Divergent genomic trajectories predate the origin of animals and fungi

22 pages, 4 figures, supplementary information https://doi.org/10.1038/s41586-022-05110-4.-- Data availability: The raw sequence data and assembled genomes generated in this study have been deposited in the European Nucleotide Archive (ENA) at EMBL-EBI under accession number PRJEB52884 (https://www.ebi.ac.uk/ena/browser/view/PRJEB52884). The genome assemblies are also available in figshare (https://doi.org/10.6084/m9.figshare.19895962.v1). Protein sequences of the species used in this study were downloaded from the GenBank public databases (https://www.ncbi.nlm.nih.gov/protein/), Uniprot (https://www.uniprot.org/), JGI genome database (https://genome.jgi.doe.gov/portal/) and Ensembl genomes (https://www.ensembl.org). The following specific databases were also used in this study: Pfam A v29 (https://pfam.xfam.org/), EggNOG emapperdb-4.5.1 (http://eggnog5.embl.de) and UniProt reference proteomes release 2016_02 (https://www.uniprot.org/). The supporting data files of this study are available in the following repository: https://doi.org/10.6084/m9.figshare.13140191.v1.-- Code availability: The most relevant custom code developed for this study (the MAPBOS pipeline and the machine learning classifiers) is available at https://doi.org/10.5281/zenodo.6586559Animals and fungi have radically distinct morphologies, yet both evolved within the same eukaryotic supergroup: Opisthokonta1,2. Here we reconstructed the trajectory of genetic changes that accompanied the origin of Metazoa and Fungi since the divergence of Opisthokonta with a dataset that includes four novel genomes from crucial positions in the Opisthokonta phylogeny. We show that animals arose only after the accumulation of genes functionally important for their multicellularity, a tendency that began in the pre-metazoan ancestors and later accelerated in the metazoan root. By contrast, the pre-fungal ancestors experienced net losses of most functional categories, including those gained in the path to Metazoa. On a broad-scale functional level, fungal genomes contain a higher proportion of metabolic genes and diverged less from the last common ancestor of Opisthokonta than did the gene repertoires of Metazoa. Metazoa and Fungi also show differences regarding gene gain mechanisms. Gene fusions are more prevalent in Metazoa, whereas a larger fraction of gene gains were detected as horizontal gene transfers in Fungi and protists, in agreement with the long-standing idea that transfers would be less relevant in Metazoa due to germline isolation3,4,5. Together, our results indicate that animals and fungi evolved under two contrasting trajectories of genetic change that predated the origin of both groups. The gradual establishment of two clearly differentiated genomic contexts thus set the stage for the emergence of Metazoa and FungiE.O.-P. was supported by a predoctoral FPI grant from MINECO (BES-2015-072241) and by ESF Investing in your future. E.O.-P., D.L-E., A.S.A. and I.R.-T. received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP7-2007-2013) (Grant agreement No. 616960) and also from grants (BFU2014-57779-P and PID2020-120609GB-I00) by MCIN/AEI/10.13039/501100011033 and ‘ERDF A way of making Europe’. E.O.-P. and G.J.Sz. received funding from the European Research Council under the European Union’s Horizon 2020 research and innovation programme (Grant agreement No. 714774). T.A.W. was supported by a Royal Society University Research Fellowship (URF\R\201024) and NERC standard grant NE/P00251X/1. This work was supported by the Gordon and Betty Moore Foundation through grant GBMF9741 to T.A.W. and G.J.Sz. J.S.P. and E.B. received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP7-2007-2013) (Grant agreement No. 615274). D.V.T. and cell culturing were supported by the Russian Science Foundation grant no. 18-14-00239, https://rscf.ru/project/18-14-00239/. Culture of P. vietnamica was obtained as the result of field work in Vietnam as part of the project ‘Ecolan 3.2’ of the Russian–Vietnam Tropical Center. P.J.K. is supported by an Investigator Award from the Gordon and Betty Moore Foundation (https://doi.org/10.37807/GBMF9201)With the institutional support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S)Peer reviewe

Megaphylogeny resolves global patterns of mushroom evolution

peerReviewe

Evolution through segmental duplications and losses : A Super-Reconciliation approach

The classical gene and species tree reconciliation, used to infer the history of gene gain and loss explaining the evolution of gene families, assumes an independent evolution for each family. While this assumption is reasonable for genes that are far apart in the genome, it is not appropriate for genes grouped into syntenic blocks, which are more plausibly the result of a concerted evolution. Here, we introduce the Super-Reconciliation problem which consists in inferring a history of segmental duplication and loss events (involving a set of neighboring genes) leading to a set of present-day syntenies from a single ancestral one. In other words, we extend the traditional Duplication-Loss reconciliation problem of a single gene tree, to a set of trees, accounting for segmental duplications and losses. Existency of a Super-Reconciliation depends on individual gene tree consistency. In addition, ignoring rearrangements implies that existency also depends on gene order consistency. We first show that the problem of reconstructing a most parsimonious Super-Reconciliation, if any, is NP-hard and give an exact exponential-time algorithm to solve it. Alternatively, we show that accounting for rearrangements in the evolutionary model, but still only minimizing segmental duplication and loss events, leads to an exact polynomial-time algorithm. We finally assess time efficiency of the former exponential time algorithm for the Duplication-Loss model on simulated datasets, and give a proof of concept on the opioid receptor genes

Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits

Mycorrhizal fungi are mutualists that play crucial roles in nutrient acquisition in terrestrial ecosystems. Mycorrhizal symbioses arose repeatedly across multiple lineages of Mucoromycotina, Ascomycota, and Basidiomycota. Considerable variation exists in the capacity of mycorrhizal fungi to acquire carbon from soil organic matter. Here, we present a combined analysis of 135 fungal genomes from 73 saprotrophic, endophytic and pathogenic species, and 62 mycorrhizal species, including 29 new mycorrhizal genomes. This study samples ecologically dominant fungal guilds for which there were previously no symbiotic genomes available, including ectomycorrhizal Russulales, Thelephorales and Cantharellales. Our analyses show that transitions from saprotrophy to symbiosis involve (1) widespread losses of degrading enzymes acting on lignin and cellulose, (2) co-option of genes present in saprotrophic ancestors to fulfill new symbiotic functions, (3) diversification of novel, lineage-specific symbiosis-induced genes, (4) proliferation of transposable elements and (5) divergent genetic innovations underlying the convergent origins of the ectomycorrhizal guild. Mycorrhizal symbioses have evolved repeatedly in diverse fungal lineages. A large phylogenomic analysis sheds light on genomic changes associated with transitions from saprotrophy to symbiosis, including divergent genetic innovations underlying the convergent origins of the ectomycorrhizal guild.Peer reviewe

Analysis of Three-Dimensional Cell Migration in Dopamine-Modified Poly(aspartic acid)-Based Hydrogels

Several types of promising cell-based therapies for tissue regeneration have been developing worldwide. However, for successful therapeutical application of cells in this field, appropriate scaffolds are also required. Recently, the research for suitable scaffolds has been focusing on polymer hydrogels due to their similarity to the extracellular matrix. The main limitation regarding amino acid-based hydrogels is their difficult and expensive preparation, which can be avoided by using poly(aspartamide) (PASP)-based hydrogels. PASP-based materials can be chemically modified with various bioactive molecules for the final application purpose. In this study, dopamine containing PASP-based scaffolds is investigated, since dopamine influences several cell biological processes, such as adhesion, migration, proliferation, and differentiation, according to the literature. Periodontal ligament cells (PDLCs) of neuroectodermal origin and SH-SY5Y neuroblastoma cell line were used for the in vitro experiments. The chemical structure of the polymers and hydrogels was proved by 1H-NMR and FTIR spectroscopy. Scanning electron microscopical (SEM) images confirmed the suitable pore size range of the hydrogels for cell migration. Cell viability assay was carried out according to a standardized protocol using the WST-1 reagent. To visualize three-dimensional cell distribution in the hydrogel matrix, two-photon microscopy was used. According to our results, dopamine containing PASP gels can facilitate vertical cell penetration from the top of the hydrogel in the depth of around 4 cell layers (~150 μm). To quantify these observations, a detailed image analysis process was developed and firstly introduced in this paper

RecPhyloXML: a format for reconciled gene trees

Motivation: A reconciliation is an annotation of the nodes of a gene tree with evolutionary events-for example, speciation, gene duplication, transfer, loss, etc.-along with a mapping onto a species tree. Many algorithms and software produce or use reconciliations but often using different reconciliation formats, regarding the type of events considered or whether the species tree is dated or not. This complicates the comparison and communication between different programs.Results: Here, we gather a consortium of software developers in gene tree species tree reconciliation to propose and endorse a format that aims to promote an integrative-albeit flexible-specification of phylogenetic reconciliations. This format, named recPhyloXML, is accompanied by several tools such as a reconciled tree visualizer and conversion utilities.Agence Nationale pour la Recherche | Ref. ANR-10-BINF-01-01Institut de Biologie Computationnelle | Ref. ANR-11-BINF-0002Swiss National Science Foundation | Ref. 15065

Data from: MHC-mediated sexual selection on bird song: generic polymorphism, particular alleles and acoustic signals

Several hypotheses predict that the major histocompatibility complex (MHC) drives mating preference in females. Olfactory, color or morphological traits are often found as reliable signals of the MHC profile, but the role of avian song mediating MHC-based female choice remains largely unexplored. We investigated the relationship between several MHC and acoustic features in the collared flycatcher (Ficedula albicollis) a European passerine with complex songs. We screened a fragment of the class IIB 2nd exon of the MHC molecule, of which individuals harbor 4-15 alleles, while considerable sequence diversity is maintained at the population level. To make statistical inferences from a large number of comparisons, we adopted both null-hypothesis testing and effect size framework in combination with randomization procedures. After controlling for potential confounding factors, neither MHC allelic diversity nor the presence of particular alleles was associated remarkably to the investigated qualitative and quantitative song traits. Furthermore, genetic similarity among males based on MHC sequences was not reflected by the similarity in their song based on syllable content. Overall, these results suggest that the relationship between features of song and the allelic composition and diversity of MHC is not strong in the studied species. However, a biologically-motivated analysis revealed that individuals that harbor an MHC allele that impairs survival perform songs with broader frequency range. This finding suggests that certain aspects of the song may bear reliable information concerning the MHC profile of the individuals, which can be used by females to optimize mate choice

song_distance

Dissimilarity in song content among males based on the frequency of use of particular syllable