Hydrogen sulphide sensitivity and tolerance in genetically distinct lineages of a selfing mangrove fish ( Kryptolebias m

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ORIGINAL ARTICLE

Hydrogen sulphide sensitivity and tolerance in genetically distinct lineages of a selfing mangrove fish (Kryptolebias marmoratus) Keri E. Martin1   · Suzanne Currie2  Received: 28 April 2020 / Revised: 16 July 2020 / Accepted: 4 August 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract Mangroves are critical marine habitats. High hydrogen sulphide (H2S) is a feature of these important ecosystems and its toxicity creates a challenge for mangrove inhabitants. The mangrove rivulus (Kryptolebias marmoratus) is a selfing, hermaphroditic, amphibious fish that can survive exposure to 1116 μM H ­ 2S in the wild. These fish rely on cutaneous respiration for gas and ion exchange when emerged. We hypothesized that the skin surface is fundamentally important in H ­ 2S tolerance in these mangrove fish by limiting H ­ 2S permeability. To test our hypothesis, we first disrupted the skin surface in one isogenic lineage and measured H ­ 2S tolerance and sensitivity. We increased water H ­ 2S concentration until emersion as a measure of the ability to sense and react to ­H2S, which we refer to as sensitivity. We then determined ­H2S tolerance by preventing emersion and increasing H ­ 2S until loss of equilibrium (LOE). The H ­ 2S concentration at emersion and LOE were significantly affected by disrupting the skin surface, providing support that the skin is involved in limiting ­H2S permeability. Capitalizing on their unique reproductive strategy, we used three distinct isogenic lineages to test the hypothesis that there would be genetic differences in ­H2S sensitivity and tolerance. We found significant differences in emersion concentration only among lineages, suggesting a genetic component to H ­ 2S sensitivity but not tolerance. Our study also demonstrated that external skin modifications and avoidance behaviours are two distinct strategies used to tolerate ecologically relevant H ­ 2S concentrations and likely facilitate survival in challenging mangrove habitats. Keywords  Mangrove rivulus · Emersion · Isogenic · Mucous

Introduction Hydrogen sulphide (­H2S) is a dangerous aquatic toxin, lethal to most animals at low concentrations (Reiffenstein et  al. 1992). ­H2S reversibly binds to cytochrome c oxidase, hemoglobin and other enzymes (e.g. succinic dehydrogenase, ATPase, glucose-6-phosphate dehydrogenase) inhibiting mitochondrial respiration and oxygen transport (Bagarinao 1992; Cooper and Brown 2008). Hydrogen sulphide is produced endogenously at low levels by enzymatic and non-enzymatic pathways and acts as a gasotransmitter Communicated by Bernd Pelster. * Suzanne Currie [email protected] 1



Department of Biology, Mount Allison University, Sackville, NB, Canada



Department of Biology, Acadia University, Wolfville, NS, Canada

2

influencing several intracellular signaling processes, dilating blood vessels and decreasing blood pressure (Olson 2008; Li et al. 2011). In the environment, H ­ 2S is produced naturally, either geothermally or by bacterial metabolism, and/ or an