C. P. Kurtzman's Evolving Concepts of Species, Genus and Higher Categories

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C. P. Kurtzman's Evolving Concepts of Species, Genus and Higher Categories FEMS Yeast Research, 18, 2018, foy103 doi: 10.1093/femsyr/foy103 Advance Access Publication Date: 20 September 2018 Minireview MINIREVIEW C. P. Kurtzman’s evolving concepts of species, genus Downloaded from https://academic.oup.com/femsyr/article/18/8/foy103/5104380 by guest on 29 September 2021 and higher categories Marc-Andre´ Lachance Department of Biology, University of Western Ontario, London, ON N6A 5B7, Canada Corresponding author: Tel. 1-519-661-3752; E-mail: [email protected] One sentence summary: Cletus P. Kurtzman revolutionised yeast systematics; this is an overview of the evolution of his thoughts on yeast species, genera and higher categories. Editor: Teun Boekhout ABSTRACT Cletus P. Kurtzman transformed the way yeast systematists practice their trade and how they perceive the yeast species. He redefined many genera of ascomycetous yeasts and provided a sound basis upon which to base higher taxonomic categories. Within his extraordinary corpus lies a trail of elements that can be used to reconstruct his evolving vision of the concepts that underlie the species and the genus, rarely set in a theoretical framework. While occasionally tipping his hat to the biological and phylogenetic species, Kurtzman espoused a concept founded primarily on genetic distance, even when claiming otherwise. In contrast, his notion of genus incorporated components of both genetic distance and phylogenetic structure, and possibly a size consideration. A phylogenetic approach predominated with higher taxa. Keywords: Cletus P. Kurtzman; yeast species; yeast genus; genetic distance; phylogenetics; Ascomycetes INTRODUCTION Kurtzman’s laboratory lived up to the highest standards and implemented forefront methodologies for imaging, ascospore ‘I have never done anything “useful”. No discovery of mine has dissection or nucleic acid analyses. He inherited from Wicker- made, or is likely to make, directly or indirectly, for good or ill, the ham a sense of minutious diligence that continued throughout least difference in the amenity of the world.’ his career (Wickerham, Kurtzman and Herman 1969). His later writings show an immense knowledge of the properties of vari- While this modest confession may be appropriate for some, ous genes in terms of evolutionary rates, concordance with other it holds true neither for its author, mathematician G.H. Hardy genes, or the best primers or cycling conditions to obtain im- (1940), nor for yeast systematist Cletus P. Kurtzman. So much peccable amplifications. The designation NRRL on a sequence could be said about Kurtzman’s monumental opus. In my task of deposit continues to be a certificate of quality. sieving through his writings to unravel his thought on the con- Ihavealluded(Lachance2018) to Clete’s generosity as cepts of species, genus and higher taxa, I was reminded of many a colleague, manifested, inter alia, in naming many taxa in other highlights of his career. Of the greatest importance was his honour of other yeast systematists. These recognitions were implementation and promotion of DNA sequencing, which gave sometimes granted in the face of criticisms, nay disparage- us a barcode identification system for all ascomycetous yeasts ments. Characterisation of nomenclatural choices as ‘point- (Kurtzman and Robnett 1998a). Although the term ‘barcode’ only less’, ‘taxonomically inept’ or ‘bordering on lunacy’ (Barnett appears late in his writings (Kurtzman 2010), Kurtzman (1994a)is 2004) still earned the critic an eponymous genus (Kurtzman, rightly credited as a pioneer of the approach (Hebert et al. 2003), Robnett and Basehoar-Powers 2008) consisting, perhaps ironi- which entails the creation of a comprehensive database of easily cally, of an eclectic brew of species formerly assigned to Pichia, accessible homologous sequences (Kurtzman and Robnett 1991). Received: 24 July 2018; Accepted: 19 September 2018 C FEMS 2018. All rights reserved. For permissions, please e-mail: [email protected] 1 2 FEMS Yeast Research, 2018, Vol. 18, No. 8 Zygohansenula, Hansenula, Williopsis and Endomycopsis. Of course, entiated the two (Kurtzman, Smiley and Baker 1975), as did dif- challenge and debate, not sycophantry, make for good science. ferences in DNA base composition. Part of Clete’s success stemmed from remaining undeterred by Following an eclipse of nearly three decades, morphology sceptics, although he was terribly displeased when I chose for resurfaced with the remarkable discovery (Kurtzman 2004)of a genus the name Diutina, meaningpermanent, to lament fre- mating and ascus formation in heterothallic strains what were quent name changes (Khunnamwong et al. 2015). Clete may reassigned to the genus Trichomonascus because the asci resem- have savoured the occasional taunt, portending the eventual bled those of Trichomonascus mycophagus. Living material for the split of my favourite genera, Metschnikowia, Starmerella and Wick- latter species was not available, but the ‘nearly identical unique erhamiella (e.g. Mendonc¸a-Hagler, Hagler and Kurtzman 1993; morphology of the sexual states of the new species and T. my- Kurtzman and Robnett 2007; Kurtzman et al. 2010). He settled cophagus leaves little doubt that they are closely related’. More the score posthumously (Kurtzman et al. 2018) with a broad phy- importantly, in the present context, species delineation was logeny of Metschnikowia in which all 30 species of large-spored entirely morphological: ‘Ascospore morphology clearly distin- Metschnikowia,mymagnum opus, were omitted. ‘Metschnikowia, guishes T. petasosoporus and T. mycophagus, despite lack of ver- Downloaded from https://academic.oup.com/femsyr/article/18/8/foy103/5104380 by guest on 29 September 2021 as presently recognized, may actually represent several gen- ification from gene sequences.’ era. The large-spored species [...] form a separate clade [...].’ Coincidentally, a well-supported phylogeny placing the large- Biological species spored group comfortably inside the genus Metschnikowia nearly In a fleeting foray into the world of Basidiomycetes, Kurtz- appeared in the same journal issue (Lee, Hsiang and Lachance man (1973) discovered mating reactions among strains identi- 2018). fied from growth responses as Cryptococcus laurentii. Although a complete sexual cycle was not documented, the mating pat- Species concepts terns suggested that the various strains represented more than one taxon. The mating strains were later resolved as Papiliotrema Mayden (1997) argued that most species concepts are an attempt flavescens, and the incompatible strains are now named Papil- to approximate the evolutionary concept, which views species iotrema laurentii, Vishniacozyma carnescens, Kwoniella heveanensis as communities that share a common fate over evolutionary or Filobasidium magnum—but not through Kurtzman’s doing (Liu time. Because of the temporal factor, detection of evolutionarily et al. 2016). The same strains were revisited (Baptist and Kurtz- cohesive units is not directly possible and must resort to other, man 1976) using isoenzyme electrophoresis and DNA base com- operational concepts. Darwin (1859) predicted that we would position, with the conclusion that they represented two taxa. one day ‘be freed from the vain search for the undiscovered and Morphology still prevailed: ‘Because the sexually reactive strains undiscoverable essence of the term species’. At a conference in cannot be separated by assimilation tests, we chose not to de- the early 2000s, Clete was apparently confident that the goal scribe them as a new species’. Discontinuities in the isoenzyme had been achieved. He opened the conversation with: ‘What’s and GC data were also used to assign the remaining strains a genus?’, implying, I believe, that the matter of the species was to species bearing three of the specific epithets listed above, a case closed. presage of the genetic species concept that will dominate Kurtz- man’s later work. Morphological species A morphological concept was implicit also in two taxonomic Theorists use the term morphology in the sense of Hennig’s studies of Saccharomycopsis species (Kurtzman and Wickerham (1966) holomorphology, which for yeasts includes both visual 1973; Kurtzman, Vesonder and Smiley 1974), even though het- appearance, growth responses or chemotaxonomic traits, what erothallic mating among strains of Saccharomycopsis crataegen- Kurtzman termed phenotype. Wickerham and Kurtzman (1971) sis and absence of mating with other species were said to be delineated two Saturn-spored Pichia species on scanning elec- a pivotal criterion in setting boundaries. Similarly, Kurtzman tron microscopy of the ascospores, although they did not explic- and Ahearn (1976) examined a group of heterothallic strains itly specify a species criterion. Spore ornamentation was also of Pichia and Candida species that physiologically resembled P. examined in Schwanniomyces (Kurtzman, Smiley and Baker 1972) spartinae, and kept them separate based on mating patterns. in the hope that it would reveal information on relationships The criterion was applied to P. kudriavzevii and P. terricola,which among species. However, two strains assigned to Schwanniomyces were mixed with mating types of several other Pichia or Candida persoonii differed in surface ornamentation, introducing an el- species (Kurtzman and Smiley 1976). Mating between P. kudri - ement of doubt. Growth test responses were added to the cir- avzevii and strains of Candida krusei or C. sorbosa led to the con- cumscription of the species. A similar morphological
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