Cécile Gueidan

The ascomycota tree of life: A phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits

We present a 6-gene, 420-species maximum-likelihood phylogeny of Ascomycota, the largest phylum of Fungi. This analysis is the most taxonomically complete to date with species sampled from all 15 currently circumscribed classes. A number of superclass-level nodes that have previously evaded resolution and were unnamed in classifications of the Fungi are resolved for the first time. Based on the 6-gene phylogeny we conducted a phylogenetic informativeness analysis of all 6 genes and a series of ancestral character state reconstructions that focused on morphology of sporocarps, ascus dehiscence, and evolution of nutritional modes and ecologies. A gene-by-gene assessment of phylogenetic informativeness yielded higher levels of informativeness for protein genes (RPB1, RPB2, and TEF1) as compared with the ribosomal genes, which have been the standard bearer in fungal systematics. Our reconstruction of sporocarp characters is consistent with 2 origins for multicellular sexual reproductive structures in Ascomycota, once in the common ancestor of Pezizomycotina and once in the common ancestor of Neolectomycetes. This first report of dual origins of ascomycete sporocarps highlights the complicated nature of assessing homology of morphological traits across Fungi. Furthermore, ancestral reconstruction supports an open sporocarp with an exposed hymenium (apothecium) as the primitive morphology for Pezizomycotina with multiple derivations of the partially (perithecia) or completely enclosed (cleistothecia) sporocarps. Ascus dehiscence is most informative at the class level within Pezizomycotina with most superclass nodes reconstructed equivocally. Character-state reconstructions support a terrestrial, saprobic ecology as ancestral. In contrast to previous studies, these analyses support multiple origins of lichenization events with the loss of lichenization as less frequent and limited to terminal, closely related species.

A class-wide phylogenetic assessment of Dothideomycetes

We present a comprehensive phylogeny derived from 5 genes, nucSSU, nucLSU rDNA, TEF1, RPB1 and RPB2, for 356 isolates and 41 families (six newly described in this volume) in Dothideomycetes. All currently accepted orders in the class are represented for the first time in addition to numerous previously unplaced lineages. Subclass Pleosporomycetidae is expanded to include the aquatic order Jahnulales. An ancestral reconstruction of basic nutritional modes supports numerous transitions from saprobic life histories to plant associated and lichenised modes and a transition from terrestrial to aquatic habitats are confirmed. Finally, a genomic comparison of 6 dothideomycete genomes with other fungi finds a high level of unique protein associated with the class, supporting its delineation as a separate taxon.

Families of Dothideomycetes

Dothideomycetes comprise a highly diverse range of fungi characterized mainly by asci with two wall layers (bitunicate asci) and often with fissitunicate dehiscence. Many species are saprobes, with many asexual states comprising important plant pathogens. They are also endophytes, epiphytes, fungicolous, lichenized, or lichenicolous fungi. They occur in terrestrial, freshwater and marine habitats in almost every part of the world. We accept 105 families in Dothideomycetes with the new families Anteagloniaceae, Bambusicolaceae, Biatriosporaceae, Lichenoconiaceae, Muyocopronaceae, Paranectriellaceae, Roussoellaceae, Salsugineaceae, Seynesiopeltidaceae and Thyridariaceae introduced in this paper. Each family is provided with a description and notes, including asexual and asexual states, and if more than one genus is included, the type genus is also characterized. Each family is provided with at least one figure-plate, usually illustrating the type genus, a list of accepted genera, including asexual genera, and a key to these genera. A phylogenetic tree based on four gene combined analysis add support for 64 of the families and 22 orders, including the novel orders, Dyfrolomycetales, Lichenoconiales, Lichenotheliales, Monoblastiales, Natipusillales, Phaeotrichales and Strigulales. The paper is expected to provide a working document on Dothideomycetes which can be modified as new data comes to light. It is hoped that by illustrating types we provide stimulation and interest so that more work is carried out in this remarkable group of fungi.

A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex

We constructed a two-locus database, comprising partial translation elongation factor (EF-1alpha) gene sequences and nearly full-length sequences of the nuclear ribosomal intergenic spacer region (IGS rDNA) for 850 isolates spanning the phylogenetic breadth of the Fusarium oxysporum species complex (FOSC). Of the 850 isolates typed, 101 EF-1alpha, 203 IGS rDNA, and 256 two-locus sequence types (STs) were differentiated. Analysis of the combined dataset suggests that two-thirds of the STs might be associated with a single host plant. This analysis also revealed that the 26 STs associated with human mycoses were genetically diverse, including several which appear to be nosocomial in origin. A congruence analysis, comparing partial EF-1alpha and IGS rDNA bootstrap consensus, identified a significant number of conflicting relationships dispersed throughout the bipartitions, suggesting that some of the IGS rDNA sequences may be non-orthologous. We also evaluated enniatin, fumonisin and moniliformin mycotoxin production in vitro within a phylogenetic framework.

Phylogenetic lineages in the Capnodiales.

The Capnodiales incorporates plant and human pathogens, endophytes, saprobes and epiphytes, with a wide range of nutritional modes. Several species are lichenised, or occur as parasites on fungi, or animals. The aim of the present study was to use DNA sequence data of the nuclear ribosomal small and large subunit RNA genes to test the monophyly of the Capnodiales, and resolve families within the order. We designed primers to allow the amplification and sequencing of almost the complete nuclear ribosomal small and large subunit RNA genes. Other than the Capnodiaceae (sooty moulds), and the Davidiellaceae, which contains saprobes and plant pathogens, the order presently incorporates families of major plant pathological importance such as the Mycosphaerellaceae, Teratosphaeriaceae and Schizothyriaceae. The Piedraiaceae was not supported, but resolves in the Teratosphaeriaceae. The Dissoconiaceae is introduced as a new family to accommodate Dissoconium and Ramichloridium. Lichenisation, as well as the ability to be saprobic or plant pathogenic evolved more than once in several families, though the taxa in the upper clades of the tree lead us to conclude that the strictly plant pathogenic, nectrotrophic families evolved from saprobic ancestors (Capnodiaceae), which is the more primitive state.

A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages

Rock surfaces are unique terrestrial habitats in which rapid changes in the intensity of radiation, temperature, water supply and nutrient availability challenge the survival of microbes. A specialised, but diverse group of free-living, melanised fungi are amongst the persistent settlers of bare rocks. Multigene phylogenetic analyses were used to study relationships of ascomycetes from a variety of substrates, with a dataset including a broad sampling of rock dwellers from different geographical locations. Rock-inhabiting fungi appear particularly diverse in the early diverging lineages of the orders Chaetothyriales and Verrucariales. Although these orders share a most recent common ancestor, their lifestyles are strikingly different. Verrucariales are mostly lichen-forming fungi, while Chaetothyriales, by contrast, are best known as opportunistic pathogens of vertebrates (e.g. Cladophialophora bantiana and Exophiala dermatitidis, both agents of fatal brain infections) and saprophytes. The rock-dwelling habit is shown here to be key to the evolution of these two ecologically disparate orders. The most recent common ancestor of Verrucariales and Chaetothyriales is reconstructed as a non-lichenised rock-inhabitant. Ancestral state reconstructions suggest Verrucariales as one of the independent ascomycetes group where lichenisation has evolved on a hostile rock surface that might have favored this shift to a symbiotic lifestyle. Rock-inhabiting fungi are also ancestral to opportunistic pathogens, as they are found in the early diverging lineages of Chaetothyriales. In Chaetothyriales and Verrucariales, specific morphological and physiological traits (here referred to as extremotolerance) evolved in response to stresses in extreme conditions prevailing on rock surfaces. These factors facilitated colonisation of various substrates including the brains of vertebrates by opportunistic fungal pathogens, as well as helped establishment of a stable lichen symbiosis.

Biodiversity of the genus Cladophialophora

Cladophialophora is a genus of black yeast-like fungi comprising a number of clinically highly significant species in addition to environmental taxa. The genus has previously been characterized by branched chains of ellipsoidal to fusiform conidia. However, this character was shown to have evolved several times independently in the order Chaetothyriales. On the basis of a multigene phylogeny (nucLSU, nucSSU, RPB1), most of the species of Cladophialophora (including its generic type C. carrionii) belong to a monophyletic group comprising two main clades (carrionii- and bantiana-clades). The genus includes species causing chromoblastomycosis and other skin infections, as well as disseminated and cerebral infections, often in immunocompetent individuals. In the present study, multilocus phylogenetic analyses were combined to a morphological study to characterize phenetically similar Cladophialophora strains. Sequences of the ITS region, partial Translation Elongation Factor 1-α and β-Tubulin genes were analysed for a set of 48 strains. Four novel species were discovered, originating from soft drinks, alkylbenzene-polluted soil, and infected patients. Membership of the both carrionii and bantiana clades might be indicative of potential virulence to humans.

Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium.

Over 200 new sequences are generated for members of the genus Acremonium and related taxa including ribosomal small subunit sequences (SSU) for phylogenetic analysis and large subunit (LSU) sequences for phylogeny and DNA-based identification. Phylogenetic analysis reveals that within the Hypocreales, there are two major clusters containing multiple Acremonium species. One clade contains Acremonium sclerotigenum, the genus Emericellopsis, and the genus Geosmithia as prominent elements. The second clade contains the genera Gliomastix sensu stricto and Bionectria. In addition, there are numerous smaller clades plus two multi-species clades, one containing Acremonium strictum and the type species of the genus Sarocladium, and, as seen in the combined SSU/LSU analysis, one associated subclade containing Acremonium breve and related species plus Acremonium curvulum and related species. This sequence information allows the revision of three genera. Gliomastix is revived for five species, G. murorum, G. polychroma, G. tumulicola, G. roseogrisea, and G. masseei. Sarocladium is extended to include all members of the phylogenetically distinct A. strictum clade including the medically important A. kiliense and the protective maize endophyte A. zeae. Also included in Sarocladium are members of the phylogenetically delimited Acremonium bacillisporum clade, closely linked to the A. strictum clade. The genus Trichothecium is revised following the principles of unitary nomenclature based on the oldest valid anamorph or teleomorph name, and new combinations are made in Trichothecium for the tightly interrelated Acremonium crotocinigenum, Spicellum roseum, and teleomorph Leucosphaerina indica. Outside the Hypocreales, numerous Acremonium-like species fall into the Plectosphaerellaceae, and A. atrogriseum falls into the Cephalothecaceae.

Phylogeny of rock-inhabiting fungi related to Dothideomycetes

The class Dothideomycetes (along with Eurotiomycetes) includes numerous rock-inhabiting fungi (RIF), a group of ascomycetes that tolerates surprisingly well harsh conditions prevailing on rock surfaces. Despite their convergent morphology and physiology, RIF are phylogenetically highly diverse in Dothideomycetes. However, the positions of main groups of RIF in this class remain unclear due to the lack of a strong phylogenetic framework. Moreover, connections between rock-dwelling habit and other lifestyles found in Dothideomycetes such as plant pathogens, saprobes and lichen-forming fungi are still unexplored. Based on multigene phylogenetic analyses, we report that RIF belong to Capnodiales (particularly to the family Teratosphaeriaceae s.l.), Dothideales, Pleosporales, and Myriangiales, as well as some uncharacterised groups with affinities to Dothideomycetes. Moreover, one lineage consisting exclusively of RIF proved to be closely related to Arthoniomycetes, the sister class of Dothideomycetes. The broad phylogenetic amplitude of RIF in Dothideomycetes suggests that total species richness in this class remains underestimated. Composition of some RIF-rich lineages suggests that rock surfaces are reservoirs for plant-associated fungi or saprobes, although other data also agree with rocks as a primary substrate for ancient fungal lineages. According to the current sampling, long distance dispersal seems to be common for RIF. Dothideomycetes lineages comprising lichens also include RIF, suggesting a possible link between rock-dwelling habit and lichenisation.

Naming and outline of Dothideomycetes-2014 including proposals for the protection or suppression of generic names

Article 59.1, of the International Code of Nomenclature for Algae, Fungi, and Plants (ICN; Melbourne Code), which addresses the nomenclature of pleomorphic fungi, became effective from 30 July 2011. Since that date, each fungal species can have one nomenclaturally correct name in a particular classification. All other previously used names for this species will be considered as synonyms. The older generic epithet takes priority over the younger name. Any widely used younger names proposed for use, must comply with Art. 57.2 and their usage should be approved by the Nomenclature Committee for Fungi (NCF). In this paper, we list all genera currently accepted by us in Dothideomycetes (belonging to 23 orders and 110 families), including pleomorphic and non-pleomorphic genera. In the case of pleomorphic genera, we follow the rulings of the current ICN and propose single generic names for future usage. The taxonomic placements of 1261 genera are listed as an outline. Protected names and suppressed names for 34 pleomorphic genera are listed separately. Notes and justifications are provided for possible proposed names after the list of genera. Notes are also provided on recent advances in our understanding of asexual and sexual morph linkages in Dothideomycetes. A phylogenetic tree based on four gene analyses supported 23 orders and 75 families, while 35 families still lack molecular data.