The use of transcriptomics in situ study through fish: a systematic review on pollution

Jessica Cardenas-Camacho^1,2, Ivonne Calderón-Delgado¹, Wilson Corredor-Santamaría¹ and Yohana M. Velasco-Santamaría¹

PDF: EN    XML: EN | Cite this article

Abstract​

---

Introduction​

---

Biological and chemical pollutants from agricultural activities, industrial wastewater and other human and animal activities can cause disturbance to aquatic ecosystems, affecting water quality and leading to a reduction in freshwater supply (Zulkifli et al., 2018). These effects on water quality due to anthropogenic activities can be increased by greenhouse gases as atmospheric temperature rises, which leads to an increase in precipitation and influences the emission and transformation of pollutants in the atmospheric, terrestrial and aquatic environments (Martel et al., 2021; Priya et al., 2023), the latter being the most affected as a result of leaching, precipitation or infiltration processes, where pollutants reach groundwater and surface water (Ribeiro et al., 2022).

Some of the contaminants that have been mostly found in these systems are pesticides and other organic solvents, such as polycyclic aromatic hydrocarbons (PAHs), which through melting processes cause the accumulation of heavy metals, which have been related to the increase of cancer and metabolic diseases in humans (Jeffrey et al.,2019; McLimans et al., 2022), as well as physiological alterations in animals (Bai et al., 2022; Marcelino et al., 2022). Among the effects of these substances on fish is a decrease in growth performance, as well as alterations in the integrity of the digestive tract, and alterations in genes involved in metabolism and basic cellular functions (Hook et al., 2010; Ye et al., 2024). Other effects on fish when exposed to contaminants are directed to the expression of genes related to reproduction, the lipid and protein profile, which affects the availability of energy and substrates necessary for the normal development of the gonads (Tolussi et al., 2018; Escalante-Rojas et al., 2021).

These alterations depend on factors such as the species and class of compound; likewise, the side effects of exposure to these compounds are related to the animals’ capacity for absorption, exposure or metabolization of these compounds (Mackay, Fraser, 2000; Wang et al., 2005; Jamil Emon et al., 2023). However, it has been determined that xenobiotics are detrimental to a wide variety of species, primarily those inhabiting aquatic ecosystems, which tend to be the first to show signs of instability due to the increasing pollutant load to which they are exposed, causing additional pressure to that already included by climate change (Priya et al., 2023; Bolan et al.,2024; Selle et al., 2024).

Among the aquatic organisms that tend to bioaccumulate these toxic pollutants are fish, which can absorb metals such as mercury, polychlorinated biphenyls (PCBs), polybrominated biphenyl ethers (PBDEs), dioxins and chlorinated pesticides from the surrounding water, sediments and their prey (Tata et al., 2023; Vreedzaam et al., 2023; Selle et al.,2024; Srisiri et al., 2024). This is even more likely for fish species that inhabit contaminated areas, especially those living on the bottom, where higher levels of these chemicals are likely to be present as they settle to the bottom of water bodies (EPA, 2013). For more than two decades, different multidisciplinary approaches have been developed and discussed for the investigation of contaminant exposure scenarios in surface waters, including the incorporation of geographic information, hydrobiological data, contaminant chemistry, fish biology and the integration of genomic, proteomic and transcriptomic data (Andersen et al.,2015; Olsvik et al., 2021; Laurent et al.,2023), which has allowed the discovery of biomarkers in fish that could be used for the monitoring of aquatic contamination (Mitra et al., 2020a). Some genes/proteins that have shown potential as markers of contamination have been cyp1a, cat, hsp, gst, vtg-a and p53 (Tolussi et al., 2018; Piazza et al.,2019; Bertel-Sevilla et al.,2020).

Aquatic ecosystems are complex and can receive different contaminants, therefore studies have moved from the analysis of selected molecules to high throughput analysis such as transcriptome analysis, which from next-generation sequencing (NGS) (Lowe et al., 2017), is not limited to predefined genes and that added to the development of de novo assembly tools by RNA-seq has become an even more powerful platform to characterize the transcriptome of a non-model organism. Generally, these organisms are the most used in situ studies, since being native species, they are a better option to globally understand the behaviour of populations and thus determine the state of health of the ecosystem (Martin et al.,2016; Zhou et al., 2018).

In these natural environments, organisms are exposed to complex mixtures of chemical compounds and the fluctuation of other stressors such as temperature, pH, dissolved solids, among others (Choi et al.,2021), which activate specific metabolic pathways that can reveal both immediate toxic effects and long-term adaptive responses, making it possible to identify early markers of environmental damage and stress, allowing to understand the adaptation of populations to these environments or to determine the alterations in their metabolism and therefore in the regulation of genes essential for their survival (Cardenas Perez et al.,2024).

On the other hand, when studies are conducted to determine the effects of pollutants on these organisms, they are mostly conducted in the laboratory, which is an important starting point with a controlled environment that offers the conditions to isolate the effects of individual pollutants (Uren Webster, Santos, 2015; Qiu et al., 2019; Corredor-Santamaría et al., 2023). However, in situ assessment can more realistically reflect the complexity of exposure scenarios in ecosystems (Beale et al.,2017; Velasco-Santamaría et al., 2019; Fé-Gonçalves et al.,2020). Transcriptomic analyses performed directly on fish populations have the potential to detect interactions between multiple stressors, demonstrating responses that may not be perceived in artificial environments (Piazza et al.,2019). Therefore, understanding the importance of these tools as an approach to evaluate the in situ response, and thus provide a broader and more holistic picture of the effects induced by pollution, the objective of this systematic review is to determine the approaches carried out in the field of transcriptomics using fish as bioindicators and focusing the analysis on 1) The biogeographic areas where the studies have been carried out, 2) The species used in these studies, 3) The type of potential pollutant to be evaluated, 4) Health in wild species 5) The biological processes detected from the transcriptome and 6) Access to the raw data used in these studies.

Material and methods

---

A search was conducted for articles related to transcriptomic studies in the field using native fish species as indicators of contamination. In the first instance, the following databases were selected: Scopus, ScienceDirect, SpringerLink, Web of Science, Scielo and PubMed. The keywords used were fishes, transcriptomic, transcriptome, RNA-sequencing, expression profile, pollution, contamination, xenobiotic, and toxicology. In the first refinement, only articles between 2014–2025 were included and as exclusion criteria those documents related to theses, conference abstracts, book chapters, books, review articles and reports. Subsequently, the PRISMA 2020 methodology was used to screen the papers. The first step was to discard duplicate articles in the databases. We excluded articles that were from studies in other taxa, not performed in situ, studies that were not performed in biological organisms, that did not include transcriptomic studies by RNA-seq and that were not contamination studies (Fig. 1).

FIGURE 1| Screening workflow for selection of articles for analysis.

Results​

---

From the screening of articles that arose from the search for articles related to transcriptomic studies in fish to evaluate in situ contamination, a total of 32 studies were found, which will be presented in relation to the issues raised in this review article.

Biogeographic study areas. Fig. 2 shows that most of the studies have been implemented in watersheds in Europe, Asia and North America, the latter being the subcontinent where the largest number of studies have been carried out concerning the species. On the other hand, in South America, studies have been carried out in two countries, Colombia and Chile, while in the African continent, there are no studies reported at the time of this review.

When relating the type of environment to which these species were exposed, it is important to differentiate the aquatic ecosystems in terms of salinity since this can modify the bioavailability, toxicity and route of exposure. Among the studies reviewed, five classifications were found: freshwater; freshwater and brackish; brackish water; marine; marine and brackish water; the brackish water classification is given to the interaction of freshwater and marine. The studies were conducted mainly in freshwater environments (n = 19), followed by marine (n = 5), freshwater and brackish (n = 4), brackish (n = 3) and with only one study in marine and brackish water environments.

Fish species and pollutant compounds in situ transcriptomics studies. In this impulse to use transcriptomics as a tool for monitoring in situ contamination using fish as bioindicators, it was found that most of these species are distributed in Europe, Asia and North America as mentioned above (Bánki et al.,2024), presenting greater support for research related to wild species to have a better understanding of natural systems (Fig. 2; Tab. 1). Additionally, and taking into account the objective of this systematic review by focusing on the compounds studied by transcriptomic profiling, we found a great variety of compounds ranging from metal contamination, wastewater, agricultural compounds, industrial compounds, organic compounds and other compounds derived from anthropogenic pressure (Tab. 1).

FIGURE 2| Countries where in situ transcriptomics studies have been performed in fish to assess environmental contamination. See Tab. 1 for species names.

TABLE 1 | Fish species used in situ contamination studies.

Species	Subject	Area of distribution	Environments	References
Ameiurus nebulosus (Lesueur, 1819)	North America	Brackish and freshwater	Contaminants of Emerging Concern (CECs) and legacy contaminants	Hahn et al. (2016)
Anabas testudineus (Bloch, 1792)	Asia	Brackish and freshwater	Heavy metals and e-waste	Zhang et al. (2019)
Anguilla anguilla (Linnaeus, 1758)	Atlantic Ocean	Brackish, freshwater and marine	Metallic and organic compounds	Baillon et al. (2015)
Anguilla rostrata (Lesueur, 1817)	From northwest to west-central Atlantic	Brackish, freshwater and marine	Metallic and organic compounds	Baillon et al. (2015)
Basilichthys microlepidotus (Jenyns, 1841)	South America	Freshwater	Chronic pollution	Cortés-Miranda et al. (2024a,b); Vega-Retter et al. (2018)
Brosme brosme (Ascanius, 1772)	Northwest and northeast Atlantic	Marine	Mercury (Hg)	Olsvik et al. (2021)
Catostomus commersonii (Lacepède, 1803)	North America	Brackish and freshwater	Contaminants of Emerging Concern (CECs) and legacy contaminants	Hahn et al. (2016)
Gadus morhua Linnaeus, 1758	North Atlantic and Arctic	Brackish and marine	Wastewater, wastes	Khan et al. (2020); Magnuson et al. (2024)
Hemiculter leucisculus (Basilewsky, 1855)	Asia	Brackish and freshwater	Phenolic compounds	Guo et al. (2021)
Siniichthys lucidus (Dybowski, 1872) (synonym Hemiculter lucidus)	Asia	Freshwater	Phenolic compounds	Guo et al. (2020)
Hypophthalmichthys molitrix (Valenciennes, 1844)	Asia	Freshwater	Harmful substances	Jeffrey et al. (2019)
Lates calcarifer (Bloch, 1790)	Indo-West Pacific	Brackish, freshwater and marine	Pesticides and compounds in agricultural soil	Hook et al. (2018, 2017a,b)
Limanda limanda (Linnaeus, 1758)	Northeast Atlantic	Marine	Anthropogenic pressure	Sepp et al. (2024)
Micropterus dolomieu Lacepède, 1802	North America	Freshwater	Mercury (Hg), contaminants of emerging concern (CECs) and legacy contaminants	Hahn et al. (2016); Blazer et al. (2023)
Micropterus salmoides (Lacepède, 1802)	North America	Freshwater	Contaminants of Emerging Concern (CECs) and legacy contaminants	Hahn et al. (2016)
Mugil incilis Hancock, 1830	West Atlantic	Brackish and marine	Industrial activity compounds	Bertel-Sevilla et al. (2020)
Oreochromis niloticus (Linnaeus, 1758)	Africa	Brackish and freshwater	Anthropogenic activity compounds	Kumar Behera et al. (2024)
Perca flavescens (Mitchill, 1814)	North America	Brackish and freshwater	Compounds from municipal fluids and agricultural activities	Defo et al. (2018); Lacaze et al. (2019)
Perca fluviatilis Linnaeus, 1758	Europe and Asia	Brackish and freshwater	Brominated dioxins, dioxin-like compounds, and radiation	Förlin et al. (2019); Lerebours et al. (2020)
Platichthys flesus (Linnaeus, 1758)	East Atlantic and Asia	Brackish, freshwater and marine	Anthropogenic pressure, nitrite, nitrate, organic pollutants	Laurent et al. (2023); Sepp et al. (2024)
Pseudopleuronectes americanus (Walbaum, 1792)	West Atlantic	Marine	Urbanization compounds and wastewater inputs	McElroy et al. (2015)
Pungitius pungitius (Linnaeus, 1758)	Circumarctic and Eurasia	Brackish and freshwater	Organic compounds	Jordan-Ward et al. (2024)
Rhinichthys cataractae (Valenciennes, 1842)	North America	Freshwater	Wastewater treatment plants	Lazaro-Côté et al. (2021)
Rita rita (Hamilton, 1822)	Asia	Brackish and freshwater	Poor water	Mitra et al. (2020)
Rutilus rutilus (Linnaeus, 1758)	Europe and Asia	Brackish and freshwater	Estrogenic substances from sewage treatment plants	Hamilton et al. (2020)
Salmo salar Linnaeus, 1758	North Atlantic Ocean	Brackish, freshwater and marine	Organohalogen compounds	Kanerva et al. (2020)
Salmo trutta fario Linnaeus, 1758	Europe and Asia	Brackish, freshwater and marine	Compounds in wastewater and diffuse agricultural runoff	Schmitz et al. (2022)
Salvelinus fontinalis (Mitchill, 1814)	North America	Brackish, freshwater and marine	Compounds from fracking	McLimans et al. (2022)

Biological processes from transcriptome. We obtained 38 genes that were divided into several groups, but which also participate in several pathways as shown in Fig. 3. They were grouped into 11 groups or metabolic pathways, which are: oxidative stress response and antioxidant defence with six genes that were detected in eight papers, lipid and cholesterol metabolism with nine genes found in 11 papers, hormonal and reproductive signalling with six genes in 10 papers, DNA repair and cell cycle with four genes in five papers, immunity and inflammatory response with four genes concerning nine papers, xenobiotic metabolism and detoxification with five genes observed in eithg papers, cell signalling with four genes in six papers, apoptosis and programmed cell death with two genes in three papers, energy production and cell metabolism with two genes found in five papers, hepatic and liver-related processes with four genes with respect to five papers, and circadian factors with one gene in two papers.

FIGURE 3| Common pathways and genes differentially expressed under contamination conditions in situ studies by transcriptional profiling in fish.

Data access. Both studies that covered contamination and those that did not were taken into account, determining the percentage of data access for the 32 papers reviewed (Fig. 4). We found that only 34.3% of them had some kind of accessibility to the data, of which 81.8% were deposited in SRA (Sequence Read Archive), that is, the NCBI database where sequencing data are stored, and which allows other researchers to know them, evaluate them and use them as a basis for other research (Wang et al.,2009). Another category within this percentage was the contings with 9.1%, which allow them to be annotated to identify genes or isoforms present in the sample, and finally, there are the scaffolds (9.1%), which are larger formed by joined contings and can have a better reconstruction of the transcriptome; however, they may have unresolved areas (gaps) due to lack of coverage (Conesa et al., 2016). On the other hand, and with a much higher percentage, we have studies that do not provide any information (59.4%) and studies from which access to data can be requested with 6.3%.

FIGURE 4| Access to data in situ transcriptomic studies in fish.

Discussion​

---

Biogeographic study areas. In situ studies with fish whose transcriptional profile has been analyzed are mostly native wild species, providing a more complete picture since it provides more accurate, relevant and adapted data to local conditions where multiple factors may influence the response of a species, unlike laboratory studies that evaluate few variables at the same time (Piazza et al.,2019). This complexity allows for a better understanding of the ecological processes in the system and the metabolic processes of the species that inhabit these environments. However, studies of this nature, i.e., in situ transcriptomics in fish to assess the health of a water ecosystem and therefore of the organisms, have been developed in specific locations around the world as shown in Fig. 2.

Studies focused on in situ transcriptomics to assess contamination focus on fish species from the European and Asian continents, while there are few studies in South America and especially the lack of information from the African continent, where a diversity of fish species can be found about the other continents (Pelayo-Villamil et al., 2015; GBIF, 2024). This can give us a perspective of the efforts that have been made in species that are native, but at the same time in species with aquaculture potential (Hahn et al., 2016; Defo et al., 2018; Hook et al., 2017a,b, 2018; Jeffrey et al., 2019; Lacaze et al., 2019; Zhang et al., 2019; Kanerva et al., 2020; McLimans et al., 2022; Schmitz et al., 2022; Blazer et al., 2023; Kumar Behera et al., 2024), this is reflected in the number of species, out of 28 fish species found to have been studied in the world with a transcriptomic approach to in situ anthropogenic disturbance conditions.

This limitation of the studies may be due to several challenges; some of these may be the complex environmental conditions and sampling in a natural environment where multiple stress factors may be present for the individuals, as well as the preservation conditions of the RNA samples as they have a high degree of degradation if they are not kept in the right conditions (Vehniäinen et al., 2019). Cost and resources are also limiting factors, because in some developing countries, environmental studies are not given the same priority as medical or agricultural research, and the cost of sequencing, which has been reduced over the years, remains unaffordable due to advanced equipment, computational analysis, and extensive databases (Helmy et al., 2016). There is also the limitation in data interpretation, focusing on the lack of reference genomes and biological variability, which makes it difficult to interpret transcriptomic data that may vary among individuals due to genetic factors, age, sex and physiological status (Matheson, McGaughran, 2022; Theissinger et al.,2023; Calcino et al.,2024). Another point is the multidisciplinary approach by combining ecotoxicology, bioinformatics, molecular biology and ecology, which may not be well developed in studies, and above all the tradition of techniques, where more traditional biomarkers (enzymatic biomarkers, acute toxicity, histopathological, among others) have been prioritized due to their easy implementation and lower cost about advanced genomic tools (Corredor-Santamaría et al., 2016, 2019; Velasco-Santamaría et al., 2024). However, if these sequencing technologies become more widely available and genetic databases are developed for more species, likely, the number of studies aimed at implementing transcriptomic technologies for in situ assessment will increase. This opens the door to identifying molecular mechanisms underlying environmental stress, allowing the development of tools with high degrees of precision for biomonitoring from indicator species such as fish.

Fish species and pollutant compounds in situ transcriptomics studies. From this systematic review we detected different types of contaminants that have been evaluated from transcriptomic analysis in fish, although most of the papers, being conducted in situ, address more than one contaminant, our main focuses were heavy metals, organic contaminants, endocrine disruptors, agricultural and urban contaminants, radiation, other contaminants of interest and finally health in wild species.

Heavy metals.Three studies were found in which trancriptomic analysis was related to heavy metals; these studies focused on four fish species. In situ ecotoxicological studies have demonstrated the negative effects of mercury (Hg), cadmium (Cd) and arsenic (As) on wild fish populations, including alterations at the molecular and genetic level in species such as Brosme brosme (Ascanius, 1772), Micropterus dolomieu Lacepède, 1802, Anguilla rostrata (Lesueur, 1817) and Anguilla anguilla (Linnaeus, 1758); although the habitats differ among these species, there are common pathways affected in the liver (Baillon et al., 2015; Olsvik et al., 2021; Blazer et al., 2023). For example, in B. brosme and M. dolomieu alterations in protein folding pathways were observed, which is presented as a response to oxidative stress, and in both species of Anguilla spp., where exposure to arsenic and cadmium involved oxidative stress genes and energy metabolism as cellular homeostasis was affected.

Furthermore, other altered pathways are lipid metabolism and immune response and apoptosis in B. brosme and Anguilla spp., suggesting that metals may affect lipid mobilization and storage, which could have consequences on growth and thus reproduction, as well as the ability to respond to infections (Baillon et al., 2015; Olsvik et al.,2021). This suggests that transcriptomic signatures may provide specificity for characterizing different contaminants by identifying mechanisms of toxicity when fish are exposed to multiple stressors.

Organic pollutants.These chemicals can come from natural or anthropogenic sources and cover a broad spectrum of compounds. With this approach, seven studies were grouped in which the transcriptome of seven species was studied in response to exposure to pollutants such as electronic residues, phenolic compounds and persistent pollutants. Different patterns of transcriptomic response were identified, and in all studies alterations in genes involved in oxidative stress and cell damage were observed (Förlin et al.,2019; Zhang et al., 2019; Guo et al., 2020a, 2021; Mitra et al., 2020; Schmitz et al., 2022; Jordan-Ward et al., 2024); for example, in Rita rita (Hamilton, 1822), genes such as hsp70, cox7a2 and cox17 showed differential expression to contamination in natural rivers, which are genes associated with heat stress response, detoxification and energy metabolism (Mitra et al.,2020). Likewise, there is an increase in the endoplasmic reticulum response in Anabas testudineus (Bloch, 1792) when exposed to heavy metals and electronic waste (Zhang et al., 2019).

Another altered pathway is the one involved in reproductive development, as was found in Salmo trutta fario Linnaeus, 1758 with differential regulation of genes involved in steroid biosynthesis (e.g., hsd3b and hsd17b1) or the suppression of gonadal development upon exposure to persistent organic pollutants (POPs, PCBs) in Pungitius pungitius (Linnaeus, 1758) species collected from Arctic areas, which may have effects on growth and reproduction by altering genes associated with hormone regulation and lipid metabolism (Schmitz et al., 2022; Jordan-Ward et al., 2024). Alterations in hepatic metabolism and cellular function were also found, with alterations in the expression of lipid and protein metabolism genes, as in the species Siniichthys lucidus (= H. lucidus)(Dybowski, 1872) exposed to Bisphenol A (BPA), nonylphenol (NP) (Guo et al.,2020) or in the synthesis and transport of cholesterol, and also in the accumulation of lipids and hepatic dysfunction in fish exposed to industrial pollutants such as PCBs (Schmitz et al., 2022;Jordan-Ward et al., 2024).

Finally, papers report gene regulation gene regulation of the innate immune response, such as lyzozyme G and activation of leukocyte migration pathways and inflammatory processes when fish species are exposed to phenolic compounds (Mitra et al., 2020; Schmitz et al., 2022); for example, differences are reported in the exposure of the immune response such as oxidative stress in Perca fluviatilis Linnaeus, 1758 in the Baltic Sea, which may be due to exposure to natural brominated compounds and anthropogenic pollutants (Förlin et al., 2019).

Endocrine disruptors.In this category there were two papers focused on endocrine disruptors, in each study a fish species was analyzed. Exposure to endocrine disruptors can alter reproductive capacity in fish, as was found with the alteration of estrogen-responsive genes such as vitellogenin (vtg) and zona pellucida glycoprotein (zp3a); as well as alteration in steroid hormone metabolism (ar), oxidative stress and detoxification pathways (hsp70, cyp1a, AhR) (Hamilton et al.,2020; McLimans et al., 2022).However, we also found possible genetic adaptations in populations exposed to long-term exposure, as in Salvelinus fontinalis (Mitchill, 1814) where the key gene cyp1a involved in the response to xenobiotics showed a negative regulation in sites with fracking activity (McLimans et al., 2022); which may be due to this adaptation or also to a chronic exposure that may lead to a negative feedback by reducing cyp1a expression, decrease in liver responsiveness, effects of environmental hypoxia or induction of other detoxification pathways.

Agricultural and urban pollutants.This group presents a broad spectrum of contaminants and therefore of great interest, which is reflected in the number of papers that we placed in this category, which were 11 papers, but interestingly has a lower number of species with only six.

Therefore, it was discussed in relation to the species, for example in Lates calcarifer (Bloch, 1790) which was exposed to contamination by pesticides and other urban pollutants in rivers in Australia, presented an interesting pattern such as activation of detoxification pathways; alterations in lipid and hepatic metabolism; effects on immune response, with inflammatory activation and immunosuppression; cellular stress and apostosis induced by exposure to pesticides and urban pollutants (Hook et al.,2017a,b, 2018).

However, what is interesting is that differences are shown in response to the type of contaminant, duration of exposure and environmental variability, as in oxidative stress and xenobiotic metabolism, where genes such as CYP1A, GST and AhR are overexpressed in response to pesticides (Hook et al., 2018), while in another study these genes were repressed by chronic exposure (Hook et al., 2017b). With exposure to agricultural pesticides, genes related to lipid metabolism (FABP, SCD, PPARα) were found to be overexpressed (Hook et al., 2017b), whereas these same genes in another study were found to be downregulated (Hook et al.,2018). It was also found that when exposed to agricultural pollutants there is a suppression of immune genes (MHC-I, IL-1β), while in the other case there was an activation of the immune response (TNF-α). A possible explanation for these variations may be that an initial exposure may produce the activation of the metabolic pathway, however, a prolonged exposure may induce a suppression of these metabolic pathways.

Different patterns were identified in Basilichthys microlepidotus (Jenyns, 1841) in the Maipo River basin (Chile) when exposed to contamination related to domestic and agricultural activities (Vega-Retter et al., 2018; Cortés-Miranda et al., 2024a,b). Their approach was based on molecular mechanisms of dense or damage such as detoxification, proliferation/apoptosis and immunity, where contamination is considered as a chronic selective factor and not only as an acute stress. For example, not all CYP genes are convenient bioindicators, considering that most of them are repressed, if their functions and location (tissue) are not considered (Cortés-Miranda et al., 2024a), highlighting that genes associated with exogenous compounds are differentially expressed in gills, which are linked to the immune response, while genes related to endogenous compounds are differentially expressed in the liver and are related to cell mitosis, organic compounds and carcinogenic processes; as well as genes of the chemical defensome show consistent repression in contaminated populations in liver tissue (Cortés-Miranda et al., 2024b). Likewise, these populations in their natural environment evidenced a combination of gene expression and genetic adaptation when exposed to contaminants, finding key genes such as odc (ornithine decarboxylase) that independently of the contamination load of two sites were overexpressed (Vega-Retter et al., 2018).

Among these pollutants of agricultural and urban origin, we have also studied Gadus morhua Linnaeus, 1758, associating antioxidant and detoxification genes with overexpression upon exposure to urban pollutants, while in agricultural sites, these same genes are negatively regulated; this same pattern is repeated with lipid metabolism and storage genes (FABP, PPARα), which may occur because urban pollutants can induce higher energy metabolism to compensate for oxidative stress, while pesticides can alter lipid homeostasis, causing accumulation in the liver. Disruption in neuroendocrine pathways was also found in urban sites, while alteration in reproductive and ovarian development genes (esr2 and cyp19a) occurs upon exposure to agricultural pollution (Khan et al.,2020; Magnuson et al., 2024).

In the same way as the previous studies, the response in other species a similar pattern was found in terms of alterations in metabolic pathways, with an increase in the expression of genes associated with lipid metabolism, suppression of the immune response and alteration in the metabolism of xenobiotics and an activation of PPARα and AhR receptors, affecting reproductive functions when the type of contamination is from urban sources (Lacaze et al.,2019; Lazaro-Côté et al.,2021). While exposure to agricultural pollutants causes the activation of antoxidant metabolism, regulation of the immune response, activating phagocytosis genes and inflammatory processes and altered expression of energy metabolism (McElroy et al., 2015; Lacaze et al., 2019).

Radiation.The transcriptome of female gonads of P. fluviatilis from lakes located inside and outside the Chernobyl exclusion zone was evaluated in situ (Lerebours et al., 2020), this study was the only one found for this category. Common genes involved in lipid metabolism, development, reproduction, cytoskeleton, cell proliferation and differentiation, DNA damage repair and epigenetic mechanisms were identified. The most relevant genes ska1, cp2g1, hus1, gthb1, star reference gene actb were validated by q-PCR. When comparing the PCR technique and differential expression results by NGS between three categories (category 1: Undeveloped/Irradiated, category 2: Developed/Irradiated and category 3: Developed/Reference), the ska1 and cp2g1 genes were only significant between category 1 about category 2 and 3 by q-PCR. On the other hand, the gthb1 and star genes were underexpressed in all conditions, except for category 2 compared to category 3, which showed no significant differences. Finally, the hus1 gene was overexpressed in categories 1 and 2 compared to category 3. These results demonstrate that the use of omics tools such as transcriptomics is a step towards a complete understanding of the complexity of radiation in fish in natural ecosystems.

Other pollutants of interest.Among the pollutants called “diverse” for this review, two studies are presented, where the transcriptional profile of three species was analyzed. It was found that oncogenic substances in natural habitats can cause negative impacts generating environmental changes. As a consequence, the interest in studying the defence mechanism against cancer in contaminated habitats through ictic species has become more relevant. For example, in the study of the hepatic transcriptome in Platichthys flesus (Linnaeus, 1758) and Limanda limanda (Linnaeus, 1758) (Sepp et al.,2024), contaminated and reference zones were compared, revealing that the species P. flesus has a lower prevalence of cancer induced by contamination compared to L. limanda, suggesting that P. flesus could possess more robust genomic mechanisms that would allow a better adaptation to these contaminated environments.

Another approach is the study of the origin of Salmo salar Linnaeus, 1758 (wild or captive-bred) and the levels of organohalogen contaminants to determine the influence on the hepatic transcriptomic profile, showing that captive-bred salmon tend to accumulate slightly higher levels of contaminants. However, the transcriptional differences were smaller between these groups, which may be due, according to the authors, to the fact that the shared marine environment during food migration and the levels of contamination have a greater impact than the origins of the individuals (Kanerva et al., 2020).

Wild species health. One of the key points of molecular studies is to identify how the health of wild fish species is being affected by anthropogenic actions, delving into the pathways and genes involved. We used this category because some studies seek to monitor the species, and not to identify contamination at the site based on the study of the species. Six articles were reviewed here in which the transcriptome of nine species was analyzed.

A strong activation of genes related to the response to oxidative stress and detoxification was found in the overexpression of the cytochrome P450 system (CYP1A, AhR, GST) in species such as P. flesus and Perca flavescens (Mitchill, 1814)(Defo et al.,2018; Laurent et al., 2023); increase in heat shock proteins (hsp70, hsp90) in fish from the contaminated Ganges River or inhibition of antioxidant enzymes (CAT, SOD, GST) when exposed to heavy metals and organic pollutants (Defo et al.,2018; Kumar Behera et al., 2024). Another essential metabolic pathway affected was that of energy and liver metabolism, in this case there is a decrease in lipid and cholesterol metabolism genes when exposed to suboptimal water quality as presented in Hypophthalmichthys molitrix (Valenciennes, 1844), which suggests impacts on the capacity to store and use energy (Jeffrey et al., 2019); deregulation in urea cycle genes when exposed to agricultural pollution, due to increased nitrogen (Laurent et al., 2023) and alteration in the metabolism of amino acids and ribosomal proteins in response to hypoxia and pollution, as occurred in Oreochromis niloticus (Linnaeus, 1758)species(Kumar Behera et al.,2024).

A decrease in genes associated with steroid hormone synthesis was also observed in fish populations of the San Lorenzo River in Brazil when exposed to industrial waste (Defo et al., 2018); impact on fertility and viability of populations determined by differential expression in gonads and alteration of thyroid regulatory pathways, which affects growth in Mugil incilis Hancock, 1830 fish in the Colombian Caribbean (Bertel-Sevilla et al.,2020). Other changes that are presented are in the genetic adaptation in chronically exposed fish with changes in SNPs of metabolic genes as presented in the species M. dolomieu, Catostomus commersonii (Lacepède, 1803), Micropterus salmoides (Lacepède, 1802)and Ameiurus nebulosus (Lesueur, 1819) or in degraded environments where the regulation of inflammation and apoptosis genes and the activation of response genes to contamination by hydrocarbons and metals are affected (Hahn et al., 2016; Bertel-Sevilla et al.,2020).

Biological processes from transcriptome. As presented in this review, several fish species have been used in transcriptomic studies to evaluate various contaminants in situ. From the information reported, it was determined that many of the differentially expressed genes were commonly addressed among the articles, obtaining 38 genes that were divided into several groups, but that also participated in several pathways as shown in Fig. 3. This is interesting because in most cases a single gene is not transcribed for the formation of a protein but rather it is a battery of genes that interact to provide an effective response to a need required by the cell and therefore in the organism.

In the first group, we have stress response genes and antioxidants such as CAT and GP that act to degrade hydrogen peroxide into harmless products avoiding the formation and accumulation of hydroxyl radicals. In turn, SOD performs an earlier step by eliminating the superoxide bond to turn it into hydrogen peroxide; these genes work together to protect the cell against oxidative damage to lipids, proteins, DNA and other components (Hook et al.,2017a, 2018; Bertel-Sevilla et al., 2020). A second group is lipid and cholesterol metabolism, which groups a larger number of genes involved such as PPARγ, which regulates the expression of genes related to reverse cholesterol transport; PPARα, as a nuclear transcription factor that regulates the expression of genes that function in fatty acid oxidation and lipid metabolism; soat1, which has as its main function the decoding of the enzyme acyl-CoA; cholesterol acyltransferase (ACAT1) to form cholesterol esters; and ApoE, which is involved in cholesterol recycling by reverse transport to the liver for excretion (Hook et al., 2017a; Guo et al., 2020; Lazaro-Côté et al., 2021; Jordan-Ward et al., 2024).

Another key pathway was hormonal and reproductive signalling with genes such as vtg, which promotes the formation of yolk precursor glycoprotein, which is produced in the liver in response to estrogen; 17βhd, which encodes an enzyme that regulates the activation or inactivation of sex steroids (estrogens and androgens); Erα, nuclear-estrogen-binding receptor that regulates the development, reproduction and maintenance of hormone-sensitive tissues (Hahn et al., 2016; Olsvik et al.,2021; Blazer et al., 2023).

A fourth group was DNA repair and cell cycle, with GADD45 genes involved in encoding DNA repair proteins by interacting with proteins encoded by the PCNA gene, which coordinates DNA repair during replication, and ATM, which encodes a key protein kinase in DNA damage signalling and, in turn, phosphorylates and activates key repair proteins such as p53, BRCA1 and CHK2 (Zhang et al., 2019; Bertel-Sevilla et al.,2020). The next group was that of immunity and inflammatory response with genes that respond to stress and protect the cell, such as WAP65 that is activated to reduce iron availability for pathogens, while the C3 gene mediates inflammation and opsonization by participating in the elimination of invading pathogens, through lectins that recognize microbial patterns and amplify the immune response; and lastly, NFIL3 that regulates the expression of genes involved with immune cells and cytokine secretion by adjusting the inflammatory response (Hahn et al., 2016; Olsvik et al., 2021; Blazer et al., 2023).

Among these pathways of importance we find that of xenobiotic metabolism and detoxification with the cytochrome P450 family involving CYP1A genes for the metabolism of PAHs and dioxins, CYP3A which is involved in the metabolism of drugs and other xenobiotics, CYP2K which participates in detoxification in aquatic environments, GST which through conjugation neutralizes reactive metabolism and ARH which is a regulator of detoxification genes (Hook et al., 2017a; Lacaze et al., 2019; Hamilton et al., 2020; Cortés-Miranda et al.,2024a). Some genes that share pathways include p53, a key gene in the response to DNA damage and related to oxidative stress, which is overexpressed in fish exposed to combined stress and is also related to the apoptosis and programmed cell death pathway as well as Casp3 which is activated to degrade essential proteins in the cell such as PARP, which is attributed to the functional and structural collapse of the cell (Bertel-Sevilla et al., 2020; Khan et al., 2020).

A ninth group or pathway was that of energy production and cellular metabolism with the cox1 gene coding for one of the subunits of cytochrome c oxidase as part of the electron transport chain in the mitochondria, while CYP27 codes for the enzyme involved mainly in the metabolism of lipids such as bile acids and cholesterol (Baillon et al., 2015; Jeffrey et al., 2019). An interesting group to address was that of hepatic processes, in which the hmgcs1 and soat1 genes have direct implications in the synthesis and storage of cholesterol and lipids, and FABP in the transport of fatty acids to understand the need for these processes (Hook et al.,2018; Lazaro-Côté et al., 2021). Finally, we have the circadian factors with the NFIL3 gene, which participates in the regulation of the expression of genes such as PER1/2 and Cry1, being part of the transcriptional-receptor loop of the circadian system by interacting with the molecular clock (Defo et al.,2018; Jeffrey et al., 2019).

Data access. Additionally, we explored the accessibility of transcriptomic data, i.e., the accessibility of raw counts and sequences or scaffolds in a database, as this allows other researchers to work with the same data and make comparisons with their studies. Of which we found that less than 35% are reported in the studies according to our review. These results indicate that although research associated with these areas is being conducted, if it is not accessible to all interested researchers, we return to the problem of limited data interpretation, which leads to a backlog of research, especially in developing countries, with major challenges in environmental risk assessment.

Transcriptional profiling analysis is a valuable tool to identify pathways and genes that are involved in some pollutant stress situation and that may have additional pressure on fish and their natural environment. From this review we found that although few studies have this transcriptomic approach, most of them are related to pollution from agriculture and wastewater derived from urban areas. Variations between pathways and genes that may be expressed in the organs are also evident, especially when a comparison is made between the liver, gills and ovaries, which have been the three target organs of study found in this review. On the other hand, we found 38 genes that are shared at least between two studies and most of them are involved in the lipid metabolism pathway, before oxidative stress and xenobiotic metabolism, which would have a greater relevance when analyzing the transcriptome for contamination. Finally, something important to highlight is that the species used in these studies are mostly from Asia, Europe and North America, which poses an information gap in other places such as Africa and South America with only two species studied, despite the diversity of species reported in these places. These findings allow us to establish that the analysis of transcriptional profiles is a tool that is becoming increasingly relevant, but it is important to join efforts in areas where research is scarce and which have the potential for new discoveries.

Acknowledgments​

---

To the Fundación Universitaria de San Gil, Universidad de los Llanos, and ABC Colombia Somos Territorio, executors of the project financed by the Sistema General de Regalías (SGR): “Strengthening of the information systems of the quality and valuation of the environmental services of water in order to contribute to the sustainable development of the agroindustrial sector of the department of Casanare. Yopal, Nunchía – BPIN 2020000100435”.

References​

---

Andersen Ø, Frantzen M, Rosland M, Timmerhaus G, Skugor A, Krasnov A. Effects of crude oil exposure and elevated temperature on the liver transcriptome of polar cod (Boreogadus saida). Aquat Toxicol. 2015; 165:9–18. https://doi.org/10.1016/j.aquatox.2015.04.023

Bai X, Jiang Y, Jiang Z, Zhu L, Feng J. Nutrient potentiate the responses of plankton community structure and metabolites to cadmium: a microcosm study. J Hazard Mater. 2022; 430:128506. https://doi.org/10.1016/j.jhazmat.2022.128506

Baillon L, Pierron F, Coudret R, Normendeau E, Caron A, Peluhet L et al. Transcriptome profile analysis reveals specific signatures of pollutants in Atlantic eels. Ecotoxicology. 2015; 24(1):71–84. https://doi.org/10.1007/s10646-014-1356-x

Bánki O, Roskov Y, Döring M, Ower G, Hernández Robles DR, Plata Corredor CA et al.Catalogue of Life Checklist. Catalogue of Life, Amsterdam, Netherlands; 2024. https://doi.org/10.48580/dg6lk

Beale DJ, Crosswell J, Karpe AV, Ahmed W, Williams M, Morrison PD et al. A multi-omics based ecological analysis of coastal marine sediments from Gladstone, in Australia’s Central Queensland, and Heron Island, a nearby fringing platform reef. Sci Total Environ. 2017; 609:842–53. https://doi.org/10.1016/j.scitotenv.2017.07.184

Bertel-Sevilla A, Alzate JF, Olivero-Verbel J. De novo assembly and characterization of the liver transcriptome of Mugil incilis (lisa) using next generation sequencing. Sci Rep. 2020; 10(1):13957. https://doi.org/10.1038/s41598-020-70902-5

Blazer VS, Walsh HL, Sperry AJ, Raines B, Willacker JJ, Eagles-Smith CA. A multi-level assessment of biological effects associated with mercury concentrations in smallmouth bass, Micropterus dolomieu. Environ Pollut. 2023; 329:121688. https://doi.org/10.1016/j.envpol.2023.121688

Bolan S, Padhye LP, Jasemizad T, Govarthanan M, Karmegam N, Wijesekara H et al. Impacts of climate change on the fate of contaminants through extreme weather events. Sci Total Environ. 2024; 909:168388. https://doi.org/10.1016/j.scitotenv.2023.168388

Calcino A, Cooke I, Cowman P, Higgie M, Massault C, Schmitz U et al.Harnessing genomic technologies for one health solutions in the tropics. Global Health. 2024; 20(1):78. https://doi.org/10.1186/s12992-024-01083-3

Cardenas Perez AS, Challis JK, Alcaraz AJ, Ji X, Ramirez AVV, Hecker M et al.Developing an approach for integrating chemical analysis and transcriptional changes to assess contaminants in water, sediment, and fish. Environ Toxicol Chem. 2024; 43(11):2252–73. https://doi.org/10.1002/etc.5886

Choi Y, Kim M, Ha SY, Han GM, Yim UH, Jung J-H. Sediment quality assessment combining chemical and biological (non)target analysis. Aquat Toxicol. 2021; 238:105883. https://doi.org/10.1016/j.aquatox.2021.105883

Conesa A, Madrigal P, Tarazona S, Gomez-Cabrero D, Cervera A, McPherson A et al. A survey of best practices for RNA-seq data analysis. Genome Biol. 2016; 17(1):13. https://doi.org/10.1186/s13059-016-0881-8

Corredor-Santamaría W, Calderón-Delgado IC, Arbeli Z, Navas JM, Velasco-Santamaría YM. Acute effects on hepatic biomarkers in the freshwater native fish Aequidens metae exposed to polycyclic aromatic hydrocarbons. Glob J Environ Sci Manage. 2023; 9(1):1–14. https://doi.org/10.22034/gjesm.2023.01.01

Corredor-Santamaría W, Serrano Gómez M, Velasco-Santamaría YM. Using genotoxic and haematological biomarkers as an evidence of environmental contamination in the Ocoa River native fish, Villavicencio-Meta, Colombia. SpringerPlus. 2016; 5(1):351. https://doi.org/10.1186/s40064-016-1753-0

Corredor-Santamaría W, Torres-Tabares A, Velasco-Santamaría YM. Biochemical and histological alterations in Aequidens metae (Pisces, Cichlidae) and Astyanax gr. bimaculatus (Pisces, Characidae) as indicators of river pollution. Sci Total Environ. 2019; 692:1234–41. https://doi.org/10.1016/j.scitotenv.2019.07.187

Cortés-Miranda J, Rojas-Hernández N, Muñoz G, Copaja S, Quezada-Romegialli C, Veliz D et al.Biomarker selection depends on gene function and organ: the case of the cytochrome P450 family genes in freshwater fish exposed to chronic pollution. PeerJ. 2024a; 12:e16925. https://doi.org/10.7717/peerj.16925

Cortés-Miranda J, Veliz D, Rojas-Hernández N, Rico C, Gutiérrez C, Vega-Retter C. Chemical-defensome and whole-transcriptome expression of the silverside fish Basilichthys microlepidotus in response to chronic pollution in the Maipo River basin, Central Chile. Aquat Toxicol. 2024b; 277:107159. https://doi.org/10.1016/j.aquatox.2024.107159

Defo MA, Douville M, Giraudo M, Brodeur P, Boily M, Houde M. RNA-sequencing to assess the health of wild yellow perch (Perca flavescens) populations from the St. Lawrence River, Canada. Environ Pollut. 2018; 243:1657–68. https://doi.org/10.1016/j.envpol.2018.09.133

Environmental Protection Agency U. S. (EPA). Indicators: fish tissue contaminants. 2013. Available from: https://www.epa.gov/national-aquatic-resource-surveys/indicators-fish-tissue-contaminants

Escalante-Rojas MC, Tolussi CE, Gomes AD, Muñoz-Peñuela M, Brambila-Souza G, Branco GS et al. Integrated use of biomarkers to evaluate the reproductive physiology of Astyanax fasciatus and Hoplias malabaricus males (Teleostei: Characiformes) in polluted reservoirs. Ecotoxicol Environ Saf. 2021; 208:111502. https://doi.org/10.1016/j.ecoenv.2020.111502

Fé-Gonçalves LM, Araújo JDA, Santos CHA, Almeida-Val VMF. Transcriptomic evidences of local thermal adaptation for the native fish Colossoma macropomum (Cuvier, 1818). Genet Mol Biol. 2020; 43(3):e20190377. https://doi.org/10.1590/1678-4685-GMB-2019-0377

Förlin L, Asker N, Töpel M, Österlund T, Kristiansson E, Parkkonen J et al. mRNA expression and biomarker responses in perch at a biomonitoring site in the Baltic Sea – possible influence of natural brominated chemicals. Front Mar Sci. 2019; 6:316 https://doi.org/10.3389/fmars.2019.00316

Global Biodiversity Information Facility (GBIF). Chordata in GBIF Secretariat (2023). Copenhagen: Denmark; 2024. Available from: https://www.gbif.org/es/species/44

Guo J, Mo J, Qi Q, Peng J, Qi G, Kanerva M et al.Prediction of adverse effects of effluents containing phenolic compounds in the Ba River on the ovary of fish (Hemiculter leucisculus) using transcriptomic and metabolomic analyses. Sci Total Environ. 2021; 801:149554. https://doi.org/10.1016/j.scitotenv.2021.149554

Guo J, Mo J, Zhao Q, Han Q, Kanerva M, Iwata H et al.De novo transcriptomic analysis predicts the effects of phenolic compounds in Ba River on the liver of female sharpbelly (Hemiculter lucidus). Environ Pollut. 2020; 264:114642. https://doi.org/10.1016/j.envpol.2020.114642

Hahn CM, Iwanowicz LR, Cornman RS, Mazik PM, Blazer VS. Transcriptome discovery in non-model wild fish species for the development of quantitative transcript abundance assays. Comp Biochem Physiol D Genomics Proteomics. 2016; 20:27–40. https://doi.org/10.1016/j.cbd.2016.07.001

Hamilton PB, Lockyer AE, Uren Webster TM, Studholme DJ, Paris JR, Baynes A et al.Investigation into adaptation in genes associated with response to estrogenic pollution in populations of roach (Rutilus rutilus) living in english rivers. Environ Sci Technol. 2020; 54(24):15935–45. https://doi.org/10.1021/acs.est.0c00957

Helmy M, Awad M, Mosa KA. Limited resources of genome sequencing in developing countries: challenges and solutions. Appl Transl Genomics. 2016; 9:15–19. https://doi.org/10.1016/j.atg.2016.03.003

Hook SE, Kroon FJ, Greenfield PA, Warne MSJ, Smith RA, Turner RD. Hepatic transcriptomic profiles from barramundi, Lates calcarifer, as a means of assessing organism health and identifying stressors in rivers in northern Queensland. Mar Environ Res. 2017a; 129:166–79. https://doi.org/10.1016/j.marenvres.2017.05.006

Hook SE, Kroon FJ, Metcalfe S, Greenfield PA, Moncuquet P, McGrath A et al.Global transcriptomic profiling in barramundi (Lates calcarifer) from rivers impacted by differing agricultural land uses. Environ Toxicol Chem. 2017b; 36(1):103–12. https://doi.org/10.1002/etc.3505

Hook SE, Lampi MA, Febbo EJ, Ward JA, Parkerton TF. Temporal patterns in the transcriptomic response of rainbow trout, Oncorhynchus mykiss, to crude oil. Aquat Toxicol. 2010; 99(3):320–29. https://doi.org/10.1016/j.aquatox.2010.05.011

Hook SE, Mondon J, Revill AT, Greenfield PA, Smith RA, Turner RDR et al.Transcriptomic, lipid, and histological profiles suggest changes in health in fish from a pesticide hot spot. Mar Environ Res. 2018; 140:299–321. https://doi.org/10.1016/j.marenvres.2018.06.020

Jamil Emon F, Rohani MF, Sumaiya N, Tuj Jannat MF, Akter Y, Shahjahan M et al.Bioaccumulation and bioremediation of heavy metals in fishes – a review. Toxics. 2023; 11(6):510. https://doi.org/10.3390/toxics11060510

Jeffrey JD, Jeffries KM, Suski CD. Physiological status of silver carp (Hypophthalmichthys molitrix) in the Illinois River: An assessment of fish at the leading edge of the invasion front. Comp Biochem Physiol D Genomics Proteomics. 2019; 32:100614. https://doi.org/10.1016/j.cbd.2019.100614

Jordan-Ward R, von Hippel FA, Wilson CA, Rodriguez Maldonado Z, Dillon D, Contreras E et al. Differential gene expression and developmental pathologies associated with persistent organic pollutants in sentinel fish in Troutman Lake, Sivuqaq, Alaska. Environ Pollut. 2024; 340:122765. https://doi.org/10.1016/j.envpol.2023.122765

Kanerva M, Tue NM, Kunisue T, Vuori K, Iwata H. Effects on the liver transcriptome in Baltic salmon: contributions of contamination with organohalogen compounds and origin of salmon. Environ Sci Technol. 2020; 54(23):15246–56. https://doi.org/10.1021/acs.est.0c04763

Khan EA, Zhang X, Hanna EM, Bartosova Z, Yadetie F, Jonassen I et al.Quantitative transcriptomics, and lipidomics in evaluating ovarian developmental effects in Atlantic cod (Gadus morhua) caged at a capped marine waste disposal site. Environ Res. 2020; 189:109906. https://doi.org/10.1016/j.envres.2020.109906

Kumar Behera B, Nayak C, Kumar Rout A, Priyambada Pradhan S, Kumar Parida P, Jyoti Sarkar D et al.Transcriptome profiling of Nile tilapia (Oreochromis niloticus) identifies candidate genes in response to riverine pollution. Curr Res Biotechnol. 2024; 7:100180. https://doi.org/10.1016/j.crbiot.2024.100180

Lacaze É, Gendron AD, Miller JL, Colson TLL, Sherry JP, Giraudo M et al.Cumulative effects of municipal effluent and parasite infection in yellow perch: a field study using high-throughput RNA-sequencing. Sci Total Environ. 2019; 665:797–809. https://doi.org/10.1016/j.scitotenv.2019.02.155

Laurent J, Le Berre I, Armengaud J, Kailasam S, Couteau J, Waeles M et al.Integration of environmental signatures and omics-based approaches on the European flounder to assist with health assessment of estuarine ecosystems in Brittany, France. Sci Total Environ. 2023; 878:163195. https://doi.org/10.1016/j.scitotenv.2023.163195

Lazaro-Côté A, Faught E, Jackson LJ, Vijayan MM. Wild longnose dace downstream of wastewater treatment plants display an obese phenotype. Environ Pollut. 2021; 285:117363. https://doi.org/10.1016/j.envpol.2021.117363

Lerebours A, Robson S, Sharpe C, Nagorskaya L, Gudkov D, Haynes-Lovatt C et al.Transcriptional changes in the ovaries of perch from chernobyl. Environ Sci Technol. 2020; 54(16):10078–87. https://doi.org/10.1021/acs.est.0c02575

Lowe R, Shirley N, Bleackley M, Dolan S, Shafee T. Transcriptomics technologies. PLOS Comput Biol. 2017; 13(5):e1005457. https://doi.org/10.1371/journal.pcbi.1005457

Mackay D, Fraser A. Bioaccumulation of persistent organic chemicals: mechanisms and models. Environ Pollut. 2000; 110(3):375–91. https://doi.org/10.1016/S0269-7491(00)00162-7

Magnuson JT, Sydnes MO, Raeder EM, Schlenk D, Pampanin DM. Transcriptomic profiles of brains in juvenile Atlantic cod (Gadus morhua) exposed to pharmaceuticals and personal care products from a wastewater treatment plant discharge. Sci Total Environ. 2024; 912:169110. https://doi.org/10.1016/j.scitotenv.2023.169110

Marcelino RC, Cardoso RM, Domingues ELBC, Gonçalves RV, Lima GDA, Novaes RD. The emerging risk of microplastics and nanoplastics on the microstructure and function of reproductive organs in mammals: a systematic review of preclinical evidence. Life Sci. 2022; 295:120404. https://doi.org/10.1016/j.lfs.2022.120404

Martel JL, Brissette FP, Lucas-Picher P, Troin M, Arsenault R. Climate change and rainfall intensity–duration–frequency curves: overview of science and guidelines for adaptation. J Hydrol Eng. 2021; 26(10):03121001. https://doi.org/10.1061/(ASCE)HE.1943-5584.0002122

Martin SAM, Dehler CE, Król E. Transcriptomic responses in the fish intestine. Dev Comp Immunol. 2016; 64:103–17. https://doi.org/10.1016/j.dci.2016.03.014

Matheson P, McGaughran A. Genomic data is missing for many highly invasive species, restricting our preparedness for escalating incursion rates. Sci Rep. 2022; 12(1):13987. https://doi.org/10.1038/s41598-022-17937-y

McElroy AE, Hice LA, Frisk MG, Purcell SL, Phillips NC, Fast MD. Spatial patterns in markers of contaminant exposure, glucose and glycogen metabolism, and immunological response in juvenile winter flounder (Pseudoplueronectes americanus). Comp Biochem Physiol D Genomics Proteomics. 2015; 14:53–65. https://doi.org/10.1016/j.cbd.2015.01.006

McLimans CJ, Shelledy K, Conrad W, Prendergast K, Le AN, Grant CJ et al.Potential biomarkers of endocrine and habitat disruption identified via RNA-Seq in Salvelinus fontinalis with proximity to fracking operations in Pennsylvania headwater stream ecosystems. Ecotoxicology. 2022; 31(6):1044–55. https://doi.org/10.1007/s10646-022-02564-0

Mitra T, Mahanty A, Ganguly S, Mohanty BP. Transcriptomic responses to pollution in natural riverine environment in Rita rita. Environ Res. 2020; 186:109508. https://doi.org/10.1016/j.envres.2020.109508

Olsvik PA, Azad AM, Yadetie F. Bioaccumulation of mercury and transcriptional responses in tusk (Brosme brosme), a deep-water fish from a Norwegian fjord. Chemosphere. 2021; 279:130588. https://doi.org/10.1016/j.chemosphere.2021.130588

Pelayo-Villamil P, Guisande C, Vari RP, Manjarrés-Hernández A, García-Roselló E, González-Dacosta J et al.Global diversity patterns of freshwater fishes – potential victims of their own success. Divers Distrib. 2015; 21(3):345–56. https://doi.org/10.1111/ddi.12271

Piazza CE, Mattos JJ, Toledo-Silva G, Flores-Nunes F, Tadra-Sfeir MZ, Trevisan R et al.Transcriptional effects in the estuarine guppy Poecilia vivipara exposed to sanitary sewage in laboratory and in situ. Ecotoxicol Environ Saf. 2019; 182:109411. https://doi.org/10.1016/j.ecoenv.2019.109411

Priya AK, Muruganandam M, Sivarethinamohan R, Sujatha S, Madhava KRG, Priya V et al. Impact of climate change and anthropogenic activities on aquatic ecosystem – a review. Environ Res. 2023; 238:117233. https://doi.org/10.1016/j.envres.2023.117233

Qiu W, Liu S, Yang F, Dong P, Yang M, Wong M et al.Metabolism disruption analysis of zebrafish larvae in response to BPA and BPA analogs based on RNA-Seq technique. Ecotoxicol Environ Saf. 2019; 174:181–88. https://doi.org/10.1016/j.ecoenv.2019.01.126

Ribeiro YM, Moreira DP, Weber AA, Sales CF, Melo RMC, Bazzoli N et al. Adverse effects of herbicides in freshwater Neotropical fish: a review. Aquat Toxicol. 2022; 252. https://doi.org/10.1016/j.aquatox.2022.106293

Schmitz M, Deutschmann B, Markert N, Backhaus T, Brack W, Brauns M et al.Demonstration of an aggregated biomarker response approach to assess the impact of point and diffuse contaminant sources in feral fish in a small river case study. Sci Total Environ. 2022; 804:150020. https://doi.org/10.1016/j.scitotenv.2021.150020

Selle B, Blume A, Höllrigl-Rosta A, Gräff T. Analysis and modelling of profiles to understand fractionation processes for contaminations with polychlorinated biphenyls observed in fish. Sci Total Environ. 2024; 920:170925. https://doi.org/10.1016/j.scitotenv.2024.170925

Sepp T, Baines C, Kreitsberg R, Scharsack JP, Nogueira P, Lang T et al.Differences on the level of hepatic transcriptome between two flatfish species in response to liver cancer and environmental pollution levels. Comp Biochem Physiol C Toxicol Pharmacol. 2024; 275:109781. https://doi.org/10.1016/j.cbpc.2023.109781

Srisiri S, Haetrakul T, Dunbar SG, Chansue N. Microplastic contamination in edible marine fishes from the upper Gulf of Thailand. Mar Pollut Bull. 2024; 198:115785. https://doi.org/10.1016/j.marpolbul.2023.115785

Tata T, Belabed BE, Boucheker A, Bououdina M, Bellucci S, Kyzas GZ. Seasonal and spatial contamination of trace elements in sediments and fish tissues (Mugil chephalus) from Annaba gulf (North East of Algeria). Sci Total Environ. 2023; 900:166137. https://doi.org/10.1016/j.scitotenv.2023.166137

Theissinger K, Fernandes C, Formenti G, Bista I, Berg PR, Bleidorn C et al.How genomics can help biodiversity conservation. TIG. 2023; 39(7):545–59. https://doi.org/10.1016/j.tig.2023.01.005

Tolussi CE, Gomes ADO, Kumar A, Ribeiro CS, Lo Nostro FL, Bain PA et al.Environmental pollution affects molecular and biochemical responses during gonadal maturation of Astyanax fasciatus (Teleostei: Characiformes: Characidae). Ecotoxicol Environ Saf. 2018; 147:926–34. https://doi.org/10.1016/j.ecoenv.2017.09.056

Uren Webster TM, Santos EM. Global transcriptomic profiling demonstrates induction of oxidative stress and of compensatory cellular stress responses in brown trout exposed to glyphosate and Roundup. BMC Genomics. 2015; 16(1):32. https://doi.org/10.1186/s12864-015-1254-5

Vega-Retter C, Rojas-Hernandez N, Vila I, Espejo R, Loyola DE, Copaja S et al.Differential gene expression revealed with RNA-Seq and parallel genotype selection of the ornithine decarboxylase gene in fish inhabiting polluted areas. Sci Rep. 2018; 8(1):4820. https://doi.org/10.1038/s41598-018-23182-z

Vehniäinen E-R, Ruusunen M, Vuorinen PJ, Keinänen M, Oikari AOJ, Kukkonen JVK. How to preserve and handle fish liver samples to conserve RNA integrity. Environ Sci Pollut Res. 2019; 26(17):17204–13. https://doi.org/10.1007/s11356-019-05033-0

Velasco-Santamaría YM, Cardenas-Camacho J, Peñuela-Díaz MM, Jaramillo-Hernández DA, Corredor-Santamaría W. Efectos agudos de fenantreno y benzo[a]pireno en Aequidens metae (Pisces: Cichlidae). Rev Colomb Biotecnol. 2024; 26(1):42–51. https://doi.org/10.15446/rev.colomb.biote.v26n1.101879

Velasco-Santamaría YM, Corredor-Santamaría W, Torres-Tabares A. Correction to: environmental pollution by hydrocarbons in Colombia and its impact on the health of aquatic ecosystems. In: Gómez-Oliván LM, editor. Pollution of water bodies in Latin America: impact of contaminants on species of ecological interest. Cham: Springer Int Publ. 2019; p.C1–C3. https://doi.org/10.1007/978-3-030-27296-8_21

Vreedzaam A, Ouboter P, Hindori-Mohangoo AD, Lepak R, Rumschlag S, Janssen S et al. Contrasting mercury contamination scenarios and site susceptibilities confound fish mercury burdens in Suriname, South America. Environ Pollut. 2023; 336:122447. https://doi.org/10.1016/j.envpol.2023.122447

Wang X, Sato T, Xing B, Tao S. Health risks of heavy metals to the general public in Tianjin, China via consumption of vegetables and fish. Sci Total Environ. 2005; 350(1):28–37. https://doi.org/10.1016/j.scitotenv.2004.09.044

Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009; 10(1):57–63. https://doi.org/10.1038/nrg2484

Ye B, Wang Q, Ye Q, Wang D, Wang Z, Dong Z et al.Effects of different combinations of koumine and gelsemine on growth performance, intestinal health, and transcriptome of Cyprinus carpio. J Hazard Mater. 2024; 465:133130. https://doi.org/10.1016/j.jhazmat.2023.133130

Zhang W, Xie HQ, Zou X, Li J, Xu L, Li Y et al.The toxic effects of in situ exposure of a native fish species (Anabas testudineus) to electronic waste pollution. Sci Total Environ. 2019; 690:1170–77. https://doi.org/10.1016/j.scitotenv.2019.06.479

Zhou S, Wei Z, Chu T, Yu H, Li S, Zhang W et al.Transcriptomic analysis of zebrafish (Danio rerio) embryos to assess integrated biotoxicity of Xitiaoxi River waters. Environ Pollut. 2018; 242:42–53. https://doi.org/10.1016/j.envpol.2018.06.060

Zulkifli SN, Rahim HA, Lau W-J. Detection of contaminants in water supply: a review on state-of-the-art monitoring technologies and their applications. Sens Actuators B Chem. 2018; 255:2657–89. https://doi.org/10.1016/j.snb.2017.09.078

Authors

---

Jessica Cardenas-Camacho^1,2, Ivonne Calderón-Delgado¹, Wilson Corredor-Santamaría¹ and Yohana M. Velasco-Santamaría¹

^[1]    Grupo de investigación en Biotecnología y Toxicología Acuática y Ambiental – BioTox, Universidad de los Llanos, 1745, AA 110 Villavicencio, Colombia. (JCC) jescardenasca@unal.edu.co, (ICD) icalderon@unillanos.edu.co, (WCS) wcorredor@unillanos.edu.co (corresponding author), (YMVS) ymvelascos@unillanos.edu.co.

^[2]    Universidad Nacional de Colombia, 111321 Bogota D.C, Colombia.

Authors’ Contribution

---

Jessica Cardenas-Camacho: Conceptualization, Formal analysis, Methodology, Visualization, Writing-review and editing.
Ivonne Calderón-Delgado: Conceptualization, Project administration, Supervision, Visualization, Writing-review and editing.

Wilson Corredor-Santamaría: Conceptualization, Formal analysis, Supervision, Writing-review and editing.

Yohana M. Velasco-Santamaría: Conceptualization, Formal analysis, Project administration, Writing-review and editing.

Ethical Statement​

---

Not applicable.

Competing Interests

---

The author declares no competing interests.

How to cite this article

---

Cardenas-Camacho J, Calderón-Delgado I, Corredor-Santamaría W, Velasco-Santamaría YM. The use of transcriptomics in situ study through fish: a systematic review on pollution. Neotrop Ichthyol. 2025; 23(2):e240133. https://doi.org/10.1590/1982-0224-2024-0133

Copyright​

---

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Distributed under

Creative Commons CC-BY 4.0

© 2025 The Authors.

Diversity and Distributions Published by SBI

Accepted April 29, 2025

Submitted December 13, 2024

Epub August 04, 2025