Fungal genomes tell a story of ecological adaptations

One genome enables a fungus to have various lifestyles and strategies depending on environmental conditions and in the presence of specific counterparts. The nature of their interactions with other living and abiotic elements is a consequence of their osmotrophism. The ability to degrade complex compounds and especially plant biomass makes them a key component of the global carbon circulation cycle. Since the first fungal genomic sequence was published in 1996 mycology has benefited from the technolgical progress. The available data create an unprecedented opportunity to perform massive comparative studies with complex study design variants targeted at all cellular processes.Grzyby odgrywają zasadniczą rolę w ekosystemach jako patogeny, saprotrofy i symbionty. Ich wszechstronne zdolności metaboliczne czynią z nich kluczowe ogniwo w obiegu węgla w przyrodzie. Dla człowieka stanowią głównie źródło infekcji, ale również zyskują na znaczeniu w biotechnologii (Fisher et al. 2012). Grzyby są obecne w naszym otoczeniu w formie zarodników, pełzaków, grzybni i owocników. Te same gatunki grzybów w zależności od warunków otoczenia mogą prezentować rożne formy morfologiczne i tworzyć różne relacje z otoczeniem, na przykład owadobójcze grzyby są często spotykane jako endosymbionty roślin (Spatafora et al. 2007). Całe to bogactwo znajduje odzwierciedlenie w genomach grzybów. Osmotroficzny tryb życia grzybów narzuca charakter interakcji grzybów z otoczeniem, która odbywa się przy pomocy wydzielanych na zewnątrz enzymów rozkładających pożywienie, białek efektorowych oraz toksyn wpływających na inne organizmy. Grzyby posiadają złożone kompozycje wydzielanych cząsteczek oraz transportery błonowe przystosowane do efektywnego przenoszenia związków chemicznych w obu kierunkach (Richards & Talbot 2013). Zdolność do rozkładania ligniny i celulozy odpowiada w dużej mierze za sukces ewolucyjny grzybów. Adaptacja organizmu do nowego ekosystemu zwykle przebiega poprzez duplikację genów z ich późniejszymi asymetrycznymi zmianami prowadzącymi do szybkiej zmiany specyficzności substratowej jednego z paralogów. Wielokrotne duplikacje jednej grupy genów prowadzą do rozrostu rodziny kodowanych przez nie białek i rozszerzenia zakresu możliwości np. rozkładanych przez nie wariantów substratów. Zwiększenie liczby genów związanych z metabolizowaniem danej grupy substratów jest jednym z podstawowych sposobów adaptacji do danej niszy ekologicznej widzianej z perspektywy genomu. Charakterystyczne więc dla grzybów związanych z roślinami będzie kodowanie licznych enzymów degradujących węglowodany, a dla dermatofitów - proteazy i lipazy. Kolejnym poziomem adaptacji patogenów/symbiontów jest zmiana profilu ekspresji genów i stały „wyścig zbrojeń” z gospodarzami. Ponadto geny te często sąsiadują z transpozonami, w obrębie szybciej ewoluującej części genomu. Geny związane z metabolizowaniem ksenobiotyków częściej ulegają też horyzontalnemu transferowi genów aniżeli geny metabolizmu podstawowego. Inna wyróżniającą grzyby cechą jest posiadanie różnorodnych modeli rozmnażania płciowego nawet pomiędzy spokrewnionymi gatunkami. Model rozmnażania jest jednym z ważniejszych sposobów dostosowania do trybu życia. Rozmnażanie jednopłciowe pojawiało się wielokrotnie w ewolucji grzybów i wydaje się być adaptacją do patogennego trybu życia

Detecting Locus Acquisition Events in Gene Trees

Horizontal Gene Transfer (HGT), a process of acquisition and fixation of foreign genetic material, is an important biological phenomenon. Several approaches to HGT inference have been proposed. However, most of them either rely on approximate, non-phylogenetic methods or on the tree reconciliation, which is computationally intensive and sensitive to parameter values. In this work, we investigate the Locus Tree Inference problem as a possible alternative that combines the advantages of both approaches. We show several algorithms to solve the problem in the parsimony framework. We introduce a novel tree mapping, which allows us to obtain a heuristic solution to the problems of locus tree inference and duplication classification. Our approach allows not only for faster comparisons of gene and species trees but also to improve known algorithms for duplication inference in the presence of polytomies in the species trees

In Silico Predictions of Ecological Plasticity Mediated by Protein Family Expansions in Early-Diverging Fungi

Early-diverging fungi (EDF) are ubiquitous and versatile. Their diversity is reflected in their genome sizes and complexity. For instance, multiple protein families have been reported to expand or disappear either in particular genomes or even whole lineages. The most commonly mentioned are CAZymes (carbohydrate-active enzymes), peptidases and transporters that serve multiple biological roles connected to, e.g., metabolism and nutrients intake. In order to study the link between ecology and its genomic underpinnings in a more comprehensive manner, we carried out a systematic in silico survey of protein family expansions and losses among EDF with diverse lifestyles. We found that 86 protein families are represented differently according to EDF ecological features (assessed by median count differences). Among these there are 19 families of proteases, 43 CAZymes and 24 transporters. Some of these protein families have been recognized before as serine and metallopeptidases, cellulases and other nutrition-related enzymes. Other clearly pronounced differences refer to cell wall remodelling and glycosylation. We hypothesize that these protein families altogether define the preliminary fungal adaptasome. However, our findings need experimental validation. Many of the protein families have never been characterized in fungi and are discussed in the light of fungal ecology for the first tim

A widespread peroxiredoxin-like domain present in tumor suppression- and progression-implicated proteins

Background Peroxide turnover and signalling are involved in many biological phenomena relevant to human diseases. Yet, all the players and mechanisms involved in peroxide perception are not known. Elucidating very remote evolutionary relationships between proteins is an approach that allows the discovery of novel protein functions. Here, we start with three human proteins, SRPX, SRPX2 and CCDC80, involved in tumor suppression and progression, which possess a conserved region of similarity. Structure and function prediction allowed the definition of P-DUDES, a phylogenetically widespread, possibly ancient protein structural domain, common to vertebrates and many bacterial species. Results We show, using bioinformatics approaches, that the P-DUDES domain, surprisingly, adopts the thioredoxin-like (Thx-like) fold. A tentative, more detailed prediction of function is made, namely, that of a 2-Cys peroxiredoxin. Incidentally, consistent overexpression of all three human P-DUDES genes in two public glioblastoma microarray gene expression datasets was discovered. This finding is discussed in the context of the tumor suppressor role that has been ascribed to P-DUDES proteins in several studies. Majority of non-redundant P-DUDES proteins are found in marine metagenome, and among the bacterial species possessing this domain a trend for a higher proportion of aquatic species is observed. Conclusions The new protein structural domain, now with a broad enzymatic function predicted, may become a drug target once its detailed molecular mechanism of action is understood in detail

Cut-and-paste transposons in fungi with diverse lifestyles

Transposons (TEs) shape genomes via recombination and transposition, lead to chromosomal rearrangements, create new gene neighbourhoods and alter gene expression. They play key roles in adaptation either to symbiosis in Amanita genus or to pathogenicity in Pyrenophora tritici-repentis. Despite growing evidence of their importance, the abundance and distribution of mobile elements replicating in a “cut and paste” fashion is barely described so far. In order to improve our knowledge on this old and ubiquitous class of transposable elements, 1,730 fungal genomes were scanned using both de novo and homology-based approaches. DNA TEs have been identified across the whole dataset and display uneven distribution from both DNA TE classification and fungal taxonomy perspectives. DNA TE content correlates with genome size, which confirms that many transposon families proliferate simultaneously. In contrast, it is independent from intron density, average gene distance and GC content. TE count is associated with species’ lifestyle and tends to be elevated in plant symbionts and decreased in animal parasites. Lastly, we found that fungi with both RIP and RNAi systems have more total DNA TE sequences but less elements retaining a functional transposase, what reflects stringent control over transposition

Terpenoid Biosynthesis Dominates among Secondary Metabolite Clusters in Mucoromycotina Genomes

Early-diverging fungi harbour unprecedented diversity in terms of living forms, biological traits and genome architecture. Before the sequencing era, non-Dikarya fungi were considered unable to produce secondary metabolites (SM); however, this perspective is changing. The main classes of secondary metabolites in fungi include polyketides, nonribosomal peptides, terpenoids and siderophores that serve different biological roles, including iron chelation and plant growth promotion. The same classes of SM are reported for representatives of early-diverging fungal lineages. Encouraged by the advancement in the field, we carried out a systematic survey of SM in Mucoromycotina and corroborated the presence of various SM clusters (SMCs) within the phylum. Among the core findings, considerable representation of terpene and nonribosomal peptide synthetase (NRPS)-like candidate SMCs was found. Terpene clusters with diverse domain composition and potentially highly variable products dominated the landscape of candidate SMCs. A uniform low-copy distribution of siderophore clusters was observed among most assemblies. Mortierellomycotina are highlighted as the most potent SMC producers among the Mucoromycota and as a source of novel peptide products. SMC identification is dependent on gene model quality and can be successfully performed on a batch scale with genomes of different quality and completeness

Utilization of cobalamin is ubiquitous in early-branching fungal phyla

Cobalamin is a cofactor present in essential metabolic pathways in animals and one of the water-soluble vitamins. It is a complex compound synthesized solely by prokaryotes. Cobalamin dependence is scattered across the tree of life. In particular, fungi and plants were deemed devoid of cobalamin. We demonstrate that cobalamin is utilized by all non-Dikarya fungi lineages. This observation is supported by the genomic presence of both B12-dependent enzymes and cobalamin modifying enzymes. Fungal cobalamin-dependent enzymes are highly similar to their animal homologs. Phylogenetic analyses support a scenario of vertical inheritance of the cobalamin usage with several losses. Cobalamin usage was probably lost in Mucorinae and at the base of Dikarya which groups most of the model organisms and which hindered B12-dependent metabolism discovery in fungi. Our results indicate that cobalamin dependence was a widely distributed trait at least in Opisthokonta, across diverse microbial eukaryotes and was likely present in the LECA

Phylogeny-Based Systematization of Arabidopsis Proteins with Histone H1 Globular Domain.

H1 (or linker) histones are basic nuclear proteins that possess an evolutionarily conserved nucleosome-binding globular domain, GH1. They perform critical functions in determining the accessibility of chromatin DNA to trans-acting factors. In most metazoan species studied so far, linker histones are highly heterogenous, with numerous nonallelic variants cooccurring in the same cells. The phylogenetic relationships among these variants as well as their structural and functional properties have been relatively well established. This contrasts markedly with the rather limited knowledge concerning the phylogeny and structural and functional roles of an unusually diverse group of GH1-containing proteins in plants. The dearth of information and the lack of a coherent phylogeny-based nomenclature of these proteins can lead to misunderstandings regarding their identity and possible relationships, thereby hampering plant chromatin research. Based on published data and our in silico and high-throughput analyses, we propose a systematization and coherent nomenclature of GH1-containing proteins of Arabidopsis (Arabidopsis thaliana [L.] Heynh) that will be useful for both the identification and structural and functional characterization of homologous proteins from other plant species

Carbon assimilation profiles of mucoralean fungi show their metabolic versatility

Most mucoralean fungi are common soil saprotrophs and were probably among the first land colonisers. Although Mucoromycotina representatives grow well on simple sugar media and are thought to be unable to assimilate more complex organic compounds, they are often isolated from plant substrates. The main goal of the study was to explore the effects of isolation origin and phylogenetic placement on the carbon assimilation capacities of a large group of saprotrophic Mucoromycotina representatives (i.e. Umbelopsidales and Mucorales). Fifty two strains representing different Mucoromycotina families and isolated from different substrates were tested for their capacity to grow on 99 different carbon sources using the Biolog phenotypic microarray system and agar plates containing selected biopolymers (i.e. cellulose, xylan, pectin, and starch) as a sole carbon source. Although our results did not reveal a correlation between phylogenetic distance and carbon assimilation capacities, we observed 20 significant differences in growth capacity on specific carbon sources between representatives of different families. Our results also suggest that isolation origin cannot be considered as a main predictor of the carbon assimilation capacities of a particular strain. We conclude that saprotrophic Mucoromycotina representatives are, contrary to common belief, metabolically versatile and able to use a wide variety of carbon sources

What can be lost? Genomic perspective on the lipid metabolism of Mucoromycota

Mucoromycota is a phylum of early diverging fungal (EDF) lineages, of mostly plant-associated terrestrial fungi. Some strains have been selected as promising biotechnological organisms due to their ability to produce polyunsaturated fatty acids and efficient conversion of nutrients into lipids. Others get their lipids from the host plant and are unable to produce even the essential ones on their own. Following the advancement in EDF genome sequencing, we carried out a systematic survey of lipid metabolism protein families across different EDF lineages. This enabled us to explore the genomic basis of the previously documented ability to produce several types of lipids within the fungal tree of life. The core lipid metabolism genes showed no significant diversity in distribution, however specialized lipid meta- bolic pathways differed in this regard among different fungal lineages. In total 165 out of 202 genes involved in lipid metabolism were present in all tested fungal lineages, while remaining 37 genes were found to be absent in some of fungal lineages. Duplications were observed for 69 genes. For the first time we demonstrate that ergosterol is not being produced by several independent groups of plant-associated fungi due to the losses of different ERG genes. Instead, they possess an ancestral pathway leading to the synthesis of cholesterol, which is absent in other fungal lineages. The lack of diacylglycerol kinase in both Mortierellomycotina and Blastocladiomycota opens the ques- tion on sterol equilibrium regulation in these organisms. Early diverging fungi retained most of beta oxidation com- ponents common with animals including Nudt7, Nudt12 and Nudt19 pointing at peroxisome divergence in Dikarya. Finally, Glomeromycotina and Mortierellomycotina representatives have a similar set of desaturases and elongases related to the synthesis of complex, polyunsaturated fatty acids pointing at an ancient expansion of fatty acid metab- olism currently being explored by biotechnological studies