Biol. Rev. (2019), pp. 000–000. 1 doi: 10.1111/brv.12510 Fungal evolution: major ecological adaptations and evolutionary transitions Miguel A. Naranjo-Ortiz1 and Toni Gabaldon´ 1,2,3∗ 1Department of Genomics and Bioinformatics, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, Barcelona 08003, Spain 2 Department of Experimental and Health Sciences, Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain 3ICREA, Pg. Lluís Companys 23, 08010 Barcelona, Spain ABSTRACT Fungi are a highly diverse group of heterotrophic eukaryotes characterized by the absence of phagotrophy and the presence of a chitinous cell wall. While unicellular fungi are far from rare, part of the evolutionary success of the group resides in their ability to grow indefinitely as a cylindrical multinucleated cell (hypha). Armed with these morphological traits and with an extremely high metabolical diversity, fungi have conquered numerous ecological niches and have shaped a whole world of interactions with other living organisms. Herein we survey the main evolutionary and ecological processes that have guided fungal diversity. We will first review the ecology and evolution of the zoosporic lineages and the process of terrestrialization, as one of the major evolutionary transitions in this kingdom. Several plausible scenarios have been proposed for fungal terrestralization and we here propose a new scenario, which considers icy environments as a transitory niche between water and emerged land. We then focus on exploring the main ecological relationships of Fungi with other organisms (other fungi, protozoans, animals and plants), as well as the origin of adaptations to certain specialized ecological niches within the group (lichens, black fungi and yeasts). Throughout this review we use an evolutionary and comparative-genomics perspective to understand fungal ecological diversity. Finally, we highlight the importance of genome-enabled inferences to envision plausible narratives and scenarios for important transitions. Key words: fungi, ecological adaptations, evolutionary transitions, fungal niches, fungal terrestrialization, fungal diversification. CONTENTS I. Introduction .............................................................................................. 2 II. In the beginning: early fungal evolution .................................................................. 2 III. Down to earth: terrestrialization in fungi ................................................................. 3 IV. Fungi and other microbial eukaryotes .................................................................... 6 (1) ‘Fungus fungo lupus’: mycoparasitism in fungi ....................................................... 6 (2) Fungi and protozoans ................................................................................ 8 V. Fungi and animals ........................................................................................ 10 (1) Overview ............................................................................................. 10 (2) Obligate parasites of animals ......................................................................... 11 (3) Facultative parasites of animals ....................................................................... 12 (4) Fungal commensals of animals ....................................................................... 14 VI. The fungus–plant biome: ecological interactions between plants and fungi .............................. 15 (1) Overview ............................................................................................. 15 (2) Mycorrhizae and plant commensal associates ........................................................ 15 (3) Plant parasitism ...................................................................................... 16 (4) Wood rot fungi ....................................................................................... 18 VII. More than the sum of their parts: lichenized fungi ....................................................... 18 * Address for correspondence (Tel: +34 616 953 333; E-mail: [email protected]). Biological Reviews (2019) 000–000 © 2019 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. 2 Miguel A. Naranjo-Ortiz and Toni Gabaldon´ VIII. Black fungi ............................................................................................... 19 IX. The yeast lifestyle ........................................................................................ 21 X. Concluding remarks ...................................................................................... 23 XI. Conclusions .............................................................................................. 23 XII. Acknowledgments ........................................................................................ 24 XIII. References ................................................................................................ 24 I. INTRODUCTION secretome that allows them to extract nutrients, even from highly polymerized and often very hydrophobic compounds, The kingdom Fungi is a highly diverse clade of eukaryotes such as cellulose or lignin, which is very difficult for other found in virtually all environments, particularly in terrestrial microbes (Richards & Talbot, 2013; Boddy & Hiscox, 2016; ecosystems (Richards, Leonard & Wideman, 2017; Stajich, Hiscox, O’Leary & Boddy, 2018). Fungi can propagate 2017). Fungi play key roles in nutrient cycling, can act over long distances by producing non-motile spores that as predators, pathogens and parasites of myriad other may or may not be the product of mating between two organisms, and can be found living in symbiotic associations compatible hyphae (Golan & Pringle, 2017). We will refer with plants, algae, animals and other organisms. Some to these general features as the mould lifestyle. Despite important groups of fungi (mostly mushrooms and lichens) being widespread, this lifestyle is not ancestral within the produce macroscopic structures that have been the focus of kingdom (Spatafora et al., 2017; Stajich, 2017) and fungi extensive morphological, cytological and biochemical studies display many other forms of cellular organization and (Lawrey & Diederich, 2009; Taylor & Ellison, 2010; de ecological lifestyles (Richards, Leonard & Wideman, 2017). Mattos-Shipley et al., 2016; Grube & Wedin, 2016). Outside Nevertheless, the mould paradigm is useful as a reference these groups, most fungi have been traditionally studied using point from which to discuss morphological and ecological culture-based microbiological techniques or by assessing the variations present across the kingdom. In this review, symptoms and specialized structures they produce on their we synthesize current knowledge on the major ecological hosts or symbiotic partners. During the past two decades, adaptations and evolutionary transitions within fungi. We the genomic revolution has positively impacted the field of define an evolutionary transition as the acquisition – within mycology, which has rapidly and enthusiastically embraced a lineage – of a new, sufficiently distinct lifestyle from a a comparative genomic paradigm to an extent that is still rare previous state. Well-known examples of such transitions in other disciplines (Cuomo & Birren, 2010). The advent of include the acquisition of a parasitic lifestyle from free-living genome and transcriptome sequencing has enabled the study ancestors, the establishment of symbiosis (e.g. lichens), or of virtually any fungal group, and this has been reflected in an radical changes in body-plan or cellular organization. When explosion of research covering a growing list of fungal species possible, we place such transitions within an evolutionary from diverse lineages. Last, but not least, environmental framework, explaining how zoosporic fungi evolved from sequencing studies are revealing a new dimension of fungal motile eukaryvorous parasitoids to moulds, and how from biology. Barcoding-based approaches have been used in those two lifestyles different groups of fungi have shaped the last two decades to study the diversity of particular their relationships with other groups of organisms and have components of environmental fungal communities, such adapted to novel ecological niches. We focus on describing as ectomycorrhizal fungi (Lilleskov et al., 2002; Landeweert phenotypic and genomic generalities, taxonomic diversity, et al., 2003; Cox et al., 2010); or to assess fungal composition evolutionary trends and culture-independent environmental in particular environments (Tedersoo et al., 2014; Xu, 2016; information for each of the discussed ecological lifestyles. Yahr, Schoch & Dentinger, 2016). Mycologists have started to embrace the use of single-cell-based techniques, although tentatively due to incompatibilities of filamentous growth II. IN THE BEGINNING: EARLY FUNGAL with cell-sorting approaches (Ahrendt et al., 2018). Each of EVOLUTION these approaches presents specific limitations, but collectively they provide an emerging picture of where fungi are, who Inferring the potential lifestyle of the last common fungal they are, and how they have become what they are. ancestor