Fungal Evolution: Cellular, Genomic and Metabolic Complexity
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Biol. Rev. (2020), 95, pp. 1198–1232. 1198 doi: 10.1111/brv.12605 Fungal evolution: cellular, genomic and metabolic complexity † Miguel A. Naranjo-Ortiz1* and Toni Gabaldón1,2,3 * 1Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, Barcelona, 08003, Spain 2Department of Experimental Sciences, Universitat Pompeu Fabra (UPF), Dr. Aiguader 88, 08003, Barcelona, Spain 3ICREA, Pg. Lluís Companys 23, 08010, Barcelona, Spain ABSTRACT The question of how phenotypic and genomic complexity are inter-related and how they are shaped through evolution is a central question in biology that historically has been approached from the perspective of animals and plants. In recent years, however, fungi have emerged as a promising alternative system to address such questions. Key to their ecological success, fungi present a broad and diverse range of phenotypic traits. Fungal cells can adopt many different shapes, often within a single species, providing them with great adaptive potential. Fungal cellular organizations span from unicellular forms to complex, macroscopic multicellularity, with multiple transitions to higher or lower levels of cellular complexity occurring throughout the evolutionary history of fungi. Similarly, fungal genomes are very diverse in their architecture. Deep changes in genome organization can occur very quickly, and these phenomena are known to mediate rapid adap- tations to environmental changes. Finally, the biochemical complexity of fungi is huge, particularly with regard to their secondary metabolites, chemical products that mediate many aspects of fungal biology, including ecological interactions. Herein, we explore how the interplay of these cellular, genomic and metabolic traits mediates the emergence of complex phenotypes, and how this complexity is shaped throughout the evolutionary history of Fungi. Key words: fungi, complexity, multicellularity, secondary metabolism, genome evolution CONTENTS I. Introduction ......................................................................1198 II. Cellular complexity .................................................................1199 (1) Unicellular fungi ................................................................1199 (2) The hyphal cell as a living pipe .....................................................1200 (3) The mycelium as a living network ...................................................1203 (4) Complex multicellularity ..........................................................1205 III. Genome complexity ................................................................1207 (1) Hybridization ..................................................................1207 (2) Heterokaryosis ..................................................................1208 (3) Aneuploidy ....................................................................1210 (4) Polyploidy .....................................................................1211 IV. Metabolic complexity ...............................................................1211 (1) Secondary metabolites in fungal biology ..............................................1213 (2) Metabolic gene clusters ...........................................................1213 * Address for correspondence (Tel:+34 933160281; E-mail: [email protected]). *Present address: Clark University, Biology Department, Cathy ’83 and Marc ’81 Lasry Center for Biosciences, 15 Maywood Street, 01610 Worcester, Massachussets, U.S.A. † Present address: Barcelona Supercomputing Centre (BSC-CNS) and Institute for Research in Biomedicine (IRB), Barcelona, Spain Biological Reviews 95 (2020) 1198–1232 © 2020 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. Evolution of fungal complexity 1199 (3) Genes on the move: horizontal gene transfer in Fungi ....................................1216 (4) From genomes to pangenomes .....................................................1217 V. Concluding remarks ................................................................1219 VI. Conclusions .......................................................................1220 Acknowledgements .................................................................1220 VII. References ........................................................................1220 I. INTRODUCTION metabolites and opens up a wide array of phenotypes in their interactions with other organisms. Although less often considered than animals or plants, the This cellular and biochemical diversity is ultimately ecological success of Fungi is equally impressive, and com- reflected in the highly dynamic nature of fungal genomes. prises a broad diversity of lineages and life styles that popu- Fungi are ideal subjects for genomic studies, since they tend late every corner of our planet (Naranjo-Ortiz & Gabaldón, to have highly compact genomes [theyrarely reach genome 2019a,b), with most estimates predicting millions of extant sizes of giga base pairs (Gbp)], are usually haploid, and can fungal species (Hawksworth, 2001; Blackwell, 2011; Aime & often be grown in axenic conditions. Consequently, the num- Brearley, 2012; Hawksworth & Lücking, 2017). At the heart ber of fully sequenced fungal genomes is now in the order of of this success lies a series of interwoven cellular and bio- thousands. Hence, in combination with decades of studies in chemical traits, which are ultimately determined by the genetics, biochemistry and cell biology, fungal genomics is genome. The question of how phenotypic complexity is revolutionizing our understanding of this group related to genomic complexity, and how these change during (Scazzocchio, 2014). The study of the genetic repertoire of evolution, historically has been approached from the per- a growing diversity of fungi is unveiling a metabolic land- spective of animals and plants. However, in recent years scape far wider and intriguing than we could have imagined fungi have increasingly been the focus of research aiming to two decades ago. In addition, evolutionary genomic analyses understand the origin and evolution of genomic and mor- are not only helping us to identify the components in the phological complexity. Fungi originated from a flagellated mycelial and multicellular fungal machinery, but also are ancestor, but most current diversity encompasses non- uncovering what processes may drive the evolution of fungal flagellated cells that often grow in a form of simple multicel- genomes. In this respect, fungi have recently challenged evo- lularity called the mycelium, a true cellular network that lutionary paradigms adopted from the study of animals and sometimes extends over large areas. From this mycelial plants. For instance, non-vertical evolutionary processes such growth, many fungal organisms can switch to a unicellular as horizontal gene transfer or hybridization seem to be far growth form (e.g. yeast), often depending on the environmen- more common in fungi than previously anticipated, and pro- tal conditions or on the stage of their life cycle. In several lin- karyotic paradigms such as that of pangenomes seem also to eages throughout the fungal tree of life, mycelial growth has be applicable to fungi. In this review, we discuss recent been abandoned, often completely but sometimes only to be advances in our understanding of the evolution of phenotypic recovered later. Some other lineages have taken multicellu- and genomic complexity within the fungal kingdom, focusing larity one step further, originating complex fruiting bodies on the cellular and biochemical traits that have driven the whose macroscopic morphologies compete in intricacy and success of fungi in the biosphere. In so doing we emphasize, beauty with those of plants and animals. Complex multicellu- when known, the genomic features that underlie those traits larity implies coordination of different cell types to form tis- as well as their evolution. sues and the existence of a tightly regulated developmental program. To achieve such levels of complexity, fungi have developed specific structural and regulatory systems that are still not fully understood. From a biochemical perspec- II. CELLULAR COMPLEXITY tive, fungi present a truly vast diversity, with levels of com- plexity that are comparable or surpass those of other The last fungal common ancestor was likely a flagellated, uni- eukaryotic clades. Fungal organisms are osmotrophs and cellular organism with a saprotrophic or parasitoid lifestyle their cells are generally in contact with the surrounding envi- (James, Porter & Martin, 2014; Karpov et al., 2014a; Powell & ronment. The relationship of a fungus with its immediate Letcher, 2014; Naranjo-Ortiz & Gabaldón, 2019b). How- environment is defined by an array of secreted proteins and ever, very early in the evolution of fungi, a shift towards more metabolites. The origin and diversification of these secreted complex forms of cellular organization occurred. This shift metabolites is of great practical interest, given the often pow- made possible the conquest of non-aquatic environments, erful effects they have on other organisms. Furthermore, pro- leading to loss of the flagellum in several