Transcriptional Basis of Copper-Induced Olfactory Impairment in the Sea Lamprey, a Primitive Invasive Fish

Abstract

Olfaction mediates behaviors necessary for survival and reproduction in fishes. Anthropogenic inputs of contaminants into aquatic environments, specifically copper, are known to disrupt a broad range of olfactory-mediated behaviors and can cause long-lasting damage even at low concentrations that have profound impacts on the biology of aquatic organisms. The sea lamprey ( Petromyzon marinus) is a primitive fish species invasive to the North American Great Lakes that relies on olfaction to navigate during natal homing and in mate choice during reproduction. To investigate effects of copper on sea lamprey olfaction and the potential for maintenance of olfactory function during copper exposure, we exposed juvenile sea lamprey to environmentally ecologically relevant copper concentrations (0, 5, 10 and 30 µg/L) for 24 hr and characterized gene transcription response in olfactory tissue ( i.e. , peripheral olfactory organ and olfactory bulb) and forebrain using whole transcriptome sequencing. Copper exposure induced a pattern of positive dose-dependent transcriptional response. Expression changes primarily reflected up-regulation of genes involved in apoptosis and wound healing. Unlike higher vertebrates, genes specifically related to the olfactory senses of the sea lamprey, e.g. , olfactory receptors, exhibited little transcriptional response to copper exposure, suggesting the mechanism of copper-induced olfactory impairment is through necrosis of the olfactory bulb and not copper-selective inhibition of olfactory receptors. Fully two-thirds of the differentially expressed genes at higher doses of copper have no known function and thus represent important candidates for further study of the responses to copper-induced olfactory injury. Our results shed light on the evolution of vertebrate olfactory repair mechanisms and have important implications for the conservation and management of both invasive and native populations of lamprey.

Transcriptomic analysis of gonadal development in parasitic and non-parasitic lampreys (Ichthyomyzonspp.), with a comparison of genomic resources in these non-model species

“…In contrast, using a strict FDR of <0.01, 2749 genes were more highly expressed in the gonads of larvae during early differentiation compared to 2308 genes in differentiated females ( Figure 4A , Supplementary Table S7B), and 2645 vs 2842 genes were found to be significantly more highly expressed in the gonads of differentiated males versus differentiated females ( Figure 4B , Supplementary Table S7C). Similarly high numbers of DEG’s have been identified following transcriptomic analyses of gonad development in other taxa ( Piprek et al 2019 ; Biscotti et al 2020 ; Chiu et al 2020 ) and in studies of sea lamprey development and environmental tolerance ( Hockman et al 2019 ; Jones et al 2019 ).…”

“…Furthermore, in addition to being a putatively 1R taxon, the lamprey genome and other basal vertebrate lineages are thought to have undergone multiple independent chromosomal and/or region-specific duplications which would lead to lineage-specific amplification of some paralogous gene families ( Smith et al 2018 ). As a reflection of these difficulties, recent studies employing transcriptomic analyses in the sea lamprey have employed genome guided, de novo transcript assembly and discovered many genes that are not present in the current annotation ( Hockman et al 2019 ; Jones et al 2019 ). Secondly, linking specific pathways or modes of function with genes by the general descriptors provided by GO is problematic due to the incomplete annotation of the sea lamprey genome and reliance on functional annotations from well-characterised taxa, although this approach is common when working in non-model vertebrates, including lampreys ( Hockman et al 2019 ).…”

“…These genomic resources have been of great use in helping to improve our understanding of genes and gene networks that control many aspects of sea lamprey biology ( Hockman et al 2019 ; Jones et al 2019 ; Parker et al 2019 ; s ee review by York et al 2019 ). However, relatively little is known about the genes involved in lamprey reproduction.…”

Applications of Next-Generation Sequencing Technologies and Computational Tools in Molecular Evolution and Aquatic Animals Conservation Studies: A Short Review

“…Expression patterns of various genes in host aquatic species corresponding to multiple environmental stressors or inducers have been well documented. 28-32…”

“…Expression patterns of various genes in host aquatic species corresponding to multiple environmental stressors or inducers have been well documented. [28][29][30][31][32] Currently used NGS platforms include Illumina (formerly Solexa) sequencing, SOLiD system of ABI, the Polonator G.007, Helicos Heliscope, PacBio SMRT sequencing, and Oxford Nanopore. The choice of technologies depends on the throughput capacity, running time, coverage depth, simultaneous multiplexing, cost, and error rates.…”