Dataset Information

Seasonal variation in the skin transcriptome of common bottlenose dolphins (Tursiops truncatus) from the northern Gulf of Mexico.

ABSTRACT: As long-lived predators that integrate exposures across multiple trophic levels, cetaceans are recognized as sentinels for the health of marine ecosystems. Their utility as sentinels requires the establishment of baseline health parameters. Because cetaceans are protected, measurements obtained with minimal disruption to free ranging animals are highly desirable. In this study we investigated the utility of skin gene expression profiling to monitor health and contaminant exposure in common bottlenose dolphins (Tursiops truncatus). Remote integument biopsies were collected in the northern Gulf of Mexico prior to the Deepwater Horizon oil spill (May 2010) and during summer and winter for two years following oil contamination (2010-2011). A bottlenose dolphin microarray was used to characterize the skin transcriptomes of 94 individuals from three populations: Barataria Bay, Louisiana, Chandeleur Sound, Louisiana, and Mississippi Sound, Mississippi/Alabama. Skin transcriptomes did not differ significantly between populations. In contrast, season had a profound effect on gene expression, with nearly one-third of all genes on the array differing in expression between winter and the warmer seasons (moderated T-test; p<0.01, fold-change?1.5). Persistent organic pollutants (POPs) in blubber changed concurrently, reaching >two-fold higher concentrations in summer compared to winter, due to a seasonal decrease in blubber thickness and loss of stored lipid. However, global gene expression did not correlate strongly with seasonally changing contaminant concentrations, most likely because the refractory, lipid-stored metabolites are not substrates for phase I or II xenobiotic detoxification pathways. Rather, processes related to cell proliferation, motility, and differentiation dominated the differences in expression in winter and the warmer seasons. More subtle differences were seen between spring and summer (1.5% of genes differentially expressed). However, two presumed oil-exposed animals from spring presented gene expression profiles more similar to the summer animals (presumed exposed) than to other spring animals. Seasonal effects have not previously been considered in studies assessing gene expression in cetaceans, but clearly must be taken into account when applying transcriptomic analyses to investigate their contaminant exposure or health status.

SUBMITTER: Van Dolah FM

PROVIDER: S-EPMC4482424 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Publications

Seasonal variation in the skin transcriptome of common bottlenose dolphins (Tursiops truncatus) from the northern Gulf of Mexico.

Van Dolah Frances M FM Neely Marion G MG McGeorge Lauren E LE Balmer Brian C BC Ylitalo Gina M GM Zolman Eric S ES Speakman Todd T Sinclair Carrie C Kellar Nicholas M NM Rosel Patricia E PE Mullin Keith D KD Schwacke Lori H LH

PloS one 20150625 6

As long-lived predators that integrate exposures across multiple trophic levels, cetaceans are recognized as sentinels for the health of marine ecosystems. Their utility as sentinels requires the establishment of baseline health parameters. Because cetaceans are protected, measurements obtained with minimal disruption to free ranging animals are highly desirable. In this study we investigated the utility of skin gene expression profiling to monitor health and contaminant exposure in common bottl ...[more]

PMID: 26110790

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Project description:Common bottlenose dolphins serve as sentinels for the health of their coastal environments as they are susceptible to health impacts from anthropogenic inputs through both direct exposure and food web magnification. Remote biopsy samples have been widely used to reveal contaminant burdens in free-ranging bottlenose dolphins, but do not address the health consequences of this exposure. To gain insight into whether remote biopsies can also identify health impacts associated with contaminant burdens, we employed RNA sequencing (RNA-seq) to interrogate the transcriptomes of remote skin biopsies from 116 bottlenose dolphins from the northern Gulf of Mexico and southeastern U.S. Atlantic coasts. Gene expression was analyzed using principal component analysis, differential expression testing, and gene co-expression networks, and the results correlated to season, location, and contaminant burden. Season had a significant impact, with over 30% of genes differentially expressed between spring/summer and winter months. Geographic location exhibited lesser effects on the transcriptome, with 15% of genes differentially expressed between the northern Gulf of Mexico and the southeastern U.S. Atlantic locations. Despite a large overlap between the seasonal and geographical gene sets, the pathways altered in the observed gene expression profiles were somewhat distinct. Co-regulated gene modules and differential expression analysis both identified epidermal development and cellular architecture pathways to be expressed at lower levels in animals from the northern Gulf of Mexico. Although contaminant burdens measured were not significantly different between regions, some correlation with contaminant loads in individuals was observed among co-expressed gene modules, but these did not include classical detoxification pathways. Instead, this study identified other, possibly downstream pathways, including those involved in cellular architecture, immune response, and oxidative stress, that may prove to be contaminant responsive markers in bottlenose dolphin skin.

Project description:As apex predators, cetaceans are recognized as sentinels for the health of marine ecosystems. The ability to identify the impacts of anthropogenic contamination on the health of a species requires long term monitoring to establish baseline health parameters. This makes health measurements that can be sampled from free ranging animals highly desirable. In the current study, we investigate the utility of skin gene expression profiling to monitor the physiological, health, and contaminant exposure status in bottlenose dolphins. Remote integument biopsies were obtained from bottlenose dolphins at three locations in the northern Gulf of Mexico prior to oil exposure (May 2010) and during summer and winter of the two years (2010-2011) following their exposure to oil from the Deepwater Horizon oil spill. A bottlenose dolphin-specific oligonucleotide microarray was used to characterize the skin transcriptomes of 94 individuals from three genetically distinguishable populations in Barataria Bay, Louisiana, Chandeleur Sound, Louisiana, and Mississippi Sound, Mississippi. Location did not significantly affect the transcriptome patterns of the dolphins included in the study. In contrast, season had a profound effect on gene expression, with nearly one-third of all genes on the array differing significantly in expression between winter and the warmer seasons (p<0.01, fold-change >1.5). Gene ontology enrichment analysis revealed that processes related to cell proliferation, motility and differentiation dominated the seasonal differences in expression, which likely reflects the differences in ambient temperature to which the skin is exposed, and possibly changes in blood flow. More subtle differences were seen between spring and summer transcriptomes (1.5% differentially expressed), with two presumed oil-exposed animals presenting gene expression profiles more similar to the summer (exposed) animals than the other spring animals. Xenobiotic pathway components also showed some seasonal trends, which may reflect crosstalk between xenobiotic pathways and those regulating corticoids, hormones, and cytokines. Seasonal effects have not previously been considered in studies assessing gene expression in cetaceans, but clearly must be taken into account when applying transcriptomic analyses to investigate their exposure or health status.

Project description:The Deepwater Horizon (DWH) oil spill profoundly impacted the health of bottlenose dolphins (Tursiops truncatus) in Barataria Bay, LA (BB). To comprehensively assess the cardiac health of dolphins living within the DWH oil spill footprint, techniques for in-water cardiac evaluation were refined with dolphins cared for by the U.S. Navy Marine Mammal Program in 2018 and applied to free-ranging bottlenose dolphins in BB (n = 34) and Sarasota Bay, Florida (SB) (n = 19), a non-oiled reference population. Cardiac auscultation detected systolic murmurs in the majority of dolphins from both sites (88% BB, 89% SB) and echocardiography showed most of the murmurs were innocent flow murmurs attributed to elevated blood flow velocity [1]. Telemetric six-lead electrocardiography detected arrhythmias in BB dolphins (43%) and SB dolphins (31%), all of which were considered low to moderate risk for adverse cardiac events. Echocardiography showed BB dolphins had thinner left ventricular walls, with significant differences in intraventricular septum thickness at the end of diastole (p = 0.002), and left ventricular posterior wall thickness at the end of diastole (p = 0.033). BB dolphins also had smaller left atrial size (p = 0.004), higher prevalence of tricuspid valve prolapse (p = 0.003), higher prevalence of tricuspid valve thickening (p = 0.033), and higher prevalence of aortic valve thickening (p = 0.008). Two dolphins in BB were diagnosed with pulmonary arterial hypertension based on Doppler echocardiography-derived estimates and supporting echocardiographic findings. Histopathology of dolphins who stranded within the DWH oil spill footprint showed a significantly higher prevalence of myocardial fibrosis (p = 0.003), regardless of age, compared to dolphins outside the oil spill footprint. In conclusion, there were substantial cardiac abnormalities identified in BB dolphins which may be related to DWH oil exposure, however, future work is needed to rule out other hypotheses and further elucidate the connection between oil exposure, pulmonary disease, and the observed cardiac abnormalities.

Project description:Urinary proteins provide valuable insights into renal health, with implications spanning human and domestic animal veterinary medical research. However, the field of marine mammal medicine lacks comprehensive studies on urine protein composition. This research aimed to fill this gap by 1) selecting an optimal search strategy that yields the highest number of protein families in the bottlenose dolphin urine based on post-translational modifications (PTMs), 2) describing the urine proteome of wild bottlenose dolphins (Tursiops truncatus) in the Gulf of the Mexico, USA, considering sex (females vs. males), site (Barataria Bay, LA vs. Sarasota Bay, FL), and comparing with California sea lions (Zalophus californianus). Ten urine samples (Barataria Bay, LA: N= 6; Sarasota Bay, FL: N=4) collected during 2023 catch-and-release heath assessment were proteolytically digested and analyzed using an UltiMate 3000 Nano LC and Fusion Lumos Orbitrap mass spectrometer. A 2-step search strategy, incorporating dehydroalanine formation and semi-trypsin on the list of unassigned spectra, significantly increased the number of identified protein families by an average of 6.2% compared to the 1-step strategy (P < 0.001, t = -8.32). The top 30 proteins in bottlenose dolphin urine were ranked according to an exponentially modified protein abundance index for comparison based on sex, site, and species. There were no significant differences in urine proteins between sexes or sites (padj > 0.05), although there was sperm contribution in two of the male bottlenose dolphin urine samples. Two putative antimicrobial proteins (cathelicidin and lysozyme) were identified and found to be abundant in bottlenose dolphin urine, similar to California sea lions. The study also identified 27 potential markers of acute kidney injury and 12 regulators of kidney stone formation. This study established a reference database of urinary proteins from bottlenose dolphins, aiding future research in monitoring and evaluating renal health in marine mammals.

Project description:Few accounts describe predator-prey interactions between common bottlenose dolphins (Tursiops truncatus Montagu 1821) and marine catfish (Ariopsis felis Linnaeus 1766, Bagre marinus Mitchill 1815). Over the course of 50,167 sightings of bottlenose dolphin groups in Mississippi Sound and along the Florida coast of the Gulf of Mexico, severed catfish heads were found floating and exhibiting movements at the surface in close proximity to 13 dolphin groups that demonstrated feeding behavior. These observations prompted a multi-disciplinary approach to study the predator-prey relationship between bottlenose dolphins and marine catfish. A review was conducted of bottlenose dolphin visual survey data and dorsal fin photographs from sightings where severed catfish heads were observed. Recovered severed catfish heads were preserved and studied, whole marine catfish were collected and examined, and stranding network pathology reports were reviewed for references to injuries related to fish spines. Photographic identification analysis confirms eight dolphins associated with severed catfish heads were present in three such sightings across an approximately 350 km expanse of coast between the Mississippi Sound and Saint Joseph Bay, FL. An examination of the severed catfish heads indicated interaction with dolphins, and fresh-caught whole hardhead catfish (A. felis) were examined to estimate the presumed total length of the catfish before decapitation. Thirty-eight instances of significant trauma or death in dolphins attributed to ingesting whole marine catfish were documented in stranding records collected from the southeastern United States of America. Bottlenose dolphins typically adhere to a ram-feeding strategy for prey capture followed by whole prey ingestion; however, marine catfish skull morphology may pose a consumption hazard due to rigid spines that can puncture and migrate through soft tissue, prompting a prey handling technique for certain dolphins, facilitating consumption of the posterior portion of the fish without the head.

Project description:In recent decades, animal welfare science has evolved to utilize a multidisciplinary approach to assess the welfare of animals in accredited zoos and aquariums. Science-based animal welfare assessments have become an essential component of management programs and widespread application is expected by animal care professionals. Management practices for bottlenose dolphins in accredited facilities incorporate several programs that potentially impact animal welfare including environmental enrichment and animal training. Additionally, habitat characteristics, such as the dimensions of the habitat, have been proposed to affect welfare. While accredited facilities are required to meet high standards of care, habitat characteristics and management practices are not standardized across locations. Knowledge and subsequent application of these practices and habitat characteristics can enhance our understanding of factors associated with positive welfare. As part of a larger study of dolphin welfare titled "Towards understanding the welfare of cetaceans in zoos and aquariums" (colloquially called the Cetacean Welfare Study), survey data were collected from 86 bottlenose dolphins in 40 habitats at 38 facilities in seven countries. The major aims of this paper are to provide general descriptive information regarding dolphin management in accredited zoos and aquariums and to provide supplemental context to the other research published from the Cetacean Welfare Study data set. This paper provides a review of current habitat characteristics and management practices at those 38 accredited zoos and aquariums. These data enabled the identification and quantification of how cetacean management practices differed between participating facilities accredited by the Alliance for Marine Mammal Parks and Aquariums and the Association of Zoos & Aquariums. Variables were selected based on their potential association with welfare including the physical habitat, environmental enrichment, and training programs. The variables were also used for subsequent research in this collection of related papers to investigate important connections between potential indicators of welfare and habitat characteristics, environmental enrichment, and training programs.

Project description:Considerable efforts have been made to better understand the immune system of bottlenose dolphins in view of the common environmental challenges they encounter, such as exposure to polychlorinated biphenyls, oil spills, or harmful algal bloom biotoxins. However, little is known about the identity and functionality of the Th1, Th2, and Treg T helper cell subsets in bottlenose dolphins. The present study aimed at validating assays and reagents to identify T helper cell subsets and their functions in a subset of dolphins from Sarasota Bay, Florida, USA, which have been long studied and often used as a reference population. A population of CD4+ FOXP3+ lymphocytes was identified representing an average <1% of blood lymphocyte population, which is in the range observed in for Treg cells in other species. The use of porcine reagents to measure TGFß, one of the key Treg cytokines, was further validated using the relatively high-throughput and highly standardized Luminex technology. The proportion of circulating Treg cells was not correlated with the serum concentrations of the Treg effector cytokines TGFß and IL-10, nor could it significantly contribute to predicting the variability of T lymphocyte proliferation, suggesting that not all dolphin circulating Treg cells are functional and active. However, stimulation of dolphin lymphocytes with TGFß and IL-2 increased the expression of the gene for TGFß and IL-10, and stimulation with IL-12 and IFN? induced a robust increase in the expression of the gene for IFN?, suggesting the potential for polarization and differentiation of dolphin T helper cells toward a Treg and Th1 response, respectively. The lack of an increase in the expression of the genes for the Th2 cytokines IL-4 and IL-13 upon stimulation with IL-4 may be due to the requirement for IL-2 for a Th2 polarization as described in mice. However, regression analysis and PCA suggested the potential ability of both the Th1 and Th2 response to be triggered upon acute inflammatory signals. These results may be useful in better understanding the mechanisms by which the dolphin immune system is affected upon exposure to environmental challenges and how it responds to pathogen challenges.

Dataset Information

Seasonal variation in the skin transcriptome of common bottlenose dolphins (Tursiops truncatus) from the northern Gulf of Mexico.

Publications

Seasonal variation in the skin transcriptome of common bottlenose dolphins (Tursiops truncatus) from the northern Gulf of Mexico.

Similar Datasets

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