RESUMEN
An important question in cell biology is how cytoskeletal proteins evolved and drove the development of novel structures and functions. Here we address the origin of SPIRE actin nucleators. Mammalian SPIREs work with RAB GTPases, formin (FMN)-subgroup actin assembly proteins and class-5 myosin (MYO5) motors to transport organelles along actin filaments towards the cell membrane. However, the origin and extent of functional conservation of SPIRE among species is unknown. Our sequence searches show that SPIRE exist throughout holozoans (animals and their closest single-celled relatives), but not other eukaryotes. SPIRE from unicellular holozoans (choanoflagellate), interacts with RAB, FMN and MYO5 proteins, nucleates actin filaments and complements mammalian SPIRE function in organelle transport. Meanwhile SPIRE and MYO5 proteins colocalise to organelles in Salpingoeca rosetta choanoflagellates. Based on these observations we propose that SPIRE originated in unicellular ancestors of animals providing an actin-myosin driven exocytic transport mechanism that may have contributed to the evolution of complex multicellular animals.
Asunto(s)
Actomiosina , Orgánulos , Animales , Orgánulos/metabolismo , Actomiosina/metabolismo , Proteínas de Microfilamentos/metabolismo , Proteínas de Microfilamentos/genética , Miosina Tipo V/metabolismo , Miosina Tipo V/genética , Actinas/metabolismo , Humanos , Coanoflagelados/metabolismo , Citoesqueleto de Actina/metabolismo , Evolución Biológica , Evolución Molecular , Forminas/metabolismo , Proteínas de Unión al GTP rab/metabolismo , Filogenia , Proteínas NuclearesRESUMEN
The Shaker family of voltage-gated K+ channels has been thought of as an animal-specific ion channel family that diversified in concert with nervous systems. It comprises four functionally independent gene subfamilies (Kv1-4) that encode diverse neuronal K+ currents. Comparison of animal genomes predicts that only the Kv1 subfamily was present in the animal common ancestor. Here, we show that some choanoflagellates, the closest protozoan sister lineage to animals, also have Shaker family K+ channels. Choanoflagellate Shaker family channels are surprisingly most closely related to the animal Kv2-4 subfamilies which were believed to have evolved only after the divergence of ctenophores and sponges from cnidarians and bilaterians. Structural modeling predicts that the choanoflagellate channels share a T1 Zn2+ binding site with Kv2-4 channels that is absent in Kv1 channels. We functionally expressed three Shakers from Salpingoeca helianthica (SheliKvT1.1-3) in Xenopus oocytes. SheliKvT1.1-3 function only in two heteromultimeric combinations (SheliKvT1.1/1.2 and SheliKvT1.1/1.3) and encode fast N-type inactivating K+ channels with distinct voltage dependence that are most similar to the widespread animal Kv1-encoded A-type Shakers. Structural modeling of the T1 assembly domain supports a preference for heteromeric assembly in a 2:2 stoichiometry. These results push the origin of the Shaker family back into a common ancestor of metazoans and choanoflagellates. They also suggest that the animal common ancestor had at least two distinct molecular lineages of Shaker channels, a Kv1 subfamily lineage predicted from comparison of animal genomes and a Kv2-4 lineage predicted from comparison of animals and choanoflagellates.
Asunto(s)
Coanoflagelados , Evolución Molecular , Canales de Potasio de la Superfamilia Shaker , Animales , Coanoflagelados/genética , Coanoflagelados/metabolismo , Canales de Potasio de la Superfamilia Shaker/genética , Canales de Potasio de la Superfamilia Shaker/metabolismo , Filogenia , Secuencia de AminoácidosRESUMEN
Thibaut Brunet is a group leader at the Institut Pasteur in Paris, France, where he works on choanoflagellates (known as 'choanos' for short). These unicellular organisms are close relatives of animals that have the potential to form multicellular assemblies under certain conditions, and Thibaut's lab are leveraging them to gain insights into how animal morphogenesis evolved. We met with Thibaut over Zoom to discuss his career path so far, and learnt how an early interest in dinosaurs contributed to his life-long fascination with evolutionary biology.
Asunto(s)
Evolución Biológica , Coanoflagelados , Biología Evolutiva , Animales , Biología Evolutiva/historia , Historia del Siglo XXI , Morfogénesis , Historia del Siglo XXRESUMEN
How do distinct species cofunction in symbiosis, despite conflicting interests? A new collection of articles explores emerging themes as researchers exploit modern research tools and new models to unravel how symbiotic interactions function and evolve.
Asunto(s)
Coanoflagelados , SimbiosisRESUMEN
Environmental bacteria influence many facets of choanoflagellate biology, yet surprisingly few examples of symbioses exist. We need to find out why, as choanoflagellates can help us to understand how symbiosis may have shaped the early evolution of animals.