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Colgren, J.

Publications and source records attributed to Colgren, J..

4 recordsLinked to original sources

Diversity and Spatial Segregation of TRP Channels in Choanoflagellates Provide Insight into the Evolutionary Origin of Animal Sensory Systems

Sensory systems, built around specialized cell types, are central to how animals perceive and respond to their environments. Yet many of the molecular components defining these systems predate the origin of animal multicellularity. Among these, transient receptor potential (TRP) channels form a polymodal and evolutionarily ancient superfamily of ion channels involved in diverse sensory processes. To better understand how sensory complexity emerged in animals, we investigated the diversity of TRP channels in choanoflagellates, the closest living relatives of animals. Using a combination of homology-based searches, phylogenetics, and structural predictions, we find extensive TRP channel repertoires across choanoflagellates, including representatives of most major animal TRP channel families. Comparative analyses across species revealed two distinct evolutionary patterns for TRP channel families: conserved, low-copy families with stable domain architectures, and lineage-specific expansions within the families TRPM and TRPW, indicative of functional diversification. Functional insights from fluorescent localization studies in the choanoflagellate Salpingoeca rosetta demonstrated that TRPA, TRPC, and TRPV channels are spatially segregated within the collar complex, a key interface for environmental sensing and feeding. Distinct localization domains, along with evidence for heteromeric interactions between TRPA paralogs, suggest that subcellular organization likely contributes to sensory specialization in these single cells. Together, our findings indicate that a diverse and functionally versatile TRP channel toolkit was already present in the last common ancestor of choanoflagellates and animals. We propose that the evolution of animal sensory systems involved both expansion and reorganization of this ancestral repertoire, with subcellular patterning in unicellular organisms representing a precursor to cell-type specialization in multicellular animals.

evolutionary biology↗

Ancient nervous system architecture in a living ctenophore

The evolutionary origin of nervous systems in animals remains elusive and is largely hidden from the fossil record. Ctenophores, one of the earliest-branching animals possessing neurons, are instrumental to our understanding of nervous system origin, and a few rare ctenophore fossils preserve traces of nervous tissue as carbonaceous remains. Cambrian ctenophores appear to exhibit a more diverse neuroanatomy than that of modern species, suggesting secondary loss in extant ctenophores. However, much remains unknown about the origin and ontogeny giving rise to the structural organization of modern ctenophore nervous systems. Here, by investigating the neural anatomy of the ctenophore Mnemiopsis leidyi during development, we identified a ladder-like nerve net (LNN) beneath the comb rows that converges into condensed neurites and connects to the aboral organ. Examination of carbon-rich areas of Ctenorhabdotus capulus, an extinct ctenophore from the Burgess Shale, reveals a pattern similar to that of M. leidyi, consistent with a shared neural organization. Furthermore, M. leidyi exhibits a condensed comb nerve, resembling the longitudinal nerve preserved in the Cambrian ctenophore Fasciculus vesanus and the giant axon of extant Euplokamis dunlapae. Our study reveals conserved evolutionary constraints shaping nervous system architectures linked to locomotory organs and indicates that the different modes of nervous system organization observed in Cambrian ctenophores are variably retained in modern species.

neuroscience↗

The 3D architecture of the ctenophore aboral organ and the evolution of complex integrative centers in animals

The ability to sense and respond to environmental cues is fundamental to animal behavior and survival. In ctenophores - early-branching marine animals - a syncytial nerve net underlies complex behaviors such as geotaxis, feeding, and escape. At the center of this system is the aboral organ (AO), a dense sensory hub that detects motion, light, and pressure and coordinates ciliary movement. However, the AOs cellular architecture and its integration with the nerve net remain poorly understood. Here, using volume electron microscopy in Mnemiopsis leidyi, we reveal that the syncytial nerve net converges and condenses around the AO, forming synaptic connections with diverse effector cells. We annotated 17 distinct cell types, including candidate light and pressure sensors, novel ciliated and secretory cells, and non-synaptic vesicle-rich cells likely involved in volume transmission. Our data shows that signal processing within the AO relies on both synaptic and non-synaptic communication. Gene expression profiling of conserved transcription factors indicates that the AO is a functionally convergent, evolutionarily distinct sensory structure that retains minimal homology. Our findings redefine the ctenophore AO as a highly integrated, multilayered sensory system critical for behavioral regulation.

evolutionary biology↗

Electrical signaling and coordinated behavior in the closest relative of animals

The transition between simple to complex multicellularity involves large degrees of division of labor and specialization of cell types. In animals, complex sensory motor systems are primarily built around the fundamental cell types of muscles and neurons, though the evolutionary origin of these cells, and their integration, remains unclear. Here, in order to investigate sensory-behavior coupling in the closest relatives of animals, we established a line of the choanoflagellate, Salpingoeca rosetta, which stably expresses the calcium indicator RGECO1. Using this, we identify a novel cellular behavior associated with electrical signaling, in which ciliary arrest is coupled with apical-basal contraction of the cell. This behavior, and the associated calcium transients, are synchronized in the multicellular state and result in coordinated ciliary arrest and colony wide contraction, suggesting information is spread amongst the cells. Our work reveals fundamental insights into how choanoflagellates sense and respond to their environment and offer a new perspective into the integration of cellular and organism wide behavior in the closest protistan relatives of animals.

evolutionary biology↗