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Understanding biological diversity is crucial for ecological and evolutionary studies. Even though a great part of animal diversity has already been documented, both morphological surveys and metabarcoding analyses have previously shown that some animal groups, such as Platyhelminthes, may harbour hidden diversity. To better understand the molecular diversity of Platyhelminthes, one of the most diverse and biomedically important animal phyla, we here combined data from six marine and two freshwater metabarcoding expeditions that cover a broad variety of aquatic habitats and analysed the data by phylogenetic placement. Our results show that a great part of the hidden diversity is located in early-branching clades such as Catenulida and Macrostomorpha, as well as in late-diverging clades such as Proseriata and Rhabdocoela. We also report the first freshwater record of Gnosonesimida, a group previously thought to be exclusively marine. Finally, we identified two putative novel freshwater Platyhelminthes clades that branch between well-defined orders of the phylum. Thus, our analyses of several environmental datasets confirm that a large part of the diversity of Platyhelminthes remains undiscovered, point to groups with more potential novel species and identify freshwater environments as potential reservoirs for novel species of flatworms. ; This work was supported by grants (BFU2014-57779-P and BFU2017-90114-P) from Ministerio de Economía y Competitividad (MINECO), Agencia Estatal de Investigación (AEI) and Fondo Europeo de Desarrollo Regional (FEDER) to I.R.-T. It has also received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. H2020-MSCA-ITN-2015-675752 (SINGEK Project, http://www.singek.eu/).

The work is part of the EU ERA-Net program BiodivERsA, under the project BioMarKs (Biodiversity of Marine euKaryotes).-- 14 pages, 8 figures, supplementary material https://doi.org/10.1038/s41598-018-27509-8 ; Although animals are among the best studied organisms, we still lack a full description of their diversity, especially for microscopic taxa. This is partly due to the time-consuming and costly nature of surveying animal diversity through morphological and molecular studies of individual taxa. A powerful alternative is the use of high-throughput environmental sequencing, providing molecular data from all organisms sampled. We here address the unknown diversity of animal phyla in marine environments using an extensive dataset designed to assess eukaryotic ribosomal diversity among European coastal locations. A multi-phylum assessment of marine animal diversity that includes water column and sediments, oxic and anoxic environments, and both DNA and RNA templates, revealed a high percentage of novel 18S rRNA sequences in most phyla, suggesting that marine environments have not yet been fully sampled at a molecular level. This novelty is especially high among Platyhelminthes, Acoelomorpha, and Nematoda, which are well studied from a morphological perspective and abundant in benthic environments. We also identified, based on molecular data, a potentially novel group of widespread tunicates. Moreover, we recovered a high number of reads for Ctenophora and Cnidaria in the smaller fractions suggesting their gametes might play a greater ecological role than previously suspected ; This work was supported by an Institució Catalana de Recerca i Estudis Avançats contract, two grants (BFU-2011-23434 and BFU2014-57779-P) from the Ministerio de Economia y Competitividad (MINECO), one of which (BFU2014-57779-P) was co-funded by the European Regional Development Fund (FEDER), and a European Research Council Consolidator Grant (ERC-2012-Co -616960) to I.R.-T. We also acknowledge financial support from the Secretaria d'Universitats i Recerca del Departament d'Economia i Coneixement de la Generalitat de Catalunya (Project 2014 SGR 619). J.d.C. was supported by a Marie Curie International Outgoing Fellowship grant (FP7-PEOPLE-2012-IOF - 331450 CAARL). J.P. acknowledges support from the European Research Council under the European Union's Seventh Framework Program (FP7/2007–2013)/ERC grant [268513] ; Peer Reviewed

Although animals are among the best studied organisms, we still lack a full description of their diversity, especially for microscopic taxa. This is partly due to the time-consuming and costly nature of surveying animal diversity through morphological and molecular studies of individual taxa. A powerful alternative is the use of high-throughput environmental sequencing, providing molecular data from all organisms sampled. We here address the unknown diversity of animal phyla in marine environments using an extensive dataset designed to assess eukaryotic ribosomal diversity among European coastal locations. A multi-phylum assessment of marine animal diversity that includes water column and sediments, oxic and anoxic environments, and both DNA and RNA templates, revealed a high percentage of novel 18S rRNA sequences in most phyla, suggesting that marine environments have not yet been fully sampled at a molecular level. This novelty is especially high among Platyhelminthes, Acoelomorpha, and Nematoda, which are well studied from a morphological perspective and abundant in benthic environments. We also identified, based on molecular data, a potentially novel group of widespread tunicates. Moreover, we recovered a high number of reads for Ctenophora and Cnidaria in the smaller fractions suggesting their gametes might play a greater ecological role than previously suspected. ; This work was supported by an Institució Catalana de Recerca i Estudis Avançats contract, two grants (BFU-2011-23434 and BFU2014-57779-P) from the Ministerio de Economia y Competitividad (MINECO), one of which (BFU2014-57779-P) was co-funded by the European Regional Development Fund (FEDER), and a European Research Council Consolidator Grant (ERC-2012-Co -616960) to I.R.-T. We also acknowledge financial support from the Secretaria d'Universitats i Recerca del Departament d'Economia i Coneixement de la Generalitat de Catalunya (Project 2014 SGR 619). J.d.C. was supported by a Marie Curie International Outgoing Fellowship grant (FP7-PEOPLE-2012-IOF - 331450 CAARL). J.P. acknowledges support from the European Research Council under the European Union's Seventh Framework Program (FP7/2007–2013)/ERC grant [268513]. The work is part of the EU ERA-Net program BiodivERsA, under the project BioMarKs (Biodiversity of Marine euKaryotes)

Parra-Acero et al. investigate cell-substrate adhesion in the filasterean C. owczarzaki, a close unicellular relative of animals. They show that cell adhesion relies on actin-dependent filopodia and is mediated by the integrin adhesome. This suggests that the role of integrins in cell-matrix adhesion was established before the emergence of animals.In animals, cell-matrix adhesions are essential for cell migration, tissue organization, and differentiation, which have central roles in embryonic development [1–6]. Integrins are the major cell surface adhesion receptors mediating cell-matrix adhesion in animals. They are heterodimeric transmembrane proteins that bind extracellular matrix (ECM) molecules on one side and connect to the actin cytoskeleton on the other [7]. Given the importance of integrin-mediated cell-matrix adhesion in development of multicellular animals, it is of interest to discover when and how this machinery arose during evolution. Comparative genomic analyses have shown that core components of the integrin adhesome pre-date the emergence of animals [8–11]; however, whether it mediates cell adhesion in non-metazoan taxa remains unknown. Here, we investigate cell-substrate adhesion in Capsaspora owczarzaki, the closest unicellular relative of animals with the most complete integrin adhesome [11, 12]. Previous work described that the life cycle of C. owczarzaki (hereafter, Capsaspora) includes three distinct life stages: adherent; cystic; and aggregative [13]. Using an adhesion assay, we show that, during the adherent life stage, C. owczarzaki adheres to surfaces using actin-dependent filopodia. We show that integrin β2 and its associated protein vinculin localize as distinct patches in the filopodia. We also demonstrate that substrate adhesion and integrin localization are enhanced by mammalian fibronectin. Finally, using a specific antibody for integrin β2, we inhibited cell adhesion to a fibronectin-coated surface. Our results suggest that adhesion to the substrate in C. owczarzaki is mediated by integrins. We thus propose that integrin-mediated adhesion pre-dates the emergence of animals. ; This work was funded by European Research Council Consolidator Grant (ERC-2012-Co-616960) to I.R.-T.; O.D. was supported by a Swiss National Science Foundation Early PostDoc Mobility fellowship (P2LAP3_171815) and a Marie Sklodowska-Curie individual fellowship (MSCA-IF 746044). M.H. received funding from the People Programme (Marie Curie Actions) of the European Union's Seventh Framework Programme FP7/ 2007-2013/ under REA grant agreement no. 330925. N.H.B.'s work on this project was supported by a Royal Society International Exchange Grant (IE141189). The CRG/UPF Proteomics Unit is part of the of Proteored, PRB3 and is supported by grant PT17/0019 of the PE I+D+i 2013-2016, funded by ISCIII and ERDF.

Single-cell genomics (SCG) appeared as a powerful technique to get genomic information from uncultured organisms. However, SCG techniques suffer from biases at the whole genome amplification step that can lead to extremely variable numbers of genome recovery (5-100%). Thus, it is unclear how useful can SCG be to address evolutionary questions on uncultured microbial eukaryotes. To provide some insights into this, we here analysed 3 single-cell amplified genomes (SAGs) of the choanoflagellate Monosiga brevicollis, whose genome is known. Our results show that each SAG has a different, independent bias, yielding different levels of genome recovery for each cell (6-36%). Genes often appear fragmented and are split into more genes during annotation. Thus, analyses of gene gain and losses, gene architectures, synteny and other genomic features can not be addressed with a single SAG. However, the recovery of phylogenetically-informative protein domains can be up to 55%. This means SAG data can be used to perform accurate phylogenomic analyses. Finally, we also confirm that the co-assembly of several SAGs improves the general genomic recovery. Overall, our data show that, besides important current limitations, SAGs can still provide interesting and novel insights from poorly-known, uncultured organisms. ; We acknowledge support by ICREA, a European Research Council Consolidator (ERC-2012-Co-616960) grant, and grant (BFU2014-57779-P) from Ministerio de Economía y Competitividad (MINECO) with FEDER funds. We also acknowledge financial support from Secretaria d'Universitats i Recerca del Departament d'Economia i Coneixement de la Generalitat de Catalunya (Project 2014 SGR 619). The authors want to acknowledge Jean-Francois Mangot for the support on the tetranucleotide frequency calculations and Ramon Massana for helpful discussions on the manuscript. We also thank Javier del Campo for some initial ideas, further discussions, and help in the experimental design. Any opinion, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation. We also thank the commitment of the following people and sponsors: CNRS (in particular Groupement de Recherche GDR3280), European Molecular Biology Laboratory (EMBL), Genoscope/CEAthe French Government 'Investissements d'Avenir' programmes OCEANOMICS (ANR-11-BTBR-0008) and FRANCE GENOMIQUE (ANR-10-INBS-09-08), Agence Nationale de la Recherche, and European Union FP7 (MicroB3/No.287589), We also thank the support and commitment of Agnès B. and Etienne Bourgois, the Veolia Environment Foundation, Region Bretagne, Lorient Agglomeration, World Courier, Illumina, the Eléctricité de France (EDF) Foundation, Fondation pour la recherche sur la biodiversité (FRB), the Foundation Prince Albert II de Monaco, the Tara Foundation, its schooner and teams. We thank MERCATOR-CORIOLIS and ACRI-ST for providing daily satellite data during the expedition. We are also grateful to the French Ministry of Foreign Affairs for supporting the expedition and to the countries who graciously granted sampling permissions. Tara Oceans would not exist without continuous support from 23 institutes (http://oceans.taraexpeditions.org/en/m/science/labs-involved/).

The unicellular ancestor of animals had a complex repertoire of genes linked to multicellular processes. This suggests that changes in the regulatory genome, rather than in gene innovation, were key to the origin of animals. Here, we carry out multiple functional genomic assays in Capsaspora owczarzaki, the unicellular relative of animals with the largest known gene repertoire for transcriptional regulation. We show that changing chromatin states, differential lincRNA expression, and dynamic cis-regulatory sites are associated with life cycle transitions in Capsaspora. Moreover, we demonstrate conservation of animal developmental transcription-factor networks and extensive network interconnection in this premetazoan organism. In contrast, however, Capsaspora lacks animal promoter types, and its regulatory sites are small, proximal, and lack signatures of animal enhancers. Overall, our results indicate that the emergence of animal multicellularity was linked to a major shift in genome cis-regulatory complexity, most notably the appearance of distal enhancer regulation. ; This work was supported by an Institució Catalana de Recerca i Estudis Avançats contract, a European Research Council Consolidator Grant (ERC-2012-Co-616960), and a grant from Ministerio de Economía y Competitividad (MINECO) (BFU-2011-23434) (to I.R.-T.). We also acknowledge financial support from Secretaria d'Universitats i Recerca del Departament d'Economia i Coneixement de la Generalitat de Catalunya (project 2014 SGR 619). The work in L.D.'s laboratory was supported by grants from the Spanish "Ministerio de Educación y Ciencia" (SAF2013-48926-P), AGAUR, and the European Commission's 7th Framework Program 4DCellFate (277899). A.S.-P. is supported by an EMBO Long-Term Fellowship (ALTF 841-2014). J.L.G.-S. was funded by grants from Ministerio de Economía y Competitividad (BFU2013-41322-P) and the Andalusian Government (BIO-396). J.J.T. has a postdoctoral grant from the University Pablo de Olavide. The CRG/UPF Proteomics Unit is part of the "Plataforma de Recursos Biomoleculares y Bioinformáticos (ProteoRed)" supported by a grant from Instituto de Salud Carlos III (ISCIII) (PT13/0001). ; Peer reviewed

Cell-specific regulation of protein levels and activity is essential for the distribution of functions among multiple cell types in animals. The finding that many genes involved in these regulatory processes have a premetazoan origin raises the intriguing possibility that the mechanisms required for spatially regulated cell differentiation evolved prior to the appearance of animals. Here, we use high-throughput proteomics in Capsaspora owczarzaki, a close unicellular relative of animals, to characterize the dynamic proteome and phosphoproteome profiles of three temporally distinct cell types in this premetazoan species. We show that life-cycle transitions are linked to extensive proteome and phosphoproteome remodeling and that they affect key genes involved in animal multicellularity, such as transcription factors and tyrosine kinases. The observation of shared features between Capsaspora and metazoans indicates that elaborate and conserved phosphosignaling and proteome regulation supported temporal cell-type differentiation in the unicellular ancestor of animals. ; The CRG/UPF Proteomics Unit is part of the "Plataforma de Recursos Biomoleculares y Bioinformáticos (ProteoRed)" supported by grant PT13/0001 of Instituto de Salud Carlos III (ISCIII). A.S.-P. is supported by an EMBO Long-Term Fellowship (ALTF 841-2014). T.G. group research is funded in part by a grant from the Spanish Ministry of Economy and Competitiveness (BIO2012-37161), a grant from the Qatar National Research Fund (NPRP 5-298-3-086), a grant from the European Union FP7 FP7-PEOPLE-2013-ITN-606786, and a grant from the European Research Council under the European Union's Seventh Framework Program (FP/2007-2013)/ERC (grant agreement no. ERC-2012-StG-310325). I.R.-T. group research is supported by an Institució Catalana de Recerca i Estudis Avançats contract, a European Research Council Consolidator Grant (ERC-2012-Co-616960), and a grant (BFU-2011-23434) from Ministerio de Economía y Competitividad (MINECO). I.R.-T. also acknowledges financial support from Secretaria d'Universitats i Recerca del Departament d'Economia i Coneixement de la Generalitat de Catalunya (Project 2014 SGR 619 and Project 2014 SGR 678)