scholarly journals Elucidating gene expression adaptation of phylogenetically divergent coral holobionts under heat stress

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Viridiana Avila-Magaña ◽  
Bishoy Kamel ◽  
Michael DeSalvo ◽  
Kelly Gómez-Campo ◽  
Susana Enríquez ◽  
...  

AbstractAs coral reefs struggle to survive under climate change, it is crucial to know whether they have the capacity to withstand changing conditions, particularly increasing seawater temperatures. Thermal tolerance requires the integrative response of the different components of the coral holobiont (coral host, algal photosymbiont, and associated microbiome). Here, using a controlled thermal stress experiment across three divergent Caribbean coral species, we attempt to dissect holobiont member metatranscriptome responses from coral taxa with different sensitivities to heat stress and use phylogenetic ANOVA to study the evolution of gene expression adaptation. We show that coral response to heat stress is a complex trait derived from multiple interactions among holobiont members. We identify host and photosymbiont genes that exhibit lineage-specific expression level adaptation and uncover potential roles for bacterial associates in supplementing the metabolic needs of the coral-photosymbiont duo during heat stress. Our results stress the importance of integrative and comparative approaches across a wide range of species to better understand coral survival under the predicted rise in sea surface temperatures.

2020 ◽  
Vol 111 (6) ◽  
pp. 539-547
Author(s):  
Sumaetee Tangwancharoen ◽  
Brice X Semmens ◽  
Ronald S Burton

Abstract Geographic variation in environmental temperature can select for local adaptation among conspecific populations. Divergence in gene expression across the transcriptome is a key mechanism for evolution of local thermal adaptation in many systems, yet the genetic mechanisms underlying this regulatory evolution remain poorly understood. Here we examine gene expression in 2 locally adapted Tigriopus californicus populations (heat tolerant San Diego, SD, and less tolerant Santa Cruz, SC) and their F1 hybrids during acute heat stress response. Allele-specific expression (ASE) in F1 hybrids was used to determine cis-regulatory divergence. We found that the number of genes showing significant allelic imbalance increased under heat stress compared to unstressed controls. This suggests that there is significant population divergence in cis-regulatory elements underlying heat stress response. Specifically, the number of genes showing an excess of transcripts from the more thermal tolerant (SD) population increased with heat stress while that number of genes with an SC excess was similar in both treatments. Inheritance patterns of gene expression also revealed that genes displaying SD-dominant expression phenotypes increase in number in response to heat stress; that is, across loci, gene expression in F1’s following heat stress showed more similarity to SD than SC, a pattern that was absent in the control treatment. The observed patterns of ASE and inheritance of gene expression provide insight into the complex processes underlying local adaptation and thermal stress response.


2021 ◽  
Vol 118 (5) ◽  
pp. e2022653118 ◽  
Author(s):  
Nils Rädecker ◽  
Claudia Pogoreutz ◽  
Hagen M. Gegner ◽  
Anny Cárdenas ◽  
Florian Roth ◽  
...  

Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral–algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral–algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral–algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.


2021 ◽  
Author(s):  
Jinding Liu ◽  
Fei Yin ◽  
Kun Lang ◽  
Wencai Jie ◽  
Suxu Tan ◽  
...  

Abstract Background: RNA-seq has become a standard tool in biology and has produced large and diverse transcriptomic datasets for users to explore fungal expression regulation. Fungal alternative splicing, which is attracting increasing attention because of evolutionary adaptations to changing external conditions has not been thoroughly investigated in previous studies, unlike that of animals and plants. However, the analyses of RNA-seq datasets are made difficult by the heterogeneity of study design and complex bioinformatics approaches. Comprehensive analyses of these published datasets should contribute new insights into fungal expression regulation.Results: We have developed a web-based platform called FungiExp hosting fungal gene expression levels and alternative splicing profiles in 35,821 curated RNA-seq experiments from 220 species. It allows users to perform retrieval via diverse terms and sequence similarity. Moreover, users can customize experimental groups to perform differential and specific expression analyses. The wide range of data visualization is an additional important feature that should help users intuitively understand retrieval and analysis results.Conclusions: With its uniform data processing, easy data accessibility, convenient retrieval, and analysis functions, FungiExp is a valuable resource and tool that allows users to (re)use published RNA-seq datasets. It is accessible at http://bioinfo.njau.edu.cn/fungiExp.


2020 ◽  
Author(s):  
Amanda Williams ◽  
Eric N. Chiles ◽  
Dennis Conetta ◽  
Jananan S. Pathmanathan ◽  
Phillip A. Cleves ◽  
...  

SummaryCoral reef systems are under global threat due to warming and acidifying oceans1. Understanding the response of the coral holobiont to environmental change is crucial to aid conservation efforts. The most pressing problem is “coral bleaching”, usually precipitated by prolonged thermal stress that disrupts the algal symbiosis sustaining the holobiont2,3. We used metabolomics to understand how the coral holobiont metabolome responds to heat stress with the goal of identifying diagnostic markers prior to bleaching onset. We studied the heat tolerant Montipora capitata and heat sensitive Pocillopora acuta coral species from the Hawaiian reef system in Kāne’ohe Bay, O’ahu. Untargeted LC-MS analysis uncovered both known and novel metabolites that accumulate during heat stress. Among those showing the highest differential accumulation were a variety of co-regulated dipeptides present in both species. The structures of four of these compounds were determined (Arginine-Glutamine, Lysine-Glutamine, Arginine-Valine, and Arginine-Alanine). These dipeptides also showed differential accumulation in symbiotic and aposymbiotic (alga free) individuals of the sea anemone model Aiptasia4, suggesting their animal provenance and algal symbiont related function. Our results identify a suite of metabolites associated with thermal stress that can be used to diagnose coral health in wild samples.


2020 ◽  
Vol 8 (8) ◽  
pp. 1227
Author(s):  
Rosa Celia Poquita-Du ◽  
Yi Le Goh ◽  
Danwei Huang ◽  
Loke Ming Chou ◽  
Peter A. Todd

The ability of corals to withstand changes in their surroundings is a critical survival mechanism for coping with environmental stress. While many studies have examined responses of the coral holobiont to stressful conditions, its capacity to reverse responses and recover when the stressor is removed is not well-understood. In this study, we investigated among-colony responses of Pocillopora acuta from two sites with differing distance to the mainland (Kusu (closer to the mainland) and Raffles Lighthouse (further from the mainland)) to heat stress through differential expression analysis of target genes and quantification of photophysiological metrics. We then examined how these attributes were regulated after the stressor was removed to assess the recovery potential of P. acuta. The fragments that were subjected to heat stress (2 °C above ambient levels) generally exhibited significant reduction in their endosymbiont densities, but the extent of recovery following stress removal varied depending on natal site and colony. There were minimal changes in chl a concentration and maximum quantum yield (Fv/Fm, the proportion of variable fluorescence (Fv) to maximum fluorescence (Fm)) in heat-stressed corals, suggesting that the algal endosymbionts’ Photosystem II was not severely compromised. Significant changes in gene expression levels of selected genes of interest (GOI) were observed following heat exposure and stress removal among sites and colonies, including Actin, calcium/calmodulin-dependent protein kinase type IV (Camk4), kinesin-like protein (KIF9), and small heat shock protein 16.1 (Hsp16.1). The most responsive GOIs were Actin, a major component of the cytoskeleton, and the adaptive immune-related Camk4 which both showed significant reduction following heat exposure and subsequent upregulation during the recovery phase. Our findings clearly demonstrate specific responses of P. acuta in both photophysiological attributes and gene expression levels, suggesting differential capacity of P. acuta corals to tolerate heat stress depending on the colony, so that certain colonies may be more resilient than others.


Biomolecules ◽  
2020 ◽  
Vol 10 (5) ◽  
pp. 701 ◽  
Author(s):  
Areej Abu Rmaileh ◽  
Balakrishnan Solaimuthu ◽  
Mayur Tanna ◽  
Anees Khatib ◽  
Michal Ben Yosef ◽  
...  

Cancer-dependent metabolic rewiring is often manifested by selective expression of enzymes essential for the transformed cells’ viability. However, the metabolic variations between normal and transformed cells are not fully characterized, and therefore, a systematic analysis will result in the identification of unknown cellular mechanisms crucial for tumorigenesis. Here, we applied differential gene expression transcriptome analysis to examine the changes in metabolic gene profiles between a wide range of normal tissues and cancer samples. We found that, in contrast to normal tissues which exhibit a tissue-specific expression profile, cancer samples are more homogenous despite their diverse origins. This similarity is due to a “proliferation metabolic signature” (PMS), composed of 158 genes (87 upregulated and 71 downregulated gene sets), where 143 are common to all proliferative cells but 15 are cancer specific. Intriguingly, the PMS gene set is enriched for genes encoding rate-limiting enzymes, and its upregulated set with genes associated with poor patient outcome and essential genes. Among these essential genes is ribulose-5-phosphate-3-epimerase (RPE), which encodes a pentose phosphate pathway enzyme and whose role in cancer is still unclear. Collectively, we identified a set of metabolic genes that can serve as novel cancer biomarkers and potential targets for drug development.


2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Shu-Hong Lin ◽  
Rohit Thakur ◽  
Mitchell J. Machiela

AbstractGenome-wide association studies have identified thousands of genetic susceptibility loci associated with cancer as well as other traits and diseases. Mapping germline variation in identified genetic susceptibility regions to alterations in nearby gene expression nominates candidate genes potentially related to disease risk for further functional investigation. We developed LDexpress as an online resource that integrates population-specific linkage disequilibrium data from the 1000 Genomes (1000G) project and tissue-specific expression data from the Genotype-Tissue Expression project to better study regional germline variation impacting gene expression. LDexpress is a publicly available web tool designed to be easy to use, flexible to conduct a wide range of variant queries, and quick to efficiently investigate dozens of query variants across multiple tissue types. We demonstrate the utility of LDexpress using example genomic queries and anticipate this tool will accelerate understanding of disease etiology by uncovering associations of regional germline variation to nearby gene expression.


2017 ◽  
Author(s):  
Raúl A. González-Pech ◽  
Sergio Vargas ◽  
Warren R. Francis ◽  
Gert Wörheide

AbstractOcean acidification is considered as one of the major threats for coral reefs at a global scale. Marine calcifying organisms, including stony corals, are expected to be the most affected by the predicted decrease of the surface water pH at the end of the century. The severity of the impacts on coral reefs remains as matter of controversy. Although previous studies have explored the physiological response of stony corals to changes in pH, the response of the holobiont (i.e. the coral itself plus its symbionts) remains largely unexplored. In the present study, we assessed the changes in overall gene expression of the coral Montipora digitata and its microalgal symbionts after a short (three days) and a longer (42 days) exposure to low pH (7.6). The short-term exposure to low pH caused small differences in the expression level of the host, impacting mostly genes associated with stress response in other scleractinians. Resilience to Acidification of a Coral Holobiont Longer exposure to low pH resulted in no significant changes in gene expression of the coral host. Gene expression in the eukaryotic symbionts remained unaltered at both exposure times. Our findings suggest resilience, in terms of gene expression, of the Montipora digitata holobiont to pH decrease, as well as capability to acclimatize to extended periods of exposure to low pH.


2021 ◽  
Vol 118 (19) ◽  
pp. e2023298118
Author(s):  
Romain Savary ◽  
Daniel J. Barshis ◽  
Christian R. Voolstra ◽  
Anny Cárdenas ◽  
Nicolas R. Evensen ◽  
...  

Corals from the northern Red Sea and Gulf of Aqaba exhibit extreme thermal tolerance. To examine the underlying gene expression dynamics, we exposed Stylophora pistillata from the Gulf of Aqaba to short-term (hours) and long-term (weeks) heat stress with peak seawater temperatures ranging from their maximum monthly mean of 27 °C (baseline) to 29.5 °C, 32 °C, and 34.5 °C. Corals were sampled at the end of the heat stress as well as after a recovery period at baseline temperature. Changes in coral host and symbiotic algal gene expression were determined via RNA-sequencing (RNA-Seq). Shifts in coral microbiome composition were detected by complementary DNA (cDNA)-based 16S ribosomal RNA (rRNA) gene sequencing. In all experiments up to 32 °C, RNA-Seq revealed fast and pervasive changes in gene expression, primarily in the coral host, followed by a return to baseline gene expression for the majority of coral (>94%) and algal (>71%) genes during recovery. At 34.5 °C, large differences in gene expression were observed with minimal recovery, high coral mortality, and a microbiome dominated by opportunistic bacteria (including Vibrio species), indicating that a lethal temperature threshold had been crossed. Our results show that the S. pistillata holobiont can mount a rapid and pervasive gene expression response contingent on the amplitude and duration of the thermal stress. We propose that the transcriptomic resilience and transcriptomic acclimation observed are key to the extraordinary thermal tolerance of this holobiont and, by inference, of other northern Red Sea coral holobionts, up to seawater temperatures of at least 32 °C, that is, 5 °C above their current maximum monthly mean.


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