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Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish.

ABSTRACT: In estuary and coastal systems, human demand for freshwater, climate change-driven precipitation variability, and extreme weather impact salinity levels, reducing connectivity between mesohaline coastal fish populations and potentially contributing to genomic divergence. We examined gill transcriptome responses to salinity in wild-caught juveniles from two populations of Sacramento splittail (Pogonichthys macrolepidotus), a species of conservation concern that is endemic to the San Francisco Estuary, USA, and the lower reaches of its tributaries. Recent extreme droughts have led to salinities above the tolerance limits for this species, creating a migration barrier between these populations, which potentially contributed to population divergence. We identified transcripts involved in a conserved response to salinity; however, the more salinity-tolerant San Pablo population had greater transcriptome plasticity (3.6-fold more transcripts responded than the Central Valley population) and a response consistent with gill remodeling after 168 hr of exposure to elevated salinity. The reorganization of the gill in response to changing osmotic gradients is a process critical for acclimation and would facilitate enhanced salinity tolerance. We detected an upregulation of receptors that control the Wnt (wingless-type) cell signaling pathway that may be required for an adaptive response to increases in salinity, patterns not observed in the relatively salinity-sensitive Central Valley population. We detected 62 single nucleotide polymorphisms (SNPs) in coding regions of 26 transcripts that differed between the populations. Eight transcripts that contained SNPs were associated with immune responses, highlighting the importance of diversity in immune gene sequences as a defining characteristic of genomic divergence between these populations. Our data demonstrate that these populations have divergent transcriptomic responses to salinity, which is consistent with observed physiological differences in salinity tolerance.

SUBMITTER: Jeffries KM

PROVIDER: S-EPMC6597873 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish.

Jeffries Ken M KM Connon Richard E RE Verhille Christine E CE Dabruzzi Theresa F TF Britton Monica T MT Durbin-Johnson Blythe P BP Fangue Nann A NA

Evolutionary applications 20190426 6

In estuary and coastal systems, human demand for freshwater, climate change-driven precipitation variability, and extreme weather impact salinity levels, reducing connectivity between mesohaline coastal fish populations and potentially contributing to genomic divergence. We examined gill transcriptome responses to salinity in wild-caught juveniles from two populations of Sacramento splittail (<i>Pogonichthys macrolepidotus</i>), a species of conservation concern that is endemic to the San Franci ...[more]

PMID: 31293632

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Project description:BackgroundAs ectothermic organisms have evolved to differing aquatic climates, the molecular basis of thermal adaptation is a key area of research. In this study, we tested for differential transcriptional response of ecologically divergent populations of redband trout (Oncorhynchus mykiss gairdneri) that have evolved in desert and montane climates. Each pure strain and their F1 cross were reared in a common garden environment and exposed over four weeks to diel water temperatures that were similar to those experienced in desert climates within the species' range. Gill tissues were collected from the three strains of fish (desert, montane, F1 crosses) at the peak of heat stress and tested for mRNA expression differences across the transcriptome with RNA-seq.ResultsStrong differences in transcriptomic response to heat stress were observed across strains confirming that fish from desert environments have evolved diverse mechanisms to cope with stressful environments. As expected, a large number of total transcripts (12,814) were differentially expressed in the study (FDR ≤ 0.05) with 2310 transcripts in common for all three strains, but the desert strain had a larger number of unique differentially expressed transcripts (2875) than the montane (1982) or the F1 (2355) strain. Strongly differentiated genes (>4 fold change and FDR ≤ 0.05) were particularly abundant in the desert strain (824 unique contigs) relative to the other two strains (montane = 58; F1 = 192).ConclusionsThis study demonstrated patterns of acclimation (i.e., phenotypic plasticity) within strains and evolutionary adaptation among strains in numerous genes throughout the transcriptome. Key stress response genes such as molecular chaperones (i.e., heat shock proteins) had adaptive patterns of gene expression among strains, but also a much higher number of metabolic and cellular process genes were differentially expressed in the desert strain demonstrating these biological pathways are critical for thermal adaptation to warm aquatic climates. The results of this study further elucidate the molecular basis for thermal adaptation in aquatic ecosystems and extend the potential for identifying genes that may be critical for adaptation to changing climates.

Project description:Crustaceans are generally considered more sensitive to ocean warming due to their lack of certain efficient regulators. However, the alterations in the physiology and behavior of crustaceans in response to thermal stress differ vastly even among the infraspecific populations of heterogeneous landscapes. Consequently, understanding the impact of temperature fluctuation on crustacean infraspecific populations might be essential for maintaining a sustainable persistence of populations at existing locations. In the present study, we chose the Japanese mantis shrimp (Oratosquilla oratoria) as the representative crustacean population, and conducted transcriptome analyses in two divergent O. oratoria populations (the Zhoushan and Qingdao populations) under same thermal stress (20-28 °C) to identify the population-specific expression response to thermal stress. The results showed significant differences in gene expressions, GO terms and metabolic pathways between the two populations. We hypothesized that intraspecific mutations in the same or different genes might lead to thermal adaptive divergences. Temperature increases from 20-28 °C produced significant enrichment in GO terms and altered the metabolic pathways in the Zhoushan population despite the lack of differentially expressed unigenes. Therefore, several functional genes with large pleiotropic effects may underlie the response to thermal stress in the Zhoushan population. Furthermore, the most significantly enriched biological processes of the Qingdao population were associated with the state or activity of cells and its significant enriched pathways with genetic information processing as well as immune and environmental information processing. In contrast, the differentially regulated unigenes of the Zhoushan population were primarily involved in the regulatory cellular and transcription processes and the most significant pathways found were metabolic and digestive. Consequently, the regulatory mechanisms of the Zhoushan population are probably more efficient than those of the Qingdao population under the same thermal stress.

Project description:Aerobic nitrification is a fundamental nitrogen biogeochemical process that links the oxidation of ammonia to the removal of fixed nitrogen in eutrophicated water bodies. However, in estuarine environments there is an enormous variability of water physicochemical parameters that can affect the ammonia oxidation biological process. For instance, it is known that salinity can affect nitrification performance, yet there is still a lack of information on the ammonia-oxidizing communities behavior facing daily salinity fluctuations. In this work, laboratory experiments using upstream and downstream estuarine sediments were performed to address this missing gap by comparing the effect of daily salinity fluctuations with constant salinity on the activity and diversity of ammonia-oxidizing microorganisms (AOM). Activity and composition of AOM were assessed, respectively by using nitrogen stable isotope technique and 16S rRNA gene metabarcoding analysis. Nitrification activity was negatively affected by daily salinity fluctuations in upstream sediments while no effect was observed in downstream sediments. Constant salinity regime showed clearly higher rates of nitrification in upstream sediments while a similar nitrification performance between the two salinity regimes was registered in the downstream sediments. Results also indicated that daily salinity fluctuation regime had a negative effect on both ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) community's diversity. Phylogenetically, the estuarine downstream AOM were dominated by AOA (0.92-2.09%) followed by NOB (0.99-2%), and then AOB (0.2-0.32%); whereas NOB dominated estuarine upstream sediment samples (1.4-9.5%), followed by AOA (0.27-0.51%) and AOB (0.01-0.23%). Analysis of variance identified the spatial difference between samples (downstream and upstream) as the main drivers of AOA and AOB diversity. Our study indicates that benthic AOM inhabiting different estuarine sites presented distinct plasticity toward the salinity regimes tested. These findings help to improve our understanding in the dynamics of the nitrogen cycle of estuarine systems by showing the resilience and consequently the impact of different salinity regimes on the diversity and activity of ammonia oxidizer communities.

Dataset Information

Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish.

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Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish.

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