Biology subjects

Venkataraman, Y. R.

Publications and source records attributed to Venkataraman, Y. R..

10 recordsLinked to original sources

bioRxiv2026

Metabolomic and lipidomic shifts underpin physiological acclimation to thermal stress in the European green crab (Carcinus maenas)

Many marine invertebrates are characterized by broad and highly plastic thermal limits, though the dynamic molecular mechanisms that enable extended thermal acclimation remain poorly understood. A classic example is the green crab (Carcinus maenas), which is a prolific and damaging non-indigenous species. Using a 22-day thermal exposure to cold (5{degrees}C), ambient (13{degrees}C), or warm (30{degrees}C) temperatures, we characterized plastic shifts in C. maenas performance using respirometry and time-to-right. We then used untargeted metabolomics and lipidomics analysis of heart tissues from days 4 and 22 to identify the molecular mechanisms underpinning plastic responses over time. Crabs at 30{degrees}C exhibited higher oxygen consumption rates than counterparts at 5{degrees}C. Interestingly, oxygen consumption rate increased over time at both temperatures, indicating thermal plasticity of aerobic respiration. Temperature-dependent metabolic reprogramming was employed by crabs to sustain aerobic respiration across temperature. Catabolism of branched-chain amino acids was important for energy production at elevated temperatures, while catabolism of arginine may have sustained the minimal energy needs of crabs exhibiting metabolic depression at cold temperatures. Righting response was positively correlated with temperature, and did not exhibit any changes over time. Lipidome remodeling consistent with homeoviscous adaptation could have enabled motor activity across temperature. Higher abundances of saturated and monounsaturated lipids likely provided structural integrity to cell membranes at 30{degrees}C, while lower abundances of these compounds may have enabled membrane fluidity at 5{degrees}C. Our work demonstrates the importance of ongoing molecular reprogramming in long-term acclimation, even when whole-animal physiology remains relatively stable. Summary StatementThis study demonstrates how the highly invasive green crab regulates metabolite and lipid pathways over time to maintain physiological performance across different temperatures.

physiology↗

bioRxiv2025

Plasticity and genetics shape thermal tolerance in non-native populations of the European green crab (Carcinus maenas)

Temperature is a major driver of individual performance in ectotherms, with this impact depending on stressor intensity and duration. Differences in individual response across temperature, time, and populations are shaped by the interplay between evolutionary adaptation and phenotypic plasticity. Some populations are able to thrive in novel and changing environments despite limited genetic diversity, raising the question of how plasticity and adaptation interact after significant genetic diversity loss. The European green crab (Carcinus maenas) is a textbook example of this phenomenon: invasive populations boast a broad thermal tolerance and exceptional thermal flexibility even after repeated genetic bottlenecks. Despite this loss of diversity overall, prior work has found a strong population-level association between variation at a specific extended genomic region (supergene), cold tolerance, and sea surface temperature. We conducted a series of three experiments using righting response to characterize sublethal thermal tolerance and plasticity in introduced green crab populations, then determined if these factors were associated with supergene genotype for individual adult crabs. Crabs showed signs of stress after exposure to a 30{degrees}C heat shock in one experiment. Interestingly, a second experiment exposing C. maenas to repeated 24-hour heat shocks showed that prior heat shock conferred beneficial plasticity during a subsequent event. The third experiment examined cold acclimation over multiple timepoints up to 94 hours. At 5{degrees}C, certain crabs exhibited an acclimatory response where righting slowed dramatically at first, and then gradually sped up after a longer period of cold exposure. Several crabs failed to right at 1.5{degrees}C, which could be indicative of dormancy employed to reduce energy consumption in colder conditions. There were no significant relationships between individual plasticity and supergene genotype in any experiment. Linking population-level genetic associations with individual-level physiology is complex, and reflects the impact of environmental conditions such as temperature throughout life history in shaping adult phenotype. Our results highlight the robust thermal tolerance and plasticity that adult green crabs maintain despite a substantial reduction in genetic diversity, and underscore the importance of probing population-level genotype-phenotype associations at the individual level.

physiology↗

bioRxiv2024

Gene expression and DNA methylation changes in response to hypoxia in toxicant-adapted Atlantic killifish (Fundulus heteroclitus)

Coastal fish populations are threatened by multiple anthropogenic impacts, including the accumulation of industrial contaminants and the increasing frequency of hypoxia. Some populations of the Atlantic killifish (Fundulus heteroclitus), like those in New Bedford Harbor (NBH), Massachusetts, have evolved a resistance to dioxin-like polychlorinated biphenyls (PCBs) that may influence their ability to cope with secondary stressors. To address this question, we compared hepatic gene expression and DNA methylation patterns in response to mild or severe hypoxia in killifish from NBH and Scorton Creek (SC), a reference population from a relatively pristine environment. We hypothesized that NBH fish would show altered responses to hypoxia due to trade-offs linked to toxicant resistance. Our results revealed substantial differences between populations. SC fish demonstrated a dose-dependent changes in gene expression in response to hypoxia, while NBH fish exhibited a muted transcriptional response to severe hypoxia. Interestingly, NBH fish showed significant DNA methylation changes in response to hypoxia, while SC fish did not exhibit notable epigenetic alterations. These findings suggest that toxicant-adapted killifish may face trade-offs in their molecular response to environmental stress, potentially impacting their ability to survive severe hypoxia in coastal habitats. Further research is needed to elucidate the functional implications of these epigenetic modifications and their role in adaptive stress responses. Summary StatementThis study reveals how evolved resistance to toxicants in killifish may compromise their ability to respond to hypoxia, highlighting trade-offs that impact survival in stressed coastal environments.

physiology↗

bioRxiv2024

DNA methylation modulates transcriptional noise in response to elevated pCO2 in the eastern oyster (Crassostrea virginica)

Ocean acidification significantly affects marine calcifiers like oysters, warranting the study of molecular mechanisms like DNA methylation that contribute to adaptive plasticity in response to environmental change. However, a consensus has not been reached on the extent to which methylation modules gene expression, and in turn plasticity, in marine invertebrates. In this study, we investigated the impact of pCO2 on gene expression and DNA methylation in the eastern oyster, Crassostrea virginica. After a 30-day exposure to control (572 ppm) or elevated pCO2 (2,827 ppm), whole genome bisulfite sequencing (WGBS) and RNA-Seq data were generated from adult female gonad tissue and male sperm samples. Although differentially methylated loci (DML) were identified in females (89) and males (2,916), there were no differentially expressed genes, and only one differentially expressed transcript in females. However, gene body methylation impacted other forms of gene activity in sperm, such as the maximum number of transcripts expressed per gene and changes in the predominant transcript expressed. Elevated pCO2 exposure increased gene expression variability (transcriptional noise) in males but decreased noise in females, suggesting a sex-specific role of methylation in gene expression regulation. Functional annotation of genes with changes in transcript-level expression or containing DML revealed several enriched biological processes potentially involved in elevated pCO2 response, including apoptotic pathways and signal transduction, as well as reproductive functions. Taken together, these results suggest that DNA methylation may regulate gene expression variability to maintain homeostasis in elevated pCO2 conditions and could play a key role in environmental resilience in marine invertebrates.

physiology↗

bioRxiv2022

Differential DNA methylation in Pacific oyster reproductive tissue associated with ocean acidification

BackgroundThere is a need to investigate mechanisms of phenotypic plasticity in marine invertebrates as negative effects of climate change, like ocean acidification, are experienced by coastal ecosystems. Environmentally-induced changes to the methylome may regulate gene expression, but methylome responses can be species- and tissue-specific. Tissue-specificity has implications for gonad tissue, as gonad-specific methylation patterns may be inherited by offspring. We used the Pacific oyster (Crassostrea gigas) -- a model for understanding pH impacts on bivalve molecular physiology due to its genomic resources and importance in global aquaculture-- to assess how low pH could impact the gonad methylome. Oysters were exposed to either low pH (7.31 {+/-} 0.02) or ambient pH (7.82 {+/-} 0.02) conditions for seven weeks. Whole genome bisulfite sequencing was used to identify methylated regions in female oyster gonad samples. C->T single nucleotide polymorphisms were identified and removed to ensure accurate methylation characterization. ResultsAnalysis of gonad methylomes revealed a total of 1,284 differentially methylated loci (DML) found primarily in genes, with several genes containing multiple DML. Gene ontologies for genes containing DML were involved in development and stress response, suggesting methylation may promote gonad growth homeostasis in low pH conditions. Additionally, several of these genes were associated with cytoskeletal structure regulation, metabolism, and protein ubiquitination -- commonly-observed responses to ocean acidification. Comparison of these DML with other Crassostrea spp. exposed to ocean acidification demonstrates that similar pathways, but not identical genes, are impacted by methylation. ConclusionsOur work suggests DNA methylation may have a regulatory role in gonad and larval development, which would shape adult and offspring responses to low pH stress. Combined with existing molluscan methylome research, our work further supports the need for tissue- and species-specific studies to understand the potential regulatory role of DNA methylation.

genomics↗

bioRxiv2021

Invertebrate methylomes provide insight into mechanisms of environmental tolerance and reveal methodological biases

There is a growing focus on the role of DNA methylation in the ability of marine invertebrates to rapidly respond to changing environmental factors and anthropogenic impacts. However, genome-wide DNA methylation studies in non-model organisms are currently hampered by limited understanding of methodological biases. Here we compare three methods for quantifying DNA methylation at single base-pair resolution -- Whole Genome Bisulfite Sequencing (WGBS), Reduced Representation Bisulfite Sequencing (RRBS), and Methyl-CpG Binding Domain Bisulfite Sequencing (MBDBS) -- using multiple individuals from two reef-building coral species with contrasting environmental sensitivity. All methods reveal substantially greater methylation in Montipora capitata (11.4%) than the more sensitive Pocillopora acuta (2.9%). The majority of CpG methylation in both species occurs in gene bodies and flanking regions. In both species, MBDBS has the greatest capacity for detecting CpGs in coding regions at our sequencing depth, however MBDBS may be influenced by intra-sample methylation heterogeneity. RRBS yields robust information for specific loci albeit without enrichment of any particular genome feature and with significantly reduced genome coverage. Relative genome size strongly influences the number and location of CpGs detected by each method when sequencing depth is limited, illuminating nuances in cross-species comparisons. As genome-wide methylation differences, supported by data across bisulfite sequencing methods, may contribute to environmental sensitivity phenotypes in critical marine invertebrate taxa, these data provide a genomic resource for investigating the functional role of DNA methylation in environmental tolerance.

genomics↗

bioRxiv2020

General DNA methylation patterns and environmentally-induced differential methylation in the eastern oyster (Crassostrea virginica)

Epigenetic modification, specifically DNA methylation, is one possible mechanism for intergenerational plasticity. Before inheritance of methylation patterns can be characterized, we need a better understanding of how environmental change modifies the parental epigenome. To examine the influence of experimental ocean acidification on eastern oyster (Crassostrea virginica) gonad tissue, oysters were cultured in the laboratory under control (491 {+/-} 49 atm) or high (2550 {+/-} 211 atm) pCO2 conditions for four weeks. DNA from reproductive tissue was isolated from five oysters per treatment, then subjected to bisulfite treatment and DNA sequencing. Irrespective of treatment, DNA methylation was primarily found in gene bodies with approximately 22% of CpGs (2.7% of total cytosines) in the C. virginica genome predicted to be methylated. In response to elevated pCO2, we found 598 differentially methylated loci primarily overlapping with gene bodies. A majority of differentially methylated loci were in exons (61.5%) with less intron overlap (31.9%). While there was no evidence of a significant tendency for the genes with differentially methylated loci to be associated with distinct biological processes, the concentration of these loci in gene bodies, including genes involved in protein ubiquitination and biomineralization suggests DNA methylation may be important for transcriptional control in response to ocean acidification. Changes in gonad methylation also indicate potential for these methylation patterns to be inherited by offspring. Understanding how experimental ocean acidification conditions modify the oyster epigenome, and if these modifications are inherited, allows for a better understanding of how ecosystems will respond to environmental change.

genomics↗

bioRxiv2019

Carry-over effects of temperature and pCO2 in multiple Olympia oyster populations

Predicting how populations will respond to ocean change across generations is critical to effective conservation of marine species. One emerging factor is the influence of parental exposures on offspring phenotype, known as intergenerational carryover effects. Parental exposure may deliver beneficial or detrimental characteristics to offspring that can influence larval recruitment patterns, thus shaping how populations and community structure respond to ocean change. Impacts of adult exposure to elevated winter temperature and pCO2 on reproduction and offspring viability were examined in the Olympia oyster (Ostrea lurida) using three populations of adult, hatchery-reared O. lurida, plus an additional cohort spawned from one of the populations. Oysters were sequentially exposed to elevated temperature (+4{degrees}C, at 10{degrees}C), followed by elevated pCO2 (+2204 {micro}atm, at 3045 {micro}atm) during winter months. Male gametes were more developed after elevated temperature exposure and less developed after high pCO2 exposure, but there was no impact on female gametes or sex ratios. Oysters previously exposed to elevated winter temperature released larvae earlier, regardless of pCO2 exposure. Those exposed to elevated winter temperature as a sole treatment released more larvae on a daily basis, but when also exposed to high pCO2 there was no effect. These combined results indicate that elevated winter temperature accelerates O. lurida spermatogenesis, resulting in earlier larval release and increased production, with elevated pCO2 exposure negating effects of elevated temperature. Altered recruitment patterns may therefore follow warmer winters due to precocious spawning, but these effects may be masked by coincidental high pCO2. Offspring were reared in common conditions for one year, then deployed for three months in four estuarine bays with distinct environmental conditions. Offspring of parents exposed to elevated pCO2 had higher survival rates in two of the four bays. This carryover effect demonstrates that parental conditions can have substantial ecologically relevant impacts that should be considered when predicting impacts of environmental change. Furthermore, Olympia oysters may be more resilient in certain environments when progenitors are pre-conditioned in stressful conditions. Combined with other recent studies, our work suggests that the Olympia may be more equipped than other oysters for the challenge of a changing ocean.

physiology↗

bioRxiv2018

Characterization of Pacific oyster (Crassostrea gigas) proteomic response to natural environmental differences

Global climate change is rapidly altering coastal marine ecosystems important for food production. A comprehensive understanding of how organisms will respond to these complex environmental changes can come only from observing and studying species within their natural environment. To this end, the effects of environmental drivers -- pH, dissolved oxygen content, salinity, and temperature -- on Pacific oyster (Crassostrea gigas) physiology were evaluated in an outplant experiment. Sibling juvenile oysters were outplanted to eelgrass and unvegetated habitat at five different estuarine sites within the Acidification Nearshore Monitoring Network in Washington State, USA to evaluate how regional environmental drivers influence molecular physiology. Within each site, we also determined if eelgrass presence that buffered pH conditions changed the oysters expressed proteome. A novel, two-step, gel-free proteomic approach was used to identify differences in protein abundance in C. gigas ctenidia tissue after a 29 day outplant by 1) identifying proteins in a data independent acquisition survey step and 2) comparing relative quantities of targeted environmental response proteins using selected reaction monitoring. While there was no difference in protein abundance detected between habitats or among sites within Puget Sound, C. gigas outplanted at Willapa Bay had significantly higher abundances of antioxidant enzymes and molecular chaperones. Environmental factors at Willapa Bay, such as higher average temperature, may have driven this protein abundance pattern. These findings generate a suite of new hypotheses for lab and field experiments to compare the effects of regional conditions on physiological responses of marine invertebrates.

ecology↗

bioRxiv2018

Pacific geoduck (Panopea generosa) resilience to natural pH variation

Pacific geoduck aquaculture is a growing industry, however, little is known about how geoduck respond to varying environmental conditions, or how the industry will fare under projected climate conditions. To understand how geoduck production may be impacted by low pH associated with ocean acidification, multi-faceted environmental heterogeneity needs to be included to understand species and community responses. In this study, eelgrass habitats and environmental heterogeneity across four estuarine bays were leveraged to examine low pH effects on geoduck under different natural regimes, using targeted proteomics to assess physiology. Juvenile geoduck were deployed in eelgrass and adjacent unvegetated habitats for 30 days while pH, temperature, dissolved oxygen, and salinity were monitored. Across the four bays, pH was lower in unvegetated habitats compared to eelgrass habitats. However this did not impact geoduck growth, survival, or proteomic abundance patterns in gill tissue. Temperature and dissolved oxygen differences across all locations corresponded to differences in growth and targeted protein abundance patterns. Specifically, three protein abundance levels (trifunctional-enzyme {beta}-subunit, puromycin-sensitive aminopeptidase, and heat shock protein 90-) and shell growth positively correlated with dissolved oxygen variability and inversely correlated with mean temperature. These results demonstrate that geoduck may be resilient to low pH in a natural setting, but other abiotic factors (i.e. temperature, dissolved oxygen variability) may have a greater influence on geoduck physiology. In addition this study contributes to the understanding of how eelgrass patches influences water chemistry.

physiology↗