Genome Fungal Species Concepts in the Genomics Era Journal: Genome Manuscript ID gen-2020-0022.R1 Manuscript Type: Current opinion Date Submitted by the 27-May-2020 Author: Complete List of Authors: Xu, Jianping; McMaster University, Department of Biology Keyword: species concepts, yeasts, molds, mushrooms, trait evolution Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : Draft https://mc06.manuscriptcentral.com/genome-pubs Page 1 of 31 Genome 1 Fungal Species Concepts in the Genomics Era 2 3 Jianping Xu 4 Department of Biology, McMaster University, 1280 Main Street West, Hamilton, Ontario, L8S 5 4K1, Canada; [email protected] 6 Draft 1 https://mc06.manuscriptcentral.com/genome-pubs Genome Page 2 of 31 7 Abstract 8 The 140,000 or so fungal species reported so far are heterogeneously defined based on varying 9 criteria such as morphological, physiological, mating, and/or molecular features. Incongruences 10 are common among traits used to separating closely related species and it is often difficult to 11 compare fungal taxonomic groups defined based on different species recognition criteria. Though 12 DNA sequence-based classification and identification have been made, a consensus has not been 13 reached, primarily due to intrinsic limitations in the proposed one or a few genes. Here, I argue 14 that the fundamental reason for the observed inconsistencies is that speciation is a stochastic 15 process with the emergence and fixation of different traits influenced differently by many non- 16 deterministic factors such as population Draftsize, random mutation, mode(s) of reproduction, selection 17 imposed by interacting biotic and abiotic factors, and chance events. Each species concept attempts 18 to capture one or a few traits emerged in the continuous process of speciation. I propose that a 19 genome sequence-based classification and identification system could unify and stabilize fungal 20 taxonomy and help integrate taxonomy with other fields of fungal biology. The genomic species 21 concept could be similarly argued for other groups of eukaryotic microbes as well as for plants 22 and animals. 23 24 Key words: species concepts, yeasts, molds, mushrooms, trait evolution, genome sequence, 25 genome species concept 2 https://mc06.manuscriptcentral.com/genome-pubs Page 3 of 31 Genome 26 1. Introduction 27 Species is a fundamental term in biology. However, species can mean different things for 28 scientists in different fields and/or working on different groups of organisms. While most 29 biologists know approximately what species means to them, no one definition has satisfied all 30 biologists. In macro-organisms such as plants and animals, features that can be seen by the human 31 naked eye have been the dominant criteria used to define species. Indeed, most species of plants 32 and animals were primarily recognized based on macro-morphological features by the end of the 33 19th century. However, due to their intrinsic diversity, different sets of morphological features have 34 been used to define species for different groups of plants and animals. In contrast, taxonomy of 35 microscopic organisms such as those in the Bacteria and Archaea Domains did not start until the 36 end of the 19th century when methods forDraft identifying their micro-morphological features, and later 37 their structural, biochemical, and genetic features, became available. Fungal taxonomy contains 38 elements and criteria used for both macro-organisms and micro-organisms. For macroscopic fungi 39 such as those that produce fruiting bodies (e.g. mushrooms) that are visible to the naked human 40 eye, the morphological species concept dominated this group of fungi in the early literature and 41 their taxonomic history largely paralleled those of plants and animals, dating back to the 18th 42 century (Linnaeus 1753). In contrast, for microscopic fungi such as yeasts and filamentous molds, 43 their taxonomic history parallels those of prokaryotes, with major advancements starting around 44 the early 20th century (Kurtzman et al. 2011; Kendrick 2014). 45 Over the past century, a variety of species concepts have been proposed and applied to define 46 species in different groups of organisms. These include the quasi-species concept for viruses 47 (Domingo and Perales 2019); the micro-morphological, physiological, ecological, and DNA-DNA 48 hybridization -based species concepts for Bacteria and Archaea (Murray and Holt 2001); and the 3 https://mc06.manuscriptcentral.com/genome-pubs Genome Page 4 of 31 49 morphological, phylogenetic, evolutionary, reproductive species concepts in eukaryotes, including 50 fungi (Cai et al. 2011; Zachos 2016). However, different groups of fungi (and other organisms) 51 are often defined based on different species concepts using different criteria, making comparative 52 studies among species often difficult to perform. In addition, the same group of organisms may 53 show different patterns of grouping using different sets of criteria or species concepts (e.g. Singer 54 1986; Dettman et al. 2001; Kwon-Chung et al. 2017). As a result, taxonomic revision is a common 55 feature in the current fungal taxonomic literature, often involving moving organisms into different 56 genera and even families (e.g. Cai et al., 2011; Wu et al. 2016; indexfungorum.org). In this paper, 57 I explore the potential reasons for the inconsistency among the species concepts and propose a 58 potential solution for moving forward. I first briefly describe the commonly used fungal species 59 concepts. I then outline the major changesDraft that could happen during speciation and how those 60 changes may be related to the different fungal species concepts. This is followed by highlighting 61 a few features of fungi that distinguish them from plants, animals, and prokaryotes and how these 62 features may have contributed to complications in fungal taxonomy and fungal species recognition. 63 I finish by discussing how genomics can help bring the diverse fungal species concepts together 64 and integrate fungal taxonomy into the broad field of fungal biology. 65 66 2. Commonly Used Species Concepts in Fungi 67 Both macro- and micro-morphological features have dominated the fungal taxonomy 68 literature, especially in its early history (Singer 1986). Some fungal species are defined completely 69 based on macro-morphological and/or microscopic features, while others include morphological 70 features for at least part of their species descriptions (e.g. Linnaeus 1753; Singer 1986; Kurtzman 71 et al. 2011; Wu et al. 2016). Indeed, dichotomous keys for species recognition based on 4 https://mc06.manuscriptcentral.com/genome-pubs Page 5 of 31 Genome 72 morphological features permeate the fungal taxonomy literature even today (e.g. Zheng et al. 73 2019). Though not intended nor substantiated, such dichotomous keys often give the impression 74 for the order on the emergence of those specific morphological traits. 75 Since the beginning of the 20th century, with advances in technology and biomedical 76 sciences, other features have been progressively introduced to help define species, including fungal 77 species. Those features include ecological factors (both abiotic and biotic interacting factors), 78 physiology, reproduction, and DNA sequences. Parallel to these developments were expanded 79 discussions and conceptual changes in how species should be defined and recognized. There are 80 over 30 species concepts in the biological literature (Zachos 2016), including common ones such 81 as the morphological, ecological, phenetic, biological, recognition, evolutionary, genotypic 82 cluster, and phylogenetic species conceptsDraft that have been applied to delineate fungal species 83 (Table 1). These concepts emphasize different but often overlapping features of organisms. Each 84 of the criteria has been and continues to be featured in defining fungal species. Example literatures 85 showing fungi defined based on different criteria and using different species concepts are presented 86 in Table 1. These literatures reported some of the environmentally, economically, and medically 87 very important fungi, including the cultivated button mushroom Agaricus bisporus (biological 88 species concept, Kerrigan et al. 1994; recognition species concept, Callac et al. 2003); the common 89 indoor mold Penicillium chrysogenum (genotypic cluster species concept, Banke et al. 1997); the 90 wild gourmet mushrooms Tricholoma nauseosum from Scandinavia (ecological species concept, 91 Kytövuori 1988) and Thelephora ganbajun from Southwestern China (morphological species 92 concept, Zang 1988); and the human fungal pathogens in the genus Cryptococcus such as 93 Cryptococcus deneoformans and Cryptococcus decagattii and other sister species (phylogenetic 94 species concept, Hagen et al. 2015). 5 https://mc06.manuscriptcentral.com/genome-pubs Genome Page 6 of 31 95 Since the late 1990s, phylogenetic analyses based on DNA sequences at one or multiple 96 loci have been increasingly used to define fungal species (Taylor et al. 2000; Schoch et al. 2012). 97 In an increasing number of cases, DNA sequence or genotype information has become the main 98 or only information used to separate strains into distinct species (e.g. Weir et al. 2012; Hagen et 99 al. 2015). This approach has led to the identification of a large number of new and cryptic species 100 within previously recognized fungal species. For example, a recent review of 51 studies involving