhibit melanized hyphae in culture and were only distinguished by an extracellular pigment, produced by M. mycetomatis and absent in M. grisea. Sequencing data revealed that the former is a member of the subclass Sordariomycetes, and the latter of Dothideomycetes – thus extremely different. Madurella mycetomatis is a desert soil fungus, while M. grisea is repeatedly found in water in temperate climates, and the similarity in pathology is coincidental. Everyone agreed that there is no relation between the two, and they should not be classified in the same genus. Madurella grisea was therefore reclassified, as Trematosphaeria grisea (Ahmed et al. 2018).
The problem of large differences between indistinguishable phenotypes is particularly pressing in ascomycetous yeasts. Reshuffling of e.g. some Candida species on phylogenetic grounds may prove to be unavoidable. A second problem is that yeast taxonomists after 2011 adhered to the sexual, ‘holomorph’ name as the species reference point, rather than the oldest name. This approach differs from that maintained in the rest of the fungal Kingdom. Application of the same rule everywhere requires change: see for example the numerous ascomycetous yeasts that have older, proven synonyms with valid types. Luckily, names can also be proposed for conservation, as was done with Coccidioides posadasii where no less than seven older, valid names were available (de Hoog et al. 2023). Procedures to protect names where changes would be disadvantageous are available. Despite this, we have to be prepared that particularly in the yeasts we will go through a period of change before we will reach stability in the future.
Name changes are generally proposed in the framework of good taxonomic work focusing on particular genera or parts thereof. The phylogenetic translocation is done because classical species appear to have similarities elsewhere rather than to e.g. Candida. However, phylogenetic trees are relative, and thus vary with what is included for comparison. General overviews including all ascomycetous yeasts, similar to the publications of e.g. Groenewald et al. (2023) and Opulente et al. (2023) are less susceptible to such taxon sampling effects, and these can be followed by detailed studies with balanced species selection. The reallocation of yeast species is certainly global effort which needs the support of the entire research and user community. We have installed a committee of ISHAM, ECMM and FDLC*, where these data can be combined and discussed by united experts and users. Hopefully, this will lead to optimal recommendations for clinical genus and species names for the years to come. The continually updated list can be found at www.atlasclinicalfungi.org/nomenclature. The list can be included as an Appendix to the International Code of Nomenclature for algae, fungi, and plants after approval by the pertinent nomenclature committees. Membership of above Nomenclatural Committee is open to all interested mycologists.
*ISHAM = International Society for Human and Animal Mycology (https://www.isham.org); ECMM = European Confederation of Medical Mycology (https://www.ecmm.info); FDLC = Fungal Diagnostic Labs Consortium (https://labs.pathology.jhu.edu).