Salinity- and population-dependent genome regulatory response during osmotic acclimation in the killifish (Fundulus heteroclitus) gill

Abstract

SUMMARYThe killifish Fundulus heteroclitus is abundant in osmotically dynamic estuaries and it can quickly adjust to extremes in environmental salinity. We performed a comparative osmotic challenge experiment to track the transcriptomic and physiological responses to two salinities throughout a time course of acclimation, and to explore the genome regulatory mechanisms that enable extreme osmotic acclimation. One southern and one northern coastal population, known to differ in their tolerance to hypo-osmotic exposure, were used as our comparative model. Both populations could maintain osmotic homeostasis when transferred from 32 to 0.4p.p.t., but diverged in their compensatory abilities when challenged down to 0.1p.p.t., in parallel with divergent transformation of gill morphology. Genes involved in cell volume regulation, nucleosome maintenance, ion transport, energetics, mitochondrion function, transcriptional regulation and apoptosis showed population-and salinity-dependent patterns of expression during acclimation. Network analysis confirmed the role of cytokine and kinase signaling pathways in coordinating the genome regulatory response to osmotic challenge, and also posited the importance of signaling coordinated through the transcription factor HNF-4. These genome responses support hypotheses of which regulatory mechanisms are particularly relevant for enabling extreme physiological flexibility. Supplementary material available online at

Tilapia (Oreochromis mossambicus) brain cells respond to hyperosmotic challenge by inducingmyo-inositol biosynthesis

“…This is surprising given the fact that the synthesis of myo-inositol phosphate from G-6-P is the more rate-limiting step of the MIB pathway (Majumder et al, 1997), but does agree with a previous study that compared the regulation of the two enzymes (Sacchi et al, 2013). Significant upregulation or downregulation of IMPA1 mRNA under hyper-and hypo-osmotic challenge, respectively, has been reported in other teleost fishes (Evans and Somero, 2008;Kalujnaia et al, 2010;Whitehead et al, 2012). In leopard sharks, an osmoconforming species, inositol-related proteins have also been reported to be regulated in rectal gland and gill tissues in response to hypo-osmotic challenge (Dowd et al, 2010).…”

Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus

“…Scott et al (2004) reported F. heteroclitus population divergence in Cl − regulation following freshwater challenges. However, previous high-salinity challenges showed no loss of osmolyte balance and no difference between northern and southern populations (Scott et al, 2008;Scott and Schulte, 2005 (Whitehead et al, 2012b). Thus, we find that osmotic challenges spanning the salinity threshold across which gills are remodeled (∼1 p.p.t.)…”

“…Other killifish studies have contrasted Atlantic coastal populations from northern and southern regions, where the FW-native population shows greatest genetic similarity to fish from the northern clade in both nuclear (Duvernell et al, 2008) and mitochondrial (Whitehead, 2009) markers. Northern fish display improved ability to maintain internal ion homeostasis in response to low salinity challenge compared with southern fish (Whitehead et al, 2012b;Scott et al, 2004).…”

“…In killifish, the seawater gill type contains recessed MRCs and ion regulation in high salinities relies on the active excretion of Cl − in MRCs and the passive diffusion of Na + through leaky cell-cell junctions between MRCs and ACs (Wilson and Laurent, 2002). In contrast, the killifish freshwater gill comprises flatsurfaced MRCs with large external surface area (Katoh et al, 2001;Whitehead et al, 2012b). In fresh water, Na + is actively imported but Cl − is not; rather, plasma Cl − concentration is maintained by preventing loss through tight cell-cell junctions (Laurent et al, 2006;Wood and Laurent, 2003) or by stimulating dietary Cl − uptake (Wood et al, 2010).…”

Deepwater Horizon Oil Spill as a Case Study for Interdisciplinary Cooperation within Developmental Biology, Environmental Sciences and Physiology

“…Indeed, even intraspecific differences in the response to environmental stressors exist, and likely influence the response to crude oil [31]. Killifish populations on the East Coast of the US have variable responses to thermal and salinity stress [32] [33], and some have developed a resistance to PAH teratogenicity, and toxicity in adults [34] [35]. RECOVER physiologists and collaborators in the ecological and molecular sciences are using populations of Fundulus grandis found along the Gulf of Mexico coast to better understand how a species of fish may react differently to PAH exposure from oil based on their respective exposure histories.…”