Adaptive cell invasion maintains lateral line organ homeostasis in response to environmental changes.

Mammalian inner ear and fish lateral line sensory hair cells (HCs) detect fluid motion to transduce environmental signals. Actively maintained ionic homeostasis of the mammalian inner ear endolymph is essential for HC function. In contrast, fish lateral line HCs are exposed to the fluctuating ionic composition of the aqueous environment. Using lineage labeling, in vivo time-lapse imaging and scRNA-seq, we discovered highly motile skin-derived cells that invade mature mechanosensory organs of the zebrafish lateral line and differentiate into Neuromast-associated (Nm) ionocytes. This invasion is adaptive as it is triggered by environmental fluctuations. Our discovery of Nm ionocytes challenges the notion of an entirely placodally derived lateral line and identifies Nm ionocytes as likely regulators of HC function possibly by modulating the ionic microenvironment. Nm ionocytes provide an experimentally accessible in vivo system to study cell invasion and migration, as well as the physiological adaptation of vertebrate organs to changing environmental conditions. [Display omitted] • Mature lateral line sensory organs contain non-lateral-line-derived cells • Skin-derived Nm ionocyte pairs migrate and invade lateral line sensory organs • Nm ionocytes are recruited in response to environmental fluctuations • Mutants that lack ionocytes possess decreased hair cell mechanotransduction Peloggia and Münch et al. report the discovery of a cell type in lateral line neuromasts, Nm ionocytes. Nm ionocytes invade mature sensory organs in a salinity- and pH-dependent manner, a process named adaptive cell invasion. This process allows for physiological adaptation of sensory organs to fluctuating environmental conditions. [ABSTRACT FROM AUTHOR]