Jordi Paps

The oyster genome reveals stress adaptation and complexity of shell formation

The Pacific oyster Crassostrea gigas belongs to one of the most species-rich but genomically poorly explored phyla, the Mollusca. Here we report the sequencing and assembly of the oyster genome using short reads and a fosmid-pooling strategy, along with transcriptomes of development and stress response and the proteome of the shell. The oyster genome is highly polymorphic and rich in repetitive sequences, with some transposable elements still actively shaping variation. Transcriptome studies reveal an extensive set of genes responding to environmental stress. The expansion of genes coding for heat shock protein 70 and inhibitors of apoptosis is probably central to the oyster’s adaptation to sessile life in the highly stressful intertidal zone. Our analyses also show that shell formation in molluscs is more complex than currently understood and involves extensive participation of cells and their exosomes. The oyster genome sequence fills a void in our understanding of the Lophotrochozoa.

The genomes of four tapeworm species reveal adaptations to parasitism.

Tapeworms (Cestoda) cause neglected diseases that can be fatal and are difficult to treat, owing to inefficient drugs. Here we present an analysis of tapeworm genome sequences using the human-infective species Echinococcus multilocularis, E. granulosus, Taenia solium and the laboratory model Hymenolepis microstoma as examples. The 115- to 141-megabase genomes offer insights into the evolution of parasitism. Synteny is maintained with distantly related blood flukes but we find extreme losses of genes and pathways that are ubiquitous in other animals, including 34 homeobox families and several determinants of stem cell fate. Tapeworms have specialized detoxification pathways, metabolism that is finely tuned to rely on nutrients scavenged from their hosts, and species-specific expansions of non-canonical heat shock proteins and families of known antigens. We identify new potential drug targets, including some on which existing pharmaceuticals may act. The genomes provide a rich resource to underpin the development of urgently needed treatments and control.

A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians

Bilateria are currently subdivided into three superclades: Deuterostomia, Ecdysozoa, and Lophotrochozoa. Within this new taxonomic frame, acoelomate Platyhelminthes, for a long time held to be basal bilaterians, are now considered spiralian lophotrochozoans. However, recent 18S rDNA [small subunit (SSU)] analyses have shown Platyhelminthes to be polyphyletic with two of its orders, the Acoela and the Nemertodermatida, as the earliest extant bilaterians. To corroborate such position and avoid the criticisms of saturation and long-branch effects thrown on the SSU molecule, we have searched for independent molecular data bearing good phylogenetic information at deep evolutionary nodes. Here we report a phylogenetic analysis of DNA sequences from the myosin heavy chain type II (myosin II) gene from a large set of metazoans, including acoels and nemertodermatids. Our study demonstrates, both for the myosin II data set alone and for a combined SSU + myosin II data set, that Platyhelminthes are polyphyletic and that acoels and nemertodermatids are the extant earliest bilaterians. Hence, the common bilaterian ancestor was not, as currently held, large and complex but small, simple, and likely with direct development. This scenario has far-reaching implications for understanding the evolution of major body plans and for perceptions of the Cambrian evolutionary explosion.

Phylogenetic Relationships within the Opisthokonta Based on Phylogenomic Analyses of Conserved Single-Copy Protein Domains

Many of the eukaryotic phylogenomic analyses published to date were based on alignments of hundreds to thousands of genes. Frequently, in such analyses, the most realistic evolutionary models currently available are often used to minimize the impact of systematic error. However, controversy remains over whether or not idiosyncratic gene family dynamics (i.e., gene duplications and losses) and incorrect orthology assignments are always appropriately taken into account. In this paper, we present an innovative strategy for overcoming orthology assignment problems. Rather than identifying and eliminating genes with paralogy problems, we have constructed a data set comprised exclusively of conserved single-copy protein domains that, unlike most of the commonly used phylogenomic data sets, should be less confounded by orthology miss-assignments. To evaluate the power of this approach, we performed maximum likelihood and Bayesian analyses to infer the evolutionary relationships within the opisthokonts (which includes Metazoa, Fungi, and related unicellular lineages). We used this approach to test 1) whether Filasterea and Ichthyosporea form a clade, 2) the interrelationships of early-branching metazoans, and 3) the relationships among early-branching fungi. We also assessed the impact of some methods that are known to minimize systematic error, including reducing the distance between the outgroup and ingroup taxa or using the CAT evolutionary model. Overall, our analyses support the Filozoa hypothesis in which Ichthyosporea are the first holozoan lineage to emerge followed by Filasterea, Choanoflagellata, and Metazoa. Blastocladiomycota appears as a lineage separate from Chytridiomycota, although this result is not strongly supported. These results represent independent tests of previous phylogenetic hypotheses, highlighting the importance of sophisticated approaches for orthology assignment in phylogenomic analyses.

Lophotrochozoa internal phylogeny: new insights from an up-to-date analysis of nuclear ribosomal genes

Resolving the relationships among animal phyla is a key biological problem that remains to be solved. Morphology is unable to determine the relationships among most phyla and although molecular data have unveiled a new evolutionary scenario, they have their own limitations. Nuclear ribosomal genes (18S and 28S rDNA) have been used effectively for many years. However, they are considered of limited use for resolving deep divergences such as the origin of the bilaterians, due to certain drawbacks such as the long-branch attraction (LBA) problem. Here, we attempt to overcome these pitfalls by combining several methods suggested in previous studies and routinely used in contemporary standard phylogenetic analyses but that have not yet been applied to any bilaterian phylogeny based on these genes. The methods used include maximum likelihood and Bayesian inference, the application of models with rate heterogeneity across sites, wide taxon sampling and compartmentalized analyses for each problematic clade. The results obtained show that the combination of the above-mentioned methodologies minimizes the LBA effect, and a new Lophotrochozoa phylogeny emerges. Also, the Acoela and Nemertodermatida are confirmed with maximum support as the first branching bilaterians. Ribosomal RNA genes are thus a reliable source for the study of deep divergences in the metazoan tree, provided that the data are treated carefully.

Bilaterian Phylogeny: A Broad Sampling of 13 Nuclear Genes Provides a New Lophotrochozoa Phylogeny and Supports a Paraphyletic Basal Acoelomorpha

During the past decade, great progress has been made in clarifying the relationships among bilaterian animals. Studies based on a limited number of markers established new hypotheses such as the existence of three superclades (Deuterostomia, Ecdysozoa, and Lophotrochozoa) but left major questions unresolved. The data sets used to the present either bear few characters for many taxa (i.e., the ribosomal genes) or present many characters but lack many phyla (such as recent phylogenomic approaches) failing to provide definitive answers for all the regions of the bilaterian tree. We performed phylogenetic analyses using a molecular matrix with a high number of characters and bilaterian phyla. This data set is built from 13 genes (8,880 bp) belonging to 90 taxa from 27 bilaterian phyla. Probabilistic analyses robustly support the three superclades, the monophyly of Chordata, a spiralian clade including Brachiozoa, the basal position of a paraphyletic Acoelomorpha, and point to an ecdysozoan affiliation for Chaetognatha. This new phylogeny not only agrees with most classical molecular results but also provides new insights into the relationships between lophotrochozoans and challenges the results obtained using high-throughput strategies, highlighting the problems associated with the current trend to increase gene number rather than taxa.

The phylogenetic position of ctenophores and the origin(s) of nervous systems

Ctenophores have traditionally been treated as eumetazoans, but some recent whole genome studies have revived the idea that they are, rather, the sister group to all other metazoans. This deep branching position implies either that nervous systems have evolved twice, in Ctenophora and in Eumetazoa, or that an ancestral metazoan nervous system has been lost in sponges and placozoans. We caution, however, that phylogenetic-tree construction artifacts may have placed ctenophores too deep in the metazoan tree. We discuss nervous system origins under these alternative phylogenies and in light of comparative data of ctenophore and eumetazoan nervous systems. We argue that characters like neuropeptide signaling, ciliary photoreceptors, gap junctions and presynaptic molecules are consistent with a shared ancestry of nervous systems. However, if ctenophores are the sister group to all other metazoans, this ancestral nervous system was likely very simple. Further studies are needed to resolve the deep phylogeny of metazoans and to have a better understanding of the early steps of nervous system evolution.

Back in time: a new systematic proposal for the Bilateria

Conventional wisdom suggests that bilateral organisms arose from ancestors that were radially, rather than bilaterally, symmetrical and, therefore, had a single body axis and no mesoderm. The two main hypotheses on how this transformation took place consider either a simple organism akin to the planula larva of extant cnidarians or the acoel Platyhelminthes (planuloid–acoeloid theory), or a rather complex organism bearing several or most features of advanced coelomate bilaterians (archicoelomate theory). We report phylogenetic analyses of bilaterian metazoans using quantitative (ribosomal, nuclear and expressed sequence tag sequences) and qualitative (HOX cluster genes and microRNA sets) markers. The phylogenetic trees obtained corroborate the position of acoel and nemertodermatid flatworms as the earliest branching extant members of the Bilateria. Moreover, some acoelomate and pseudocoelomate clades appear as early branching lophotrochozoans and deuterostomes. These results strengthen the view that stem bilaterians were small, acoelomate/pseudocoelomate, benthic organisms derived from planuloid-like organisms. Because morphological and recent gene expression data suggest that cnidarians are actually bilateral, the origin of the last common bilaterian ancestor has to be put back in time earlier than the cnidarian–bilaterian split in the form of a planuloid animal. A new systematic scheme for the Bilateria that includes the Cnidaria is suggested and its main implications discussed.

Molecular phylogeny of unikonts: new insights into the position of apusomonads and ancyromonads and the internal relationships of opisthokonts.

The eukaryotic supergroup Opisthokonta includes animals (Metazoa), fungi, and choanoflagellates, as well as the lesser known unicellular lineages Nucleariidae, Fonticula alba, Ichthyosporea, Filasterea and Corallochytrium limacisporum. Whereas the evolutionary positions of the well-known opisthokonts are mostly resolved, the phylogenetic relationships among the more obscure lineages are not. Within the Unikonta (Opisthokonta and Amoebozoa), it has not been determined whether the Apusozoa (apusomonads and ancyromonads) or the Amoebozoa form the sister group to opisthokonts, nor to which side of the hypothesized unikont/bikont divide the Apusozoa belong. Aiming at elucidating the evolutionary tree of the unikonts, we have assembled a dataset with a large sampling of both organisms and genes, including representatives from all known opisthokont lineages. In addition, we include new molecular data from an additional ichthyosporean (Creolimax fragrantissima) and choanoflagellate (Codosiga botrytis). Our analyses show the Apusozoa as a paraphyletic assemblage within the unikonts, with the Apusomonadida forming a sister group to the opisthokonts. Within the Holozoa, the Ichthyosporea diverge first, followed by C. limacisporum, the Filasterea, the Choanoflagellata, and the Metazoa. With our data-enriched tree, it is possible to pinpoint the origin and evolution of morphological characters. As an example, we discuss the evolution of the unikont kinetid.

Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges.

BackgroundOne of the hallmarks of multicellular organisms is the ability of their cells to trigger responses to the environment in a coordinated manner. In recent years primary cilia have been shown to be present as ‘antennae’ on almost all animal cells, and are involved in cell-to-cell signaling in development and tissue homeostasis; how this sophisticated sensory system arose has been little-studied and its evolution is key to understanding how sensation arose in the Animal Kingdom. Sponges (Porifera), one of the earliest evolving phyla, lack conventional muscles and nerves and yet sense and respond to changes in their fluid environment. Here we demonstrate the presence of non-motile cilia in sponges and studied their role as flow sensors.ResultsDemosponges excrete wastes from their body with a stereotypic series of whole-body contractions using a structure called the osculum to regulate the water-flow through the body. In this study we show that short cilia line the inner epithelium of the sponge osculum. Ultrastructure of the cilia shows an absence of a central pair of microtubules and high speed imaging shows they are non-motile, suggesting they are not involved in generating flow. In other animals non-motile, ‘primary’, cilia are involved in sensation. Here we show that molecules known to block cationic ion channels in primary cilia and which inhibit sensory function in other organisms reduce or eliminate sponge contractions. Removal of the cilia using chloral hydrate, or removal of the whole osculum, also stops the contractions; in all instances the effect is reversible, suggesting that the cilia are involved in sensation. An analysis of sponge transcriptomes shows the presence of several transient receptor potential (TRP) channels including PKD channels known to be involved in sensing changes in flow in other animals. Together these data suggest that cilia in sponge oscula are involved in flow sensation and coordination of simple behaviour.ConclusionsThis is the first evidence of arrays of non-motile cilia in sponge oscula. Our findings provide support for the hypothesis that the cilia are sensory, and if true, the osculum may be considered a sensory organ that is used to coordinate whole animal responses in sponges. Arrays of primary cilia like these could represent the first step in the evolution of sensory and coordination systems in metazoans.