Two paused Trichoplax adhaerens feeding on a bed of microalgae (dark particles). Photo credit: Carolyn Smith.

Two paused Trichoplax adhaerens feeding on a bed of microalgae (dark particles). Photo credit: Carolyn Smith.

Gliding on microscopic beating hairs as it grazes upon microalgae coating surfaces in warm oceans, tiny Trichoplax adhaerens is one of the most ancient and simplest animals on the planet. Lacking a brain, gut and nervous system, the 1 mm diameter flat creatures are composed of only six different cell types that perform a variety of roles, including sensing their surroundings, digestion and movement. Without nerves to coordinate their actions, it was unclear how the small animals organise their basic grazing lifestyle and cease moving when they encounter food. Another ancient family of animals, jellyfish, release short protein-like molecules – called neuropeptides, which can trigger nerve signals – from sensory cells to control their actions, so Carolyn Smith, from the National Institutes of Health, USA, and her colleagues Adriano Senatore and Thomas Reese began investigating whether Trichoplax also produce neuropeptide-like molecules to control their movements without the benefit of a nervous system.

As many of these neuropeptide-like molecules are produced as inactive precursors, which are then activated by trimming, Smith and her team selected a range of off-the-shelf neuropeptides that are similar to neuropeptide precursors that had previously been identified in the Trichoplax genome, including two versions of the activated mammalian neuropeptide, endomorphin. After being injected into the animals’ water, both of the mammalian endomorphin neuropeptides caused the microscopic hairs that propel the flat creatures along to cease moving, and the animals paused. But could the trio find evidence of genes that are similar to the endomorphin neuropeptide in Trichoplax?

A search of the animal's gene database turned up a gene that could produce an inactive endomorphin-like neuropeptide molecule, and when the team produced an artificial version of the neuropeptide and injected minute quantities of it into the water immediately surrounding Trichoplax individuals, the animals paused within 30 s: the synthetic endomorphin-like neuropeptide seems to control the animal's ability to pause when feeding. Also, when the team filmed clusters of grazing Trichoplax, they noticed that as soon as one animal paused, other animals in close proximity did so too. The team then used fluorescent antibody tags to reveal that the endomorphin-like neuropeptide was located in tiny granules in sensory cells that are clustered around the edge of the animal's disk-shaped body.

But one question puzzled the team: how could secretions from a small number of endomorphin-like neuropeptide producing cells on the Trichoplax surface trigger all of the hairs distributed across the animal's surface to stop beating? ‘The answer we propose comes from the observation that animals in groups pause in coordination’, says Smith. She suspects that when Trichoplax encounter algae, the sensory cells that detect the algae release the endomorphin-like neuropeptide, which then triggers other nearby sensory cells to release more neuropeptide, sparking a cascade of neuropeptide release across the animal, stopping it in its tracks. ‘By these means, a small number of secretory cells detecting algal cells can arrest ciliary beating across the entire animal’, says Smith, adding that these secretory cells ‘share many of the molecular characteristics of sensory neurons in more complex animals and appear to perform a similar function’.

Senatore
,
A.
,
Reese
,
T. S.
and
Smith
,
C. L.
(
2017
).
Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses
.
J. Exp. Biol.
220
,
3381
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3390
.