A systems biology approach reveals the role of a novel methyltransferase in response to chemical stress and lipid homeostasis

Using small molecule probes to understand gene function is an attractive approach that allows functional characterization of genes that are dispensable in standard laboratory conditions and provides insight into the mode of action of these compounds. Using chemogenomic assays we previously identified yeast Crg1, an uncharacterized SAM-dependent methyltransferase, as a novel interactor of the protein phosphatase inhibitor cantharidin. In this study we used a combinatorial approach that exploits contemporary high-throughput techniques available in Saccharomyces cerevisiae combined with rigorous biological follow-up to characterize the interaction of Crg1 with cantharidin. Biochemical analysis of this enzyme followed by a systematic analysis of the interactome and lipidome of CRG1 mutants revealed that Crg1, a stress-responsive SAM-dependent methyltransferase, methylates cantharidin in vitro. Chemogenomic assays uncovered that lipid-related processes are essential for cantharidin resistance in cells sensitized by deletion of the CRG1 gene. Lipidome-wide analysis of mutants further showed that cantharidin induces alterations in glycerophospholipid and sphingolipid abundance in a Crg1-dependent manner. We propose that Crg1 is a small molecule methyltransferase important for maintaining lipid homeostasis in response to drug perturbation. This approach demonstrates the value of combining chemical genomics with other systems-based methods for characterizing proteins and elucidating previously unknown mechanisms of action of small molecule inhibitors.     

A method to construct confidence interval for expected response to multi-trait selection

Summary Confidence intervals are constructed for the expected responses to three types of multi-trait selection. The influence of numbers of replicates and genotypes used in a progeny test experiment on the precision of response of multi-trait selection is discussed based on the structure of the established intervals. Special attention is paid to the characteristics of the intervals constructed for the conventional least square selection indices.     

A novel proteomic approach reveals a role for Mg-protoporphyrin IX in response to oxidative stress

The presence of genes encoding organellar proteins in different cellular compartments necessitates a tight coordination of expression by the different genomes of the eukaryotic cell. This coordination of gene expression is achieved by organelle-to-nucleus communication. Stress-induced perturbations of the tetrapyrrole pathway trigger large changes in nuclear gene expression. In order to investigate whether the tetrapyrrole Mg-ProtoIX itself is an important part of plastid-to-nucleus communication, we used an affinity column containing Mg-ProtoIX covalently linked to an Affi-Gel matrix. The proteins that bound to Mg-ProtoIX were analyzed by sodium dodecyl sulfate polyacrylamide gel electrophoresis combined with nano liquid chromatography-mass spectrometry (MS)/MS. Thus, we present a novel proteomic approach to address the mechanisms involved in cellular signaling and we identified interactions between Mg-ProtoIX and a large number of proteins associated with oxidative stress responses. Our approach revealed an interaction between Mg-ProtoIX and the heat shock protein 90-type protein, HSP81-2 suggesting that a regulatory complex including HSP90 proteins and tetrapyrroles controlling gene expression is evolutionarily conserved between yeast and plants. In addition, our list of putative Mg-ProtoIX-binding proteins demonstrated that binding of tetrapyrroles does not depend on a specific amino acid motif but possibly on a specific fold of the protein.     

Factors affecting the evolution of bleaching resistance in corals

We present a mathematical model of coevolutionary interactions between partners in a coral-algae mutualistic symbiosis. Our goal is to better understand factors affecting the potential evolution of bleaching resistance in corals in response to increased average sea temperatures. We explore the evolutionary consequences of four factors: (i) trade-offs among fitness components, (ii) different proximate mechanisms of coral bleaching, (iii) the genetic determination of bleaching resistance, and (iv) the mode of sexual reproduction. We show that traits in mutualistic symbioses, such as thermal tolerance in corals, are potentially subject to novel kinds of evolutionary constraints and that these constraints are mediated by ecological dynamics. We also show that some proximate mechanisms of bleaching yield faster evolutionary responses to temperature stress and that the nature of interspecific control of bleaching resistance and the mode of sexual reproduction interact to strongly influence the rate of spread of resistance alleles. These qualitative theoretical results highlight important future directions for empirical research in order to quantify the potential for coral reefs to evolve resistance to thermal stress.     

Susceptibility of central Red Sea corals during a major bleaching event

A major coral bleaching event occurred in the central Red Sea near Thuwal, Saudi Arabia, in the summer of 2010, when the region experienced up to 10–11 degree heating weeks. We documented the susceptibility of various coral taxa to bleaching at eight reefs during the peak of this thermal stress. Oculinids and agaricids were most susceptible to bleaching, with up to 100 and 80 % of colonies of these families, respectively, bleaching at some reefs. In contrast, some families, such as mussids, pocilloporids, and pectinids showed low levels of bleaching (<20 % on average). We resurveyed the reefs 7 months later to estimate subsequent mortality. Mortality was highly variable among taxa, with some taxa showing evidence of full recovery and some (e.g., acroporids) apparently suffering nearly complete mortality. The unequal mortality among families resulted in significant change in community composition following the bleaching. Significant factors in the likelihood of coral bleaching during this event were depth of the reef and distance of the reef from shore. Shallow reefs and inshore reefs had a higher prevalence of bleaching. This bleaching event shows that Red Sea reefs are subject to the same increasing pressures that reefs face worldwide. This study provides a quantitative, genus-level assessment of the vulnerability of various coral groups from within the Red Sea to bleaching and estimates subsequent mortality. As such, it can provide valuable insights into the future for reef communities in the Red Sea.     

Skeletal records of community-level bleaching in Porites corals from Palau

Tropical Pacific sea surface temperature is projected to rise an additional 2–3 °C by the end of this century, driving an increase in the frequency and intensity of coral bleaching. With significant global coral reef cover already lost due to bleaching-induced mortality, efforts are underway to identify thermally tolerant coral communities that might survive projected warming. Massive, long-lived corals accrete skeletal bands of anomalously high density in response to episodes of thermal stress. These “stress bands” are potentially valuable proxies for thermal tolerance, but to date their application to questions of community bleaching history has been limited. Ecological surveys recorded bleaching of coral communities across the Palau archipelago during the 1998 and 2010 warm events. Between 2011 and 2015, we extracted skeletal cores from living Porites colonies at 10 sites spanning barrier reef and lagoon environments and quantified the proportion of stress bands present in each population during bleaching years. Across Palau, the prevalence of stress bands tracked the severity of thermal stress, with more stress bands occurring in 1998 (degree heating weeks = 13.57 °C-week) than during the less severe 2010 event (degree heating weeks = 4.86 °C-week). Stress band prevalence also varied by reef type, as more corals on the exposed barrier reef formed stress bands than did corals from sheltered lagoon environments. Comparison of Porites stress band prevalence with bleaching survey data revealed a strong correlation between percent community bleaching and the proportion of colonies with stress bands in each year. Conversely, annual calcification rates did not decline consistently during bleaching years nor did annually resolved calcification histories always track interannual variability in temperature. Our data suggest that stress bands in massive corals contain valuable information about spatial and temporal trends in coral reef bleaching and can aid in conservation efforts to identify temperature-tolerant coral reef communities.

     

A cytomic approach reveals population heterogeneity of Cupriavidus necator in response to harmful phenol concentrations

The understanding of functions of cells within microbial populations or communities is certainly needed for existing and novel cytomic approaches which grip the individual scale. Population behaviour results from single cell performances and is caused by the individual genetic pool, history, life cycle states and microenvironmental surroundings. Mimicking natural impaired environments, the paper shows that the Gram-negative Betaproteobacterium Cupriavidus necator dramatically altered its population heterogeneity in response to harmful phenol concentrations. Multiparametric flow cytometry was used to follow variations in structural cellular parameters like chromosome contents and storage materials. The functioning of these different cell types was resolved by ensuing proteomics after the cells' spatial separation by cell sorting, finding 11 proteins changed in their expression profile, among them elongation factor Tu and the trigger factor. At least one third of the individuals clearly underwent starving states; however, simultaneously these cells prepared themselves for entering the life cycle again. Using cytomics to recognise individual structure and function on the microbial scale represents an innovative technical design to describe the complexity of such systems, overcoming the disadvantage of small cell volumes and, thus, to resolve bacterial strategies to survive harmful environments by altering population heterogeneity.     

Coral bleaching response index: a new tool to standardize and compare susceptibility to thermal bleaching

As coral bleaching events become more frequent and intense, our ability to predict and mitigate future events depends upon our capacity to interpret patterns within previous episodes. Responses to thermal stress vary among coral species; however the diversity of coral assemblages, environmental conditions, assessment protocols, and severity criteria applied in the global effort to document bleaching patterns creates challenges for the development of a systemic metric of taxon‐specific response. Here, we describe and validate a novel framework to standardize bleaching response records and estimate their measurement uncertainties. Taxon‐specific bleaching and mortality records (2036) of 374 coral taxa (during 1982–2006) at 316 sites were standardized to average percent tissue area affected and a taxon‐specific bleaching response index (taxon‐BRI) was calculated by averaging taxon‐specific response over all sites where a taxon was present. Differential bleaching among corals was widely variable (mean taxon‐BRI = 25.06 ± 18.44%, ±SE). Coral response may differ because holobionts are biologically different (intrinsic factors), they were exposed to different environmental conditions (extrinsic factors), or inconsistencies in reporting (measurement uncertainty). We found that both extrinsic and intrinsic factors have comparable influence within a given site and event (60% and 40% of bleaching response variance of all records explained, respectively). However, when responses of individual taxa are averaged across sites to obtain taxon‐BRI, differential response was primarily driven by intrinsic differences among taxa (65% of taxon‐BRI variance explained), not conditions across sites (6% explained), nor measurement uncertainty (29% explained). Thus, taxon‐BRI is a robust metric of intrinsic susceptibility of coral taxa. Taxon‐BRI provides a broadly applicable framework for standardization and error estimation for disparate historical records and collection of novel data, allowing for unprecedented accuracy in parameterization of mechanistic and predictive models and conservation plans.     

The effect of species and colony size on the bleaching response of reef-building corals in the Florida Keys during the 2005 mass bleaching event

Understanding the variation in coral bleaching response is necessary for making accurate predictions of population changes and the future state of reefs in a climate of increasing thermal stress events. Individual coral colonies, belonging to inshore patch reef communities of the Florida Keys, were followed through the 2005 mass bleaching event. Overall, coral bleaching patterns followed an index of accumulated thermal stress more closely than in situ temperature measurements. Eight coral species (Colpophyllia natans, Diploria strigosa, Montastraea cavernosa, M. faveolata, Porites astreoides, P. porites, Siderastrea siderea, and Stephanocoenia intersepta), representing >90% of the coral colonies studied, experienced intense levels of bleaching, but responses varied. Bleaching differed significantly among species: Colpophyllia natans and Diploria strigosa were most susceptible to thermal stress, while Stephanocoenia intersepta was the most tolerant. For colonies of C. natans, M. faveolata, and S. siderea, larger colonies experienced more extensive bleaching than smaller colonies. The inshore patch reef communities of the Florida Keys have historically been dominated by large colonies of Montastraea sp. and Colpophyllia natans. These results provide evidence that colony-level differences can affect bleaching susceptibility in this habitat and suggest that the impact of future thermal stress events may be biased toward larger colonies of dominant reef-building species. Predicted increases in the frequency of mass bleaching and subsequent mortality may therefore result in significant structural shifts of these ecologically important communities.     

Photophysiological stress in scleractinian corals in response to short-term sedimentation

Effects of short-term sedimentation on common coastal coral species were investigated in laboratory and field experiments on the Great Barrier Reef (GBR) using pulse-amplitude modulated (PAM) chlorophyll fluorometry. In the laboratory, changes in maximal quantum yields of photosystem II (F_v/F_m) in Montipora peltiformis were examined in response to the amount of sedimentation (79-234 mg cm⁻²) and duration of exposure (0-36 h). In control colonies, F_v/F_m ranged from 0.67 to 0.71, and did not show any temporal trend, while maximum yields of sediment-covered fragments declined steadily and reached levels below 0.1 in most colonies after 36 h coverage. Maximal quantum yield in M. peltiformis declined linearly in relation to both the amount of sediment deposited per unit surface area and the duration of exposure. Zooxanthellae densities and chlorophyll concentrations per unit area of sediment-treated corals decreased in the same manner, however, their responses were not quite as strong as the changes in F_v/F_m. Within the ranges measured, sedimentation stress of colonies exposed to large amounts of sediment for short periods of time was similar to that exposed to low amounts of sediments for prolonged periods of time. Colonies were recovered from short-term, or low-level, sedimentation within <36 h, whereas long-term exposure, or high levels of sedimentation, killed exposed colony parts. Field experiments comparing susceptibilities of common coastal coral species towards sedimentation showed significant reductions in effective quantum yields (ΔF/F_m′) in 9 out of 12 common coastal species after 22 h of exposure. Three out of twelve investigated species were not affected by the experimental application of sediments (Galaxea fascicularis, Fungia crassa, and Pectinia lactuca). Our results suggest that anthropogenic sediment deposition can negatively affect the photosynthetic activity of zooxanthellae and thus the viability of corals. However, the results also showed the ability of corals to compartmentalise sedimentation stress, as the photosynthetic activity only from tissues directly underneath the sediment declined, whereas that of adjacent clean tissues did not change measurably.     

Photoinhibition, bleaching susceptibility and mortality in two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata, in response to thermal and light stresses

In the present study, we examined the effect of thermal stress on the photoinhibitory light threshold in a bleaching susceptible (Stylophora pistillata) and a bleaching resistant (Platygyra ryukyuensis) coral. Four light (0, 110, 520, 1015 micromol quantam(-2)s(-1)) and three temperature (26, 32 and 34 degrees C) conditions were used over a 3-h period, followed by 24- and 48-h recovery periods at approximately 21 degrees C under dim light. Dynamic photoinhibition could be detected in both P. ryukyuensis and S. pistillata under 520 and 1015 micromol quantam(-2)s(-1) at 26 degrees C and under 110 micromol quantam(-2)s(-1) at 32 degrees C only in S. pistillata. Chronic photoinhibition was recorded under 520 and 1015 micromol quantam(-2)s(-1) at 34 degrees C in P. ryukyuensis, and under 1015 micromol quantam(-2)s(-1) at 32 degrees C and under all light levels at 34 degrees C in S. pistillata. These results show that high temperature reduced the threshold light intensity for photoinhibition differently in two corals with different bleaching susceptibilities under thermal stress. No visual paling and mortality in P. ryukyuensis was observed at any treatment, even in chronically photoinhibited specimens, while paling and high mortality of S. pistillata was noted in all treatments, apart from samples at 26 degrees C. These observations suggest a potential role of the host in differential bleaching and mortality determination.     

Taking a systems approach to ecological systems

Increasingly, there is interest in a systems‐level understanding of ecological problems, which requires the evaluation of more complex, causal hypotheses. In this issue of the Journal of Vegetation Science, Soliveres et al. use structural equation modeling to test a causal network hypothesis about how tree canopies affect understorey communities. Historical analysis suggests structural equation modeling has been under‐utilized in ecology.     

A multi-trait,field-based examination of personality in a semi-aquatic turtle

Studies documenting and quantifying personality traits are common in animal behavior. Such studies often consider the nature of individual variation and personality as correlated with a variety of natural history, physiological, or ecological traits, and therefore consider the importance of personality for strategies in wild systems. Though such studies have contributed markedly to our understanding of the important aspects of personality that may covary with a variety of factors that might affect fitness, much of the research on animal personalities is taxonomically limited. To supplement and compliment the laboratory study of reptile personality, we examined the patterns of multiple personality traits in wild Eastern painted turtles (Chrysemys picta) in the field. We examined patterns of aggression, sociability, and boldness across these traits in different contexts in 103 adult, wild-caught turtles. We found strong correlations both within and among the focal behavioral axes, representing robust evidence for personality in this species. Specifically, we found strong relationships among many measures of aggression, as well as relationships between aggression and our measures of boldness. Finally, we note a tendency for sociability in our turtles, with animals scoring high on sociability showing lower tendency toward aggression. Overall, our study provides robust evidence for correlated suites of behavioral traits, or personality, in a semi-aquatic turtle surveyed in the wild. Future work should continue to expand the range of traits examined to more fully consider the ecological consequences of variation in personality in this and similar species.     

A systems approach to prion disease

Prions cause transmissible neurodegenerative diseases and replicate by conformational conversion of normal benign forms of prion protein (PrP^C) to disease‐causing PrP^Sc isoforms. A systems approach to disease postulates that disease arises from perturbation of biological networks in the relevant organ. We tracked global gene expression in the brains of eight distinct mouse strain–prion strain combinations throughout the progression of the disease to capture the effects of prion strain, host genetics, and PrP concentration on disease incubation time. Subtractive analyses exploiting various aspects of prion biology and infection identified a core of 333 differentially expressed genes (DEGs) that appeared central to prion disease. DEGs were mapped into functional pathways and networks reflecting defined neuropathological events and PrP^Sc replication and accumulation, enabling the identification of novel modules and modules that may be involved in genetic effects on incubation time and in prion strain specificity. Our systems analysis provides a comprehensive basis for developing models for prion replication and disease, and suggests some possible therapeutic approaches.