Pressure-Sensing Ciliary Photoreceptors Regulate Depth-Retention Behavior in Marine Zooplankton

Conceptos Básicos

Ciliary photoreceptor cells in the brain of marine zooplankton larvae function as pressure sensors, activating a neuronal circuit that increases ciliary beating to drive upward swimming in response to increased pressure.

Resumen

The study investigates the cellular and neuronal mechanisms underlying the pressure response in the planktonic larvae of the marine annelid Platynereis dumerilii. The key findings are:

Platynereis larvae exhibit a graded, rapid, and adapting upward swimming response upon increases in hydrostatic pressure. This barokinetic response helps the larvae maintain their position in the water column.

Calcium imaging reveals that the brain ciliary photoreceptor cells (cPRCs) show a graded activation in response to pressure increases. The cPRCs are the primary pressure sensors in the larvae.

Genetic knockout of the ciliary opsin c-ops-1 in the cPRCs leads to a weaker pressure response, due to structural defects in the cPRC cilia.

The cPRCs synaptically connect to serotonergic ciliomotor neurons (Ser-h1), which are required to increase ciliary beating frequency upon pressure increase. Inhibiting synaptic transmission from Ser-h1 neurons dampens the pressure-induced increase in ciliary beating.

The study proposes that the cPRC-Ser-h1 circuit functions as a depth-retention mechanism, allowing the larvae to compensate for changes in depth and hydrostatic pressure through modulation of ciliary beating.

Overall, the findings reveal that multiciliated sensory cells can function as pressure receptors, integrating multiple sensory modalities to guide depth-regulating behaviors in marine zooplankton.

Estadísticas

"Pressure levels between 10 and 100 mb with 10 mb increments were chosen and applied in a randomized order."
"The maximum ciliary beat frequency (max. CBF) during the stimulus period showed a statistically significant increase for all but the lowest pressure steps tested relative to the period before the onset of the stimulus (85 mb p = 0.046, 237.5 mb p = 2.08 E-05, 556 mb p = 8.35 E-07, 988 mb p = 7.8 E-07)."
"The difference in the response between pressure levels was statistically significant for some of the cPRCs."

Citas

"Increased pressure induced a rapid, graded and adapting upward swimming response due to the faster beating of cilia in the head multiciliary band."
"Genetic inhibition of the serotonergic cells blocked pressure-dependent increases in ciliary beating."
"Our experiments suggest that Platynereis larvae react to relative increases in pressure in a graded manner proportional to the magnitude of the increase."

Ideas clave extraídas de

Mechanism of barotaxis in marine zooplankton

by Bezares Cald... a las www.biorxiv.org 03-01-2023

https://www.biorxiv.org/content/10.1101/2023.02.28.530398v3

Consultas más profundas

How do the pressure sensing mechanisms in the cPRCs compare to other known mechanosensory structures, such as the statocysts in crabs or the vestibular organs in vertebrates?

The pressure sensing mechanisms in the ciliary photoreceptor cells (cPRCs) of marine zooplankton, such as Platynereis larvae, show similarities and differences compared to other known mechanosensory structures. In the case of the statocysts in crabs, these structures typically contain sensory hairs that detect changes in pressure due to the movement of statoliths within the chamber. The movement of these statoliths in response to gravity or pressure changes triggers sensory neurons, leading to a physiological response. On the other hand, in vertebrates, the vestibular organs, such as the utricle and saccule in the inner ear, contain hair cells that detect changes in head position and movement, including changes in pressure.
In contrast, the cPRCs in marine zooplankton like Platynereis larvae detect pressure changes through the faster beating of cilia in the head multiciliary band. These cPRCs function as pressure sensors and activate ciliary beating through serotonergic signaling during barokinesis. The cPRCs respond to pressure increases by showing a graded and adapting upward swimming response, which is proportional to the magnitude of the pressure change. This mechanism is unique in that it involves the activation of specific sensory cells with cilia, which then transmit signals to the downstream circuit to regulate swimming behavior in response to pressure changes.
Overall, while the basic principle of detecting pressure changes through sensory structures is shared among these different organisms, the specific mechanisms and structures involved in pressure sensing can vary based on the evolutionary adaptations and ecological niches of the organisms.

How do the potential evolutionary origins and selective pressures that led to the development of multiciliated pressure receptors in marine zooplankton?

The development of multiciliated pressure receptors in marine zooplankton, such as the ciliary photoreceptor cells (cPRCs) in Platynereis larvae, can be attributed to evolutionary origins and selective pressures related to their ecological niche and behavioral adaptations.
One potential evolutionary origin of multiciliated pressure receptors is the need for marine zooplankton to sense and respond to changes in hydrostatic pressure, which is a dominant environmental cue for vertically migrating organisms in the ocean. The ability to detect pressure changes allows these organisms to regulate their depth in the water column, which is crucial for survival, predator avoidance, and finding optimal environmental conditions. The development of specialized sensory cells like cPRCs with multiple cilia may have provided a selective advantage in detecting and responding to pressure changes with precision and efficiency.
Selective pressures related to the marine environment, such as changes in water pressure due to depth variations, tidal rhythms, and currents, could have driven the evolution of multiciliated pressure receptors. Organisms that could sense and respond to these pressure changes effectively would have had a higher likelihood of survival and reproductive success. Over time, natural selection may have favored the development and refinement of multiciliated pressure receptors in marine zooplankton as an adaptive trait for navigating and thriving in their dynamic aquatic habitats.
In summary, the evolutionary origins of multiciliated pressure receptors in marine zooplankton likely stem from the need to adapt to the environmental challenges and selective pressures of the marine ecosystem, where precise pressure sensing and response mechanisms are essential for survival and fitness.

Could the integration of pressure and light sensing in the cPRCs be a common feature across different marine invertebrate larvae, and how might this influence their vertical migration behaviors and depth regulation?

The integration of pressure and light sensing in the ciliary photoreceptor cells (cPRCs) of marine invertebrate larvae, such as Platynereis larvae, could be a common feature across different species and may play a significant role in influencing their vertical migration behaviors and depth regulation.
Many marine invertebrate larvae exhibit vertical migration behaviors to optimize their position in the water column for feeding, predator avoidance, and reproduction. By integrating pressure and light sensing in the cPRCs, these larvae can effectively regulate their depth and position in response to environmental cues. The cPRCs act as multifunctional sensory cells that can detect changes in hydrostatic pressure and light intensity, allowing larvae to make informed decisions about their vertical movements.
The integration of pressure and light sensing in cPRCs may provide marine invertebrate larvae with a comprehensive sensory system for navigating and responding to their surroundings. For example, changes in pressure due to depth variations or water currents could trigger upward or downward swimming responses, while light cues could influence their orientation and movement towards or away from light sources. By combining these sensory inputs, larvae can adjust their vertical migration behaviors to optimize their chances of survival and reproductive success in the marine environment.
Overall, the integration of pressure and light sensing in cPRCs is likely a common feature in marine invertebrate larvae, and it serves as a sophisticated mechanism for depth regulation and vertical migration behaviors in response to environmental stimuli. This sensory integration allows larvae to adapt to changing conditions in their aquatic habitats and maximize their fitness in dynamic marine ecosystems.