Electrical signaling and coordinated behavior in the closest relative of animals

[Chip (OP)]

Source: https://www.science.org/doi/10.1126/sciadv.adr7434

Science Advances, 8 Jan 2025, Vol 11, Issue 2

DOI: 10.1126/sciadv.adr7

Abstract

The transition from simple to complex multicellularity involves division of labor and specialization of cell types. In animals, complex sensory-motor systems are primarily built around specialized cells of muscles and neurons, though the evolutionary origins of these and their integration remain unclear.

Here, 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 previously unknown cellular behavior associated with electrical signaling, in which ciliary arrest (they stop moving) is coupled with apical-basal contraction (orientation of the cell's membrane domains) 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 that information is spread among the cells.

Our work reveals fundamental insights into how choanoflagellates sense and respond to their environment and enhances our understanding of the integration of cellular and organism-wide behavior in the closest protistan relatives of animals and are
a diverse group of eukaryotic microorganisms that are not plants, animals, or fungi.

**Choanoflagellates** are fascinating unicellular or colonial protozoans that are considered to be the closest living relatives of animals.

INTRODUCTION

Animals move through and interact with their environments in ways unique to life on earth.

Calcium signaling is at the crux of this sensory-behavioral integration, playing a role in every modality from initial signal detection to downstream responses. This is achieved through dynamic control of free cytoplasmic calcium concentrations, and modulation of calcium entry, release, and clearance.

Although the emergence of calcium as a signaling molecule is very ancient, there are marked differences in the mechanisms used by plants, fungi, and animals; the major lineages where complex multicellularity is present.

It is hypothesized that stable multicellularity provides strong pressure for the development of versatile communication systems between cells.

In animals, sensory-motor integration and coordinated behavior is primarily achieved by the activity of specialized cell types, neurons, and myocytes which are also known as **muscle cells**.

These excitable cells that depend on large and tightly regulated calcium events to trigger a rapid response.

On short timescales, this response can act to convert environmental information into electrical or chemical signals, propagate these signals, or convert the signal into force generation or movements.

On the basis of their broad phylogenetic distribution, muscles and neurons likely arose very early in animal evolution and potentially multiple times through convergence --
**Phylogenetics** is the study of the evolutionary relationships among species, organisms, or genes.

Furthermore, many of the proteins involved in these pathways are also found outside of animals, with a large collection found in the closest unicellular relatives of animals.

However, the function of these components and their level of integration within these organisms largely remains unstudied.

The ability to precipitate phosphate ions makes high calcium concentrations inherently toxic to life as we know it, resulting in strong evolutionary pressure on sequestering, compartmentalizing, and extruding calcium ions.

In animal cells, cytoplasmic (intra-cellular) levels of free calcium are in the nanomolar range, while extra-cellular concentrations are in the millimolar range, and major intercellular stores in the micromolar range (up to the millimolar range in excitable cells, such as muscles and neurons).

Calcium is an important secondary messenger in animal excitable cells. As a general mechanism, membrane depolarization activates voltage-gated calcium channels (VGCCs), which leads to an influx in calcium.

(FYI: drugs like Gabapentin and Pregabalin VGCC inhibitors or blockers)

This influx can then trigger an immediate response (such as vesicle-, which are small, membrane-bound sacs that transport and store various substances within cells, -fusion in neurons) or further release of calcium stores (as in muscle contraction).

These are transient events, and clearing of signal occurs via segregation by calcium binding proteins, compartmentalization into internal stores, and/or extrusion from the cell.

VGCCs are broadly distributed in eukaryotes (which have a nucleus enclosed within a nuclear envelope. This group includes animals, plants, fungi, and protists), and have been shown to influence/regulate flagellar (little tails to mobilise them) movements in paramecium (a single-celled organism that belongs to the kingdom Protista) and Chlamydomonas and mediate infection by various parasitic protists, as well as leaf movement in plants.

In animals, these channels can be broadly characterized into low-voltage activation and high-voltage activated channels.
Phylogenetic analyses have shown that choanoflagellates, the closest known living relative to animals, have a single member of each of these categories.

Choanoflagellates are bacterivorous filter feeders and are highly polarized cells characterized by a single apical flagellum, surrounded by a microvilli-(tiny, finger-like projections found on the surface of certain cells)-based collar.

The planar beating of the flagellum generates flow, which draws bacterial prey into contact with the collar where it is phagocytized (to **phagocytize** means to engulf and digest particles, such as bacteria or other foreign substances).

Choanoflagellates have complex life cycles, with some displaying transient multicellularity, which is generally achieved through serial cell division.

The choanoflagellate model Salpingoeca rosetta has at least six distinct cell stages:

1. linear chain colonies,
2. rosette colonies,
3. slow swimming solitary cells,
4. fast swimming solitary cells,
5. attached cells, and
6. ameboid-like cells following physical confinement.

Both chain colonies and rosette colonies occur through serial cell division followed by incomplete abscission (**Abscission** is the process by which plants shed their leaves, flowers, fruits, or seeds. This is a natural phenomenon that allows plants to conserve resources, dispose of damaged or unnecessary parts), which leaves a small cytoplasmic bridge between the cells.

These bridges have only been observed by electron microscopy and contain two electron-dense structures each localized near one of the cells.

Under nutrient-rich conditions, cells divide rapidly in chains before separating into slow swimmers.

Environmental cues, such as the presence of specific bacterial sulfonolipids (fats and oils that contain sulphur), can trigger the development of rosette colonies.

In this case, the cells secrete extracellular matrix (ECM) from their base into the central region of the group of cells. The result is a multicellular ball with the collars and flagella facing outward.

The cytoplasmic bridges are maintained in this state and can take on a highly complex arrangement.

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