* Indicates student co-author
Poo, Cindi, Gautam Agarwal, Niccolò Bonacci, and Zachary F. Mainen. “Spatial Maps in Piriform Cortex During Olfactory Navigation.” Nature, vol. 601, 2021, pp. 595-599.
Abstract: Odours are a fundamental part of the sensory environment used by animals to guide behaviours such as foraging and navigation. Primary olfactory (piriform) cortex is thought to be the main cortical region for encoding odour identity. Here, using neural ensemble recordings in freely moving rats performing an odour-cued spatial choice task, we show that posterior piriform cortex neurons carry a robust spatial representation of the environment. Piriform spatial representations have features of a learned cognitive map, being most prominent near odour ports, stable across behavioural contexts and independent of olfactory drive or reward availability. The accuracy of spatial information carried by individual piriform neurons was predicted by the strength of their functional coupling to the hippocampal theta rhythm. Ensembles of piriform neurons concurrently represented odour identity as well as spatial locations of animals, forming an odour-place map. Our results reveal a function for piriform cortex in spatial cognition and suggest that it is well-suited to form odour-place associations and guide olfactory-cued spatial navigation
Ezenwa, Vanessa O., Sarah A. Budischak, Peter Buss, Mauricio Seguel, Gordon Luikart, Anna E. Jolles, and Kaori Sakamoto. “Natural Resistance to Worms Exacerbates Bovine Tuberculosis Severity Independently of Worm Coinfection.” Proceedings of the National Academy of Sciences of the United States of America, vol. 118, issue 3, 2021, e2015080118.
Abstract: Pathogen interactions arising during coinfection can exacerbate disease severity, for example when the immune response mounted against one pathogen negatively affects defense of another. It is also possible that host immune responses to a pathogen, shaped by historical evolutionary interactions between host and pathogen, may modify host immune defenses in ways that have repercussions for other pathogens. In this case, negative interactions between two pathogens could emerge even in the absence of concurrent infection. Parasitic worms and tuberculosis (TB) are involved in one of the most geographically extensive of pathogen interactions, and during coinfection worms can exacerbate TB disease outcomes. Here, we show that in a wild mammal natural resistance to worms affects bovine tuberculosis (BTB) severity independently of active worm infection. We found that worm-resistant individuals were more likely to die of BTB than were nonresistant individuals, and their disease progressed more quickly. Anthelmintic treatment moderated, but did not eliminate, the resistance effect, and the effects of resistance and treatment were opposite and additive, with untreated, resistant individuals experiencing the highest mortality. Furthermore, resistance and anthelmintic treatment had nonoverlapping effects on BTB pathology. The effects of resistance manifested in the lungs (the primary site of BTB infection), while the effects of treatment manifested almost entirely in the lymph nodes (the site of disseminated disease), suggesting that resistance and active worm infection affect BTB progression via distinct mechanisms. Our findings reveal that interactions between pathogens can occur as a consequence of processes arising on very different timescales.
Coleman, Melissa J. “Wrens Synchronize Their Brains in Order to Sing Spectacular Duets.” Melissa Coleman interviewed by Bob McDonald. Quirks & Quarks, June 11, 2021.
Coleman, Melissa J. and Eric Fortune. “The Neuroscience of Taking Turns in a Conversation.” Scientific American, July 13, 2021.
Coleman, Melissa J., Nancy F. Day, Pamela Rivera-Parra, and Eric S. Fortune. “Neurophysical Coordination of Duet Singing.” Proceedings of the National Academy of Sciences, vol. 118, issue 23, e2018188118.
Abstract: Coordination of behavior for cooperative performances often relies on linkages mediated by sensory cues exchanged between participants. How neurophysiological responses to sensory information affect motor programs to coordinate behavior between individuals is not known. We investigated how plain-tailed wrens (Pheugopedius euophrys) use acoustic feedback to coordinate extraordinary duet performances in which females and males rapidly take turns singing. We made simultaneous neurophysiological recordings in a song control area “HVC” in pairs of singing wrens at a field site in Ecuador. HVC is a premotor area that integrates auditory feedback and is necessary for song production. We found that spiking activity of HVC neurons in each sex increased for production of its own syllables. In contrast, hearing sensory feedback produced by the bird’s partner decreased HVC activity during duet singing, potentially coordinating HVC premotor activity in each bird through inhibition. When birds sang alone, HVC neurons in females but not males were inhibited by hearing the partner bird. When birds were anesthetized with urethane, which antagonizes GABAergic (𝛾-aminobutyric acid) transmission, HVC neurons were excited rather than inhibited, suggesting a role for GABA in the coordination of duet singing. These data suggest that HVC integrates information across partners during duets and that rapid turn taking may be mediated, in part, by inhibition.
Coleman, Melissa J. and Stephanie A. White. “Basal Ganglia: Bursting with Song.” Current Biology, vol. 31, issue 12, 2021, pp. R791-R793.
Abstract: The songs of mature zebra finches are notoriously repetitious, or ‘crystallized’. Despite this stability, new work reveals that chronic pharmacologically driven bursting of cortical inputs to the basal ganglia can drive cumulative and lasting changes to multiple vocal features, including phenomena reminiscent of human stuttering.
Ferree, Elise, Ravi Sadhu*, Kennedy Holland*, and Olivia Wu*. “Vocal Coordination of Provisioning in Black Phoebes (Sayornis nigricans).” The Wilson Journal of Ornithology, vol. 113, issue 2, 2021, pp. 318-325.
Abstract: Parent birds often vocalize near the nest to communicate with each other and their young. We observed a call made by Black Phoebes (Sayornis nigricans) as they approach the nest to feed their young that has not previously been studied in this context. The Wee call is more complex than the simple call that males and females commonly make near the nest. We hypothesized that one parent makes the call when arriving at the nest with food to signal to a brooding parent to depart from the nest. Over 3 years, we collected observational data at phoebe nests by observing them once during the incubation stage and then early and late in the nestling stage. As we predicted, phoebes did not make the Wee call during the incubation stage. When individuals approached the nest with food and made the Wee call during the nestling stage, the brooding parent normally responded by leaving the nest. Additionally, the brooding bird was likely to return to the nest if the other parent made the Wee call upon departing. While vocalizations near the nest can attract predators, in phoebes these calls appear to coordinate parental care efforts.
Dalla Benetta, Elena, Omar S. Akbari, and Patrick M. Ferree. “Mechanistically Comparing Reproductive Manipulations Caused by Selfish Chromosomes and Bacterial Symbionts.” Heredity, vol. 126, 2021, pp. 707-716.
Abstract: Insects naturally harbor a broad range of selfish agents that can manipulate their reproduction and development, often leading to host sex ratio distortion. Such effects directly benefit the spread of the selfish agents. These agents include two broad groups: bacterial symbionts and selfish chromosomes. Recent studies have made steady progress in uncovering the cellular targets of these agents and their effector genes. Here we highlight what is known about the targeted developmental processes, developmental timing, and effector genes expressed by several selfish agents. It is now becoming apparent that: (1) the genetic toolkits used by these agents to induce a given reproductive manipulation are simple, (2) these agents target sex-specific cellular processes very early in development, and (3) in some cases, similar processes are targeted. Knowledge of the molecular underpinnings of these systems will help to solve long-standing puzzles and provide new tools for controlling insect pests.
External Grant: Ferree, Patrick, Principal Investigator. “Role of the Haploidizer Gene in Genome Elimination by a Selfish B Chromosome.” National Science Foundation, 2021-2025, $923,538, award 2127460.
Abstract: This project aims to elucidate how selfish genetic elements disrupt normal genetic inheritance patterns. A certain class of selfish elements—B chromosomes—are pervasive among plants and animals. In certain cases, B chromosomes cause harmful effects to reproduction and extreme sex ratio distortion. In the jewel wasp, Nasonia vitripennis, one such B chromosome destroys the part of the genome that comes from the father, resulting in all-male broods of progeny carrying hereditary material only from the mother and the B chromosome. Recent work has revealed a toxin-like gene expressed by this B chromosome; this gene is needed for the B chromosome’s genome elimination activity, making it the only gene known to underlie selfish chromosome behavior in any organism. This research aims to uncover how this gene functions at the molecular level, providing insights into how other selfish genetic elements alter inheritance patterns. The project will facilitate rigorous research training opportunities for a diverse group of undergraduate students and a postdoctoral researcher. A new laboratory-based course will be developed around one of the proposal’s aims; in this course, students will perform the research, learning the practice of science through hands-on experimentation. Students from the two-year college level will be involved in the research, helping to enhance their retention in STEM and the likelihood of their continuation to 4-year degree-granting institutions. Collectively, this work will help to train the rising STEM workforce.
Finseth, Findley R., Thomas C. Nelson, and Lila Fishman. “Selfish Chromosomal Drive Shapes Recent Centromeric Histone Evolution in Monkeyflowers.” PLoS Genetics, vol. 17, issue 4, 2021, e1009418.
Abstract: Centromeres are essential mediators of chromosomal segregation, but both centromeric DNA sequences and associated kinetochore proteins are paradoxically diverse across species. The selfish centromere model explains rapid evolution by both components via an arms-race scenario: centromeric DNA variants drive by distorting chromosomal transmission in female meiosis and attendant fitness costs select on interacting proteins to restore Mendelian inheritance. Although it is clear than centromeres can drive and that drive often carries costs, female meiotic drive has not been directly linked to selection on kinetochore proteins in any natural system. Here, we test the selfish model of centromere evolution in a yellow monkeyflower (Mimulus guttatus) population polymorphic for a costly driving centromere (D). We show that the D haplotype is structurally and genetically distinct and swept to a high stable frequency within the past 1500 years. We use quantitative genetic mapping to demonstrate that context-dependence in the strength of drive (from near-100% D transmission in interspecific hybrids to near-Mendelian in within-population crosses) primarily reflects variable vulnerability of the non-driving competitor chromosomes, but also map an unlinked modifier of drive coincident with kinetochore protein Centromere-specific Histone 3 A (CenH3A). Finally, CenH3A exhibits a recent (<1000 years) selective sweep in our focal population, implicating local interactions with D in ongoing adaptive evolution of this kinetochore protein. Together, our results demonstrate an active co-evolutionary arms race between DNA and protein components of the meiotic machinery in Mimulus, with important consequences for individual fitness and molecular divergence.
Nelson, Thomas C., Angela M. Stathos, Daniel D. Vanderpool, Findley R. Finseth, Yao-wu Yuan, and Lila Fishman. “Ancient and Recent Introgression Shape the Evolutionary History of Pollinator Adaptation and Speciation in a Model Monkeyflower Radiation (Mimulus section Erythranthe).” PLoS Genetics, vol. 17, issue 2, 2021, e1009095.
Abstract: Inferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species). Taxa within Erythranthe, particularly the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M. cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M. lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele sharing (Patterson’s D-statistic and related tests) indicate that gene tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M. lewisii and M. cardinalis. Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M. lewisii and Southern Californian M. parishii each carrying organelle genomes nested within respective sympatric M. cardinalis clades. A recent organellar transfer from M. cardinalis, an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M. parishii organelles in hybrids with M. lewisii. Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.
Hayford, Hilary A., Sarah E. Gilman, and Emily Carrington. “Tidal Cues Reduce Thermal Risk of Climate Change in a Foraging Marine Snail.” Climate Change Ecology, vol. 1, 2021, 100003.
Abstract: Accurate predictions of the effects of warming temperatures under climate change on an individual species require an accurate characterization of its current and future thermal environment. Behavioral responses to environmental heterogeneity are an important but poorly understood determinant of species’ body temperatures and thermal risks. In this paper we describe the steps necessary for determining a species’ opportunities for behavioral buffering of climate change, and provide examples using a combination of previously published studies and new results for the intertidal snail Nucella ostrina. We find that N. ostrina “current patterns of daily microhabitat selection have the potential to buffer it from warming temperatures under climate change. N. ostrina‚” foraging behavior is highly correlated with the 14.5 d semilunar tidal cycle, shielding it from both current and future thermal stress.
Nguyen, Ngan* Hongfei Chen*, Benjamin Jin*, Walker Quinn*, Conrad Tyler*, and Adam Landsberg. “Cultural Dissemination: An Agent-Based Model with Social Influence.” Journal of Artificial Societies and Social Simulation, vol. 24 , issue 4, 2021, article 5.
Abstract: We study cultural dissemination in the context of an Axelrod-like agent-based model describing the spread of cultural traits across a society, with an added element of social influence. This modification produces absorbing states exhibiting greater variation in number and size of distinct cultural regions compared to the original Axelrod model, and we identify the mechanism responsible for this amplification in heterogeneity. We develop several new metrics to quantitatively characterize the heterogeneity and geometric qualities of these absorbing states. Additionally, we examine the dynamical approach to absorbing states in both our Social Influence Model as well as the Axelrod Model, which not only yields interesting insights into the differences in behavior of the two models over time, but also provides a more comprehensive view into the behavior of Axelrod's original model. The quantitative metrics introduced in this paper have broad potential applicability across a large variety of agent-based cultural dissemination models.
Arul, Boopala, Daniel Lee*, and Sarah Marzen. “A Proposed Probabilistic Method for Distinguishing Between Delusions and Other Environmental Judgments, With Implications to Psychotherapy.” Frontiers in Psychology, 2021, 3300.
Abstract: How can individuals with schizophrenia best be equipped to distinguish delusions from accurate judgements about their environment? This study presents an approach based on the principles of Bayesian probability and presents the results of a series of tests in which a simulated observer classifies randomly generated data characteristic of a simulated environment. The complexity of the data ranges from scalars to vectors of variable lengths, and the simulated observer makes its decisions based on either perfect or imperfect models of its environment. We find that when a low-dimensional observation is considered characteristic of both real observations and delusions, the prior probabilities of any observation being real or fake are of greater importance to the final decision than the attributes of the observation. However, when an observation is high-dimensional (complex), classification accuracy tends to improve toward 100% with increasing complexity of observations, as long as the patient’s model of the world isn’t drastically inaccurate. On the contrary, when the observer’s model is sufficiently inaccurate, the accuracy rate decreases with increasing observational complexity. Overall, the results suggest applicability of the Bayesian model to the use of interventional therapy for those who suffer from psychosis.
Marzen, Sarah. “Choosing Dynamical Systems that Predict Weak Input.” Physical Review E, vol. 104, 2021, 014409.
Abstract: Somehow, our brain and other organisms manage to predict their environment. Behind this must be an input-dependent dynamical system, or recurrent neural network, whose present state reflects the history of environmental input. The design principles for prediction—in particular, what kinds of attractors allow for greater predictive capability—are still unknown. We offer some clues to design principles using an attractor picture when the environment perturbs the system’s state weakly, motivating and developing some theory for continuous-time time-varying linear reservoirs along the way. Reservoirs that inherently support only stable fixed points are generically good predictors, while reservoirs with limit cycles are good predictors for noisy periodic input.
Zhong, Weishun, Jacob M. Gold, Sarah Marzen, Jeremy L. England, and Nicole Yunger Halpern. “Machine Learning Outperforms Thermodynamics in Measuring How Well a Many-Body System Learns a Drive.” Nature, vol. 11, 2021, 9333.
Abstract: Diverse many-body systems, from soap bubbles to suspensions to polymers, learn and remember patterns in the drives that push them far from equilibrium. This learning may be leveraged for computation, memory, and engineering. Until now, many-body learning has been detected with thermodynamic properties, such as work absorption and strain. We progress beyond these macroscopic properties first defined for equilibrium contexts: We quantify statistical mechanical learning using representation learning, a machine-learning model in which information squeezes through a bottleneck. By calculating properties of the bottleneck, we measure four facets of many-body systems’ learning: classification ability, memory capacity, discrimination ability, and novelty detection. Numerical simulations of a classical spin glass illustrate our technique. This toolkit exposes self-organization that eludes detection by thermodynamic measures: Our toolkit more reliably and more precisely detects and quantifies learning by matter while providing a unifying framework for many-body learning.
Lundberg, Joyce and Donald A. McFarlane. “The Impact of Burning on the Structure and Material Composition of Bat Guano.” International Journal of Speleology, vol. 50, issue 2, 2021, pp. 189-202.
Abstract: Here we addressed the question of whether burning of guano produces a characteristic suite of morphological changes and/or unique mineralogical products. The changes observed in our experimental burning of guano (both fresh and decayed) included colour change (blackening), grain size and morphological change (grain size generally reduced, morphology rendered generally less distinct), alteration of minerals by dehydration (e.g., gypsum to anhydrite, brushite to whitlockite), and production of new minerals or compounds (e.g., augelite, bayerite, giniite, graphite, oldhamite, strontium apatite, tridymite). The key morphological feature we found that may be diagnostic of burning was severe damage to crystals from rapid dehydration (cracks and striations, leading to eventual fragmentation). The key mineralogical feature we found was production of graphite. The high temperature exotic minerals that were produced (giniite, augelite, tridymite, oldhamite) were all found not to be high temperature obligate. Evidence gleaned from the literature suggests that a great number of the minerals associated with high temperatures can also be synthesized in low temperature settings such as weathering or microbial action (exemplified in the extremely complex biology and biochemistry of decaying guano). While the presence of any one of these minerals is not diagnostic of fire, it could be argued that the suite taken as a whole is moderately strong evidence for burning. In future studies, the chemistry of carbon aromaticity may prove to be the best diagnostic test for pyrolysis. A survey of the conditions under which documented spontaneous ignition occurs leads us to conclude that spontaneous ignition of guano inside a cave is an extremely unlikely event, and any suggestion/assertion to this effect should be rigorously supported.
McFarlane, Donald A. and Joyce Lundberg. “Geochronological Implications of 210Pb and 137Cs Mobility in Cave Guano Deposits.” International Journal of Speleology, vol. 50, issue 3, 2021, pp. 239-248.
Abstract: Some recent publications on the paleo- and historical environmental interpretation of bat guano sequences have relied on 210Pb and 137Cs distribution to establish age-depth models, even when these are at odds with radiocarbon models in the lower parts of the sequence. Here, we present both field and laboratory evidence for the unpredictable mobility of lead and cesium in decomposing bat guano deposits. We suggest that 210Pb- and 137Cs-based chronologies of bat guano deposits should only be used when independently supported, for example, by a robust radiocarbon age-depth model.
Bélair, Jacques, Fahima Nekka, and John G. Milton. “Introduction to Focus Issue: Dynamical Disease: A Translational Approach.” Chaos, vol. 31, issue 6, 2021, 060401.
Abstract: The concept of Dynamical Diseases provides a framework to understand physiological control systems in pathological states due to their operating in an abnormal range of control parameters: this allows for the possibility of a return to normal condition by a redress of the values of the governing parameters. The analogy with bifurcations in dynamical systems opens the possibility of mathematically modeling clinical conditions and investigating possible parameter changes that lead to avoidance of their pathological states. Since its introduction, this concept has been applied to a number of physiological systems, most notably cardiac, hematological, and neurological. A quarter century after the inaugural meeting on dynamical diseases held in Mont Tremblant, Québec [Bélair et al., Dynamical Diseases: Mathematical Analysis of Human Illness (American Institute of Physics, Woodbury, NY, 1995)], this Focus Issue offers an opportunity to reflect on the evolution of the field in traditional areas as well as contemporary data-based methods. In 1977, Leon Glass and Michael C. Mackey introduced the idea that certain diseases, which they labeled dynamical diseases, arise when an intact physiological control system operates in a range of control parameters that leads to abnormal dynamics and human pathology. This idea was closely associated with the mathematical concept of bifurcations that can occur in dynamical systems as certain parameters are changed. This observation opened the door for “mathematicians at the bedside.” Over the last four decades, the impact of mathematical insights into human illness has been palpable. Mathematical contributions have provided important insights into the nature of many life-threatening illnesses, including cardiac and respiratory arrhythmias, epileptic seizures, periodic hematological diseases, falls in the elderly, and certain psychiatric disorders and diseases.
Gyebrószki, Gergely, Gábor Csernák, John G. Milton, and Tamás Insperger. “The Effects of Sensory Quantization and Control Torque Saturation on Human Balance Control.” Chaos, vol. 31, issue 3, 2021, 033145.
Abstract: The effect of reaction delay, temporal sampling, sensory quantization, and control torque saturation is investigated numerically for a single-degree-of-freedom model of postural sway with respect to stability, stabilizability, and control effort. It is known that reaction delay has a destabilizing effect on the balancing process: the later one reacts to a perturbation, the larger the possibility of falling. If the delay is larger than a critical value, then stabilization is not even possible. In contrast, numerical analysis showed that quantization and control torque saturation have a stabilizing effect: the region of stabilizing control gains is greater than that of the linear model. Control torque saturation allows the application of larger control gains without overcontrol while sensory quantization plays a role of a kind of filter when sensory noise is present. These beneficial effects are reflected in the energy demand of the control process. On the other hand, neither control torque saturation nor sensory quantization improves stabilizability properties. In particular, the critical delay cannot be increased by adding saturation and/or sensory quantization. Aging western societies are facing an epidemic of falling. For example, in the United States, an older adult is treated for a fall in the emergency room every 11 min, and every 19 min, an elderly person dies from a fall. Measurements of postural sway, namely, the fluctuations in the center-of-pressure (COP) while a subject stands quietly on a force platform with eyes closed, can identify those most at risk for a fall. The principle sensory input for postural sway is proprioception at the ankle joint. Since the sensory threshold for proprioception increases with aging and certain diseases that affect the nervous system (e.g., diabetic neuropathy), it has been suggested that this sensory threshold increases the risk of falling. Generalization of sensory dead zone is sensory quantization, which is a combination of a series of shifted sensory dead zones. However, mathematical and computer modeling studies suggest that sensory quantization can have stabilizing effects. Computer simulations of an inverted pendulum model for balance stabilized by time-delayed feedback are used to assess the effects of sensory quantization on control effort. The results suggest that sensory quantization can slightly decrease control effort and that this benefit increases due to the effects of sensory masking to alter quantization thresholds. These observations provide insights into the possible benefits of shoes with “noisy insoles” for reducing falling risk in elderly subjects.
Zelei, Ambrus, John Milton, Gabor Stepan, and Tamas Insperger. “Response to Perturbation During Quiet Standing Resembles Delayed State Feedback Optimized for Performance and Robustness.” Scientific Reports, vol 11, 2021, 11392.
Abstract: Postural sway is a result of a complex action–reaction feedback mechanism generated by the interplay between the environment, the sensory perception, the neural system and the musculation. Postural oscillations are complex, possibly even chaotic. Therefore fitting deterministic models on measured time signals is ambiguous. Here we analyse the response to large enough perturbations during quiet standing such that the resulting responses can clearly be distinguished from the local postural sway. Measurements show that typical responses very closely resemble those of a critically damped oscillator. The recovery dynamics are modelled by an inverted pendulum subject to delayed state feedback and is described in the space of the control parameters. We hypothesize that the control gains are tuned such that (H1) the response is at the border of oscillatory and nonoscillatory motion similarly to the critically damped oscillator; (H2) the response is the fastest possible; (H3) the response is a result of a combined optimization of fast response and robustness to sensory perturbations. Parameter fitting shows that H1 and H3 are accepted while H2 is rejected. Thus, the responses of human postural balance to “large” perturbations matches a delayed feedback mechanism that is optimized for a combination of performance and robustness.
Hessel, Anthony L., Jenna A. Monroy, and Kiisa C. Nishikawa. “Non-cross Bridge Viscoelastic Elements Contribute to Muscle Force and Work During Stretch-Shortening Cycles: Evidence from Whole Muscles and Permeabilized Fibers.” Frontiers in Physiology, vol. 12, 2021, 648019.
Abstract: The sliding filament-swinging cross bridge theory of skeletal muscle contraction provides a reasonable description of muscle properties during isometric contractions at or near maximum isometric force. However, it fails to predict muscle force during dynamic length changes, implying that the model is not complete. Mounting evidence suggests that, along with cross bridges, a Ca2+-sensitive viscoelastic element, likely the titin protein, contributes to muscle force and work. The purpose of this study was to develop a multi-level approach deploying stretch-shortening cycles (SSCs) to test the hypothesis that, along with cross bridges, Ca2+-sensitive viscoelastic elements in sarcomeres contribute to force and work. Using whole soleus muscles from wild type and mdm mice, which carry a small deletion in the N2A region of titin, we measured the activation- and phase-dependence of enhanced force and work during SSCs with and without doublet stimuli. In wild type muscles, a doublet stimulus led to an increase in peak force and work per cycle, with the largest effects occurring for stimulation during the lengthening phase of SSCs. In contrast, mdm muscles showed neither doublet potentiation features, nor phase-dependence of activation. To further distinguish the contributions of cross bridge and non-cross bridge elements, we performed SSCs on permeabilized psoas fiber bundles activated to different levels using either [Ca2+] or [Ca2+] plus the myosin inhibitor 2,3-butanedione monoxime (BDM). Across activation levels ranging from 15 to 100% of maximum isometric force, peak force, and work per cycle were enhanced for fibers in [Ca2+] plus BDM compared to [Ca2+] alone at a corresponding activation level, suggesting a contribution from Ca2+-sensitive, non-cross bridge, viscoelastic elements. Taken together, our results suggest that a tunable viscoelastic element such as titin contributes to: (1) persistence of force at low [Ca2+] in doublet potentiation; (2) phase- and length-dependence of doublet potentiation observed in wild type muscles and the absence of these effects in mdm muscles; and (3) increased peak force and work per cycle in SSCs. We conclude that non-cross bridge viscoelastic elements, likely titin, contribute substantially to muscle force and work, as well as the phase-dependence of these quantities, during dynamic length changes.
Ahmad Ludin, Norasikin, Nurfarhana Alyssa Ahmad Affandi, Kathleen Purvis-Roberts, Azah Ahmad, Mohd Adib Ibrahim, Kamaruzzaman Sopian, and Sufian Jusoh. “Environmental Impact and Levelised Cost of Energy Analysis of Solar Photovoltaic Systems in Selected Asia Pacific Region: A Cradle-to-Grave Approach.” Sustainability, vol. 13, issue 1, 2021, 396.
Abstract: Sustainability has been greatly impacted by the reality of budgets and available resources as a targeted range of carbon emission reduction greatly increases due to climate change. This study analyses the technical and economic feasibility for three types of solar photovoltaic (PV) renewable energy (RE) systems; (i) solar stand-alone, a non-grid-connected building rooftop-mounted structure, (ii) solar rooftop, a grid-connected building rooftop-mounted structure, (iii) solar farm, a grid-connected land-mounted structure in three tropical climate regions. Technical scientific and economic tools, including life cycle assessment (LCA) and life cycle cost assessment (LCCA) with an integrated framework from a Malaysian case study were applied to similar climatic regions, Thailand, and Indonesia. The short-term, future scaled-up scenario was defined using a proxy technology and estimated data. Environmental locations for this scenario were identified, the environmental impacts were compared, and the techno-economic output were analysed. The scope of this study is cradle-to-grave. Levelised cost of energy (LCOE) was greatly affected due to PV performance degradation rate, especially the critical shading issues for large-scale installations. Despite the land use impact, increased CO2 emissions accumulate over time with regard to energy mix of the country, which requires the need for long-term procurement of both carbon and investment return. With regards to profitably, grid-connected roof-mounted systems achieve the lowest LCOE as compared to other types of installation, ranging from 0.0491 USD/kWh to 0.0605 USD/kWh under a 6% discounted rate. A simple payback (SPB) time between 7–10 years on average depends on annual power generated by the system with estimated energy payback of 0.40–0.55 years for common polycrystalline photovoltaic technology. Thus, maintaining the whole system by ensuring a low degradation rate of 0.2% over a long period of time is essential to generate benefits for both investors and the environment. Emerging technologies are progressing at an exponential rate in order to fill the gap of establishing renewable energy as an attractive business plan. Life cycle assessment is considered an excellent tool to assess the environmental impact of renewable energy.
Ahmad Ludin, Norasikin, Nurfarhana Alyssa Ahmad Affandi, Norul Hisham Hamid, Mirratul Mukminah Junedi, Kathleen Purvis-Roberts, and Sufian Jusof. “Sustainability and the Life Cycle Cost Analysis of Solar Photovoltaic-Generation Systems in ASEAN Countries.” Energy Sustainability and Climate Change in ASEAN, edited by Han Phoumin, Farhad Taghizadeh-Hesary, Fukunari Kimura, and Jun Arima. Springer, 2021, pp. 277-302.
Abstract: Solar energy is a renewable source that can help the Association of Southeast Asian Nations (ASEAN) region realise its 23% renewable energy target by 2025. However, its development is slow due to a lack of awareness and funds. Many financial institutions are willing to invest in renewable energy projects, but data reliability has been a concern. Approaches that can be used to gather and to analyse data, therefore, should be identified to attract investors towards renewable energy. Quantitative analyses could also help governments more accurately develop reusable energy plans and integrate the procurement of reliable renewable energy systems into them. This study aims to provide a comprehensive assessment of the environmental and economic impacts of various types of solar photovoltaic (PV) systems (e.g., stand-alone, rooftop, and solar farm) by using sustainable quantitative approaches, such as life-cycle analysis and life-cycle cost analysis. Data normalisation was also conducted to compare the performance of each system. It was found that the solar PV rooftop system has the lowest greenhouse gas emissions, life-cycle cost, and levelised cost of energy. This study then offers policy recommendations to attract high, sustainable green investment to the region.
Purvis-Roberts, Kathleen L. “Collaborative Environmental Science Courses: Energy Focused Comparisons between Malaysia and the United States.” ASIANetwork Exchange, vol. 27, issue 2, 2021, pp. 6-12.
Abstract: With support from the EnviroLab Asia initiative at the Claremont Colleges, I redeveloped my Environmental Chemistry course for undergraduates to focus on environmental issues in Asia. I collaborated with a colleague from the Universiti Kebangsaan Malaysia (UKM) who was teaching a similar course for master’s-level students in Bangi, Malaysia. Our students worked on projects together comparing different aspects of renewable energy in the two countries. At the end of the semester, my students traveled to UKM for a symposium with my colleague’s students and continued working on their research projects to turn them into publishable papers. The Claremont Colleges students greatly benefited from both the academic and cultural learning that occurred during our travel. I am currently developing a network of faculty at universities in Asia-Pacific Economic Cooperation (APEC) economies who have their students work on data-gathering and/or analysis projects that can be useful for policymaking by the APEC Energy Working Group.
Van Rooy, Paul, Ryan Drover*, Tanner Cress*, Cara Michael*, Kathleen L. Purvis-Roberts, Philip Silva, Matthew J. Nee, and David Cocker. “Methanesulfonic Acid and Sulfuric Acid Aerosol Formed through Oxidation of Reduced Sulfur Compounds in a Humid Environment.” Atmospheric Environment, vol. 261, 2021, 118504.
Abstract: Particulate sulfuric acid and methanesulfonic acid (MSA) are known to form through oxidation of reduced sulfur compounds, however, the mechanisms by which these compounds form are not well understood. Additionally, the aerosol yields and ratio of MSA to sulfuric acid particulate formation are not well documented, making it difficult to estimate the health and climate impacts of reduced sulfur compounds. To investigate these unknowns, dimethylsulfide (DMS) and dimethyldisulfide (DMDS) were oxidized, using a variety of oxidants, in a 37.5 cubic meter Teflon environmental chamber with relative humidity ranging from 2% to 55%. The mass fraction of particulate MSA was estimated based on unique aerosol fragments, at m/z 79 and 96, measured by a High Resolution Time-of-Flight Mass Spectrometer. MSA to sulfuric acid particulate ratios varied depending on initial conditions. This study revealed that substantial water vapor is necessary to form MSA. The mass fraction of MSA increases in the presence of NOx. Nitrate radical oxidation of DMS and DMDS resulted in nearly 100% of the aerosol estimated to be MSA, suggesting nighttime chemistry may play an important role in ambient MSA formation. This study builds upon results from similar experiments, presented in Van Rooy et al. (2021), which were conducted under extreme dry conditions.
Van Rooy, Paul, Kathleen L. Purvis-Roberts, Philip J. Silva, Matthew J. Nee, and David Cocker. “Characterization of Secondary Products Formed Through Oxidation of Reduced Sulfur Compounds.” Atmospheric Environment, vol. 256, 2021, 118148.
Abstract: Dimethylsulfide (DMS) and dimethyldisulfide (DMDS) are precursors to products, like sulfuric acid and methanesulfonic acid (MSA), which are important to secondary aerosol formation. The formation and yields of particulate MSA and sulfuric acid from the oxidation of reduced sulfur compounds is not well understood. In this study, a 37.5 cubic meter Teflon environmental chamber was utilized to study the oxidation mechanism and aerosol forming potential of DMS and DMDS under dry conditions. Experiments were conducted in both the presence and absence of NOx, using hydroxyl radical, nitrate radical, as well O(3P) as an oxidant. With initial NOx concentrations of 100 part-per-billion, relatively low for laboratory oxidation experiments, O(3P) dominated oxidation of the reduced sulfur precursor and resulted in aerosol mass yields of greater than 40%. Hydroxyl radical oxidation of DMS and DMDS in the absence of NOx resulted in aerosol yields of 6% and 13%, respectively, while nitrate radical oxidation in the presence of NOx resulted in yields of 8% and less than 1%, respectively. Evidence of sulfuric acid formation was present during all particle-forming experiments, as was evidence of additional unknown sulfur-containing organic particulate. There was no evidence of MSA formation in the gas- or particle-phase throughout this study. The absence of MSA formation in the presence of NOx has not been reported in previous studies and indicates a lack of understanding of the MSA formation mechanism. The observations made during this chamber study diverge from observations made during previous studies conducted under high precursor and NOx concentrations, emphasizing the importance of atmospherically relevant initial conditions.
Choiniere, Jonah J., James M. Neenan, Lars Schmitz, David P. Ford, Kimberley E. J. Chapelle, Amy M. Balanoff, Justin S. Sipla, Justin A. Georgi, Stig A. Walsh, Mark A. Norell, Xing Xu, James M. Clark, and Roger B.J. Benson. “Evolution of Vision and Hearing Modalities in Theropod Dinosaurs.” Science, vol. 372, issue 6542, 2021, 610-613.
Abstract: Owls and nightbirds are nocturnal hunters of active prey that combine visual and hearing adaptations to overcome limits on sensory performance in low light. Such sensory innovations are unknown in nonavialan theropod dinosaurs and are poorly characterized on the line that leads to birds. We investigate morphofunctional proxies of vision and hearing in living and extinct theropods and demonstrate deep evolutionary divergences of sensory modalities. Nocturnal predation evolved early in the nonavialan lineage Alvarezsauroidea, signaled by extreme low-light vision and increases in hearing sensitivity. The Late Cretaceous alvarezsauroid Shuvuuia deserti had even further specialized hearing acuity, rivaling that of today’s barn owl. This combination of sensory adaptations evolved independently in dinosaurs long before the modern bird radiation and provides a notable example of convergence between dinosaurs and mammals.
Higham, Timothy E., Lara A. Ferry, Lars Schmitz, Duncan J. Irschick, Samuel Starko, Philip S.L. Anderson, Philip J. Bermann, Heather A. Jamniczky, Leandro R. Monteiro, Dina Navon, Julie Messier, Emily Carrington, Stacy C. Farina, Kara L. Feilich, L. Patricia Hernandez, Michele A. Johnson, Sandy M. Kawano, Chris J. Law, Sarah J. Longo, Christopher H. Martin, Patrick T. Martone, Alejandro Rico-Guevara, Sharlene E. Santana, and Karl J. Niklas. “Linking Ecomechanical Models and Functional Traits to Understand Phenotypic Diversity.” Trends in Ecology & Evolution, vol. 36, issue 9, 2021, pp. 860-873.
Abstract: All organisms must comply with physical laws, which place rigid or hard constraints on survival and reproduction. Ecomechanics is the expression of that interplay, and assumes a central role when considering organismal development, ecology, and evolution. How organisms will respond to changes in the environment, such as human-mediated climate change, will depend strongly on ecomechanics. Functional traits are commonly used to investigate the consequences of ecological variation. Ecomechanical models that incorporate functional traits and environmental variables are key to deciphering the rules of life and expand upon functional trait studies. The use of the ecomechanical framework is illustrated using multiple examples (e.g., wind-induced bending mechanics in trees and gecko adhesion in the real world). We emphasize safety factors as a key metric when assessing the evolution of form and performance. Biologists can apply our framework to many other systems. We offer suggestions for constructing and tailoring the data pipeline for future ecomechanical models to enhance their availability and utility for various disciplines.
Sander, P. Martin, Eva Marie Griebeler, Nicole Klein, Jorge Velez Juarbe, Tanja Wintrich, Liam J. Revell, and Lars Schmitz. “Early Giant Reveals Faster Evolution of Large Body Size in Ichthyosaurs than in Cetaceans.” Science, vol. 374, issue 6575, 2021, pp. 1554-1555.
Abstract: Body sizes of marine amniotes span six orders of magnitude, yet the factors that governed the evolution of this diversity are largely unknown. High primary production of modern oceans is considered a prerequisite for the emergence of cetacean giants, but that condition cannot explain gigantism in Triassic ichthyosaurs. We describe the new giant ichthyosaur Cymbospondylus youngorum sp. nov. with a 2-meter-long skull from the Middle Triassic Fossil Hill Fauna of Nevada, USA, underscoring rapid size evolution despite the absence of many modern primary producers. Surprisingly, the Fossil Hill Fauna rivaled the composition of modern marine mammal faunas in terms of size range, and energy-flux models suggest that Middle Triassic marine food webs were able to support several large-bodied ichthyosaurs at high trophic levels, shortly after ichthyosaur origins.
Sheung, Janet Y., Daisy H. Achiriloaie*, Christopher Currie, Karthik Peddireddy, Aaron Xie*, Jessalyn Simon-Parker*, Gloria Lee, Michael J. Rust, Moumita Das, Jennifer L. Ross, and Rae M. Robertson-Anderson. “Motor-Driven Restructuring of Cytoskeleton Composites Leads to Tunable Time-Varying Elasticity.” ACS Macro Letters, vol. 10, issue 9, 2021, pp. 1151-1158.
Abstract: The composite cytoskeleton, comprising interacting networks of semiflexible actin and rigid microtubules, generates forces and restructures by using motor proteins such as myosins to enable key processes including cell motility and mitosis. Yet, how motor-driven activity alters the mechanics of cytoskeleton composites remains an open challenge. Here, we perform optical tweezers microrheology and confocal imaging of composites with varying actin–tubulin molar percentages (25–75, 50–50, and 75–25), driven by light-activated myosin II motors, to show that motor activity increases the elastic plateau modulus by over 2 orders of magnitude by active restructuring of both actin and microtubules that persists for hours after motor activation has ceased. Nonlinear microrheology measurements show that motor-driven restructuring increases the force response and stiffness and suppresses actin bending. The 50–50 composite exhibits the most dramatic mechanical response to motor activity due to the synergistic effects of added stiffness from the microtubules and sufficient motor substrate for pronounced activity.
Sheung, Janet Y., Megan Otsuka*, Gabriella Seifert*, Athena Lin, and Wallace F. Marshall. “Analysis of Motility Patterns of Stentor During and After Oral Apparatus Regeneration Using Cell Tracking.” Journal of Visualized Experiments, vol. 170, 2021, e62352.
Abstract: Stentor coeruleus is a well-known model organism for the study of unicellular regeneration. Transcriptomic analysis of individual cells revealed hundreds of genes—many not associated with the oral apparatus (OA)—that are differentially regulated in phases throughout the regeneration process. It was hypothesized that this systemic reorganization and mobilization of cellular resources towards growth of a new OA will lead to observable changes in movement and behavior corresponding in time to the phases of differential gene expression. However, the morphological complexity of S. coeruleus necessitated the development of an assay to capture the statistics and timescale. A custom script was used to track cells in short videos, and statistics were compiled over a large population (N ~100). Upon loss of the OA, S. coeruleus initially loses the ability for directed motion; then starting at ~4 h, it exhibits a significant drop in speed until ~8 h. This assay provides a useful tool for the screening of motility phenotypes and can be adapted for the investigation of other organisms.
Sheung, Janet Y., Megan Otsuka*, Athena Lin, Gabriella Seifert*, and Wallace Marshall. “Motility and Behavior of S. Coerleus During Regeneration.” Biophysical Journal, vol. 120, issue 3, 2021, 235a.
Vyas, Aditi, Anna V. Freitas, Zachary A. Ralston, and Zhaohua Tang. “Fission Yeast Schizosaccharomyces pombe: A Unicellular ‘Micromammal’ Model Organism.” Current Protocols, vol. 1, issue 6, 2021, e151.
Abstract: The fission yeast Schizosaccharomyces pombe is a rod-shaped unicellular eukaryote, well known for its contributions as a model organism for our understanding of regulation and conservation of the eukaryotic cell cycle. As a yeast divergent from the budding yeast Saccharomyces cerevisiae, S. pombe shares more common features with humans including gene structures, chromatin dynamics, and the prevalence of introns, as well as the control of gene expression through pre-mRNA splicing, epigenetic gene silencing, and RNAi pathways. With the advent of new methodologies for research, S. pombe has become an increasingly used model to investigate various molecular and cellular processes over the last 50 years. Also, S. pombe serves as an excellent system for undergraduate students to obtain hands-on research experience. Versatile experimental approaches are amenable using the fission yeast system due to its relative ease of maintenance, its inherent cellular properties, its power in classic and molecular genetics, and its feasibility in genomics and proteomics analyses. This article provides an overview of S. pombe’s rise as a valuable model organism and presents examples to highlight the significance of S. pombe as a unicellular “micromammal” in investigating biological questions. We especially focus on the advantages of and the advancements in using fission yeast for studying biological processes that are characteristic of metazoans to decipher the underlining molecular mechanisms fundamental to all eukaryotes.
Thomson, Diane M. “Novel Data Support Model Linking Floral Resources and Honey Bee Competition with Bumble Bee Abundances in Coastal Scrub.” Journal of Pollination Ecology, vol. 27, issue 4, 2021, pp. 47-56.
Abstract: Growing evidence supports that many bee populations are declining, with potentially serious consequences for pollination services. Mechanistic models that predict bee abundances from drivers like floral resource availability can be a powerful way to understand and address declines, but remain rare and largely unvalidated. I used temporally and spatially novel data to validate previous analyses linking bumble bee (Bombus spp.) declines in California coastal scrub with loss of floral resources, mediated by drought and competition with non-native honey bees (Apis mellifera). New observations from 2015-2018 were combined with data from 1999-2014 to further test these mechanistic hypotheses and evaluate predictions of a statistical model for Bombus abundances. As predicted, positive associations between spring rainfall and floral abundances and between Bombus and key forage plants were consistent between time periods. Increased A. mellifera abundance corresponded with reduced Bombus use of the most abundant forage plant and lower Bombus abundances in the following year. Quantitative predictions from the Bombus statistical model previously developed for 1999-2014 were relatively unbiased and strongly rank correlated with either spatially or temporally novel data. However, the model consistently underpredicted Bombus abundances when both flower patch and time period were novel. Overall, four new years of data further strengthen evidence that loss of floral resources due to drought and competition with feral Apis mellifera is an important cause of Bombus decline in this habitat. These findings reinforce the value of even simple models that are mechanistically framed, both in understanding past patterns of change and for qualitative prediction.
Thomson, Diane M., Wallace M. Meyer III, and Isobel F. Whitcomb*. “Non-Native Plant Removal and High Rainfall Years Promote Post-Fire Recovery of Artemisia californica in Southern California Sage Scrub.” PLOS One, vol. 16, issue 7, 2021, e0254398.
Abstract: Non-native plant invasions, changes in fire regime, and increasing drought stress all pose important threats to biodiverse mediterranean-climate shrublands. These factors can also interact, with fire and drought potentially creating opportunities for non-native species to establish dominance before native shrubs recover. We carried out post-fire demographic monitoring of the common native shrub Artemisia californica in a southern California sage scrub fragment for 7 years, including several with very low rainfall. Experimental removals of non-native plants were included for the first 4 years. We quantified A. californica post-fire crown resprouting and seedling emergence, and tested effects of precipitation, non-native plants, and their interactions on seedling and adult survival. Only 7 A. californica were confirmed as resprouts; almost all individuals established after the fire from seedlings, with 90% of emergence occurring in the second growing year after fire (spring 2015). Higher spring precipitation increased both adult and seedling survival. Non-native grasses and forbs rapidly recolonized control plots, but the removal treatment reduced non-native cover by nearly 60%. For seedlings, non-native removal reduced the probability of dropping leaves by start of summer drought and increased survival both directly and through positive interactions with rainfall. Non-native removal also reduced mortality in smaller adult plants. By 2020, mean A. californica canopy area was nearly four times greater in non-native removal plots. These findings reinforce the high vulnerability of sage scrub habitat to post-fire loss of shrub cover and potential type conversion, particularly with increasing drought frequency and in stands and species with limited crown resprouting. Yet they also illustrate the potential for targeted management of non-natives immediately after fire to promote recovery of native shrubs in this increasingly endangered community.
External Grant: Guillams, C. Matt, K. Hasenstab-Lehman. K. McEachern and Diane M. Thomson. “Using Genetic Data to Guide Conservation Actions for the Endangered Single-Island Endemic Plant Castilleja Mollis Pennell (Soft-Leaved Island Paintbrush).” U.S. Fish and Wildlife Service, Recovery Challenge Program, 2021-2023, $98,319.
Abstract: Castilleja mollis Pennell (soft-leaved paintbrush) is completely endemic to Santa Rosa Island, California within Channel Islands National Park, limited to two sub-populations 7 km apart along the north shore. This species occurs in fragmented coastal scrub habitat on shore bluffs and marine terraces, in a narrow band of cool and moist micro-habitat within 300 meters of the ocean. C. mollis was listed as endangered in 2000 because of damage to plants and habitats from ranching (USFWS 1997, USFWS 2000), since addressed by removal of non-native vertebrate herbivores (Priority 1 Task already completed). At the time of listing, potential hybrids between C. mollis and C. affinis Hook. & Arn. ssp. affinis were observed farther inland where the two species occurred in close proximity. Hybridization was identified as a possible threat to the persistence of C. mollis as an independent evolutionary lineage. Monitoring data, mapping, and pilot genetic studies from 1995-2019 suggest that hybrids may be increasing rapidly in abundance and spatial extent within the Carrington Point subpopulation, potentially linked with hotter and drier weather conditions. The Jaw Gulch subpopulation appears to still support pure C. mollis, but numbers there have declined steeply over the last decade. Current status and population trends for pure C. mollis are highly uncertain because morphological traits used to identify potential hybrids have not been fully confirmed by genetic analyses. We propose to quantify genetic composition across the current C. mollis distribution, assess how quickly hybrids are spreading, identify morphological traits that can be used to distinguish hybrids, and collect seed from the pure C. mollis lineage. We will also map and characterize current and potential habitat for pure C. mollis. Determining the extent, spatial distribution and morphological characteristics of hybrids is crucial to completion of seed collection and appropriate restoration plantings, both Priority 1 Tasks. The proposed work will also inform several Priority 2 Tasks (determining connectedness between populations, development of seed banking program). This work will enable planning for seed collection, plant propagation and outplanting. Without better genetic data, these conservation actions cannot be designed and targeted to conserve pure C. mollis effectively. We have a potentially narrow window of opportunity to collect pure C. mollis, as well as to identify potential habitat and assess needs for future planting.
Fukuda, Taise T. H., Eric J. N. Helfrich, Emily Mevers, Weilan G. P. Melo, Ethan B. Van Arnam, David R. Andes, Cameron R. Currie, Monica T. Pupo, and Jon Clardy. “Specialized Metabolites Reveal Evolutionary History and Geographic Dispersion of a Multilateral Symbiosis.” ACS Central Science, vol. 7, issue 2, 2021, pp. 292-299.
Abstract: Fungus-growing ants engage in a multilateral symbiosis: they cultivate a fungal garden as their primary food source and host symbiotic actinobacteria (Pseudonocardia spp.) that provide chemical defenses. The bacterial symbionts produce small specialized metabolites that protect the fungal garden from specific fungal pathogens (Escovopsis spp.), and in return, they are fed by the ant hosts. Multiple studies on the molecules underlying this symbiotic system have led to the discovery of a large number of structurally diverse antifungal molecules, but somewhat surprisingly no shared structural theme emerged from these studies. A large systematic study of Brazilian nests led to the discovery of the widespread production of a potent but overlooked antifungal agent, which we named attinimicin, by nearly two-thirds of all Pseudonocardia strains from multiple sites in Brazil. Here we report the structure of attinimicin, its putative biosynthetic gene cluster, and the evolutionary relationship between attinimicin and two related peptides, oxachelin A and cahuitamycin A. All three nonribosomal peptides are structural isomers with different primary peptide sequences. Attinimicin shows iron-dependent antifungal activity against specific environmental fungal parasites but no activity against the fungal cultivar. Attinimicin showed potent in vivo activity in a mouse Candida albicans infection model comparable to clinically used azole-containing antifungals. In situ detection of attinimicin in both ant nests and on worker ants supports an ecological role for attinimicin in protecting the fungal cultivar from pathogens. The geographic spread of the attinimicin biosynthetic gene cluster in Brazilian Pseudonocardia spp. marks attinimicin as the first specialized metabolite from ant-associated bacteria with broad geographic distribution.
Doherty, John, Branwen Williams, Esme Kline*, Walter Adey, and Benoit Thibodeau. “Climate-Modulated Nutrient Conditions Along the Labrador Shelf: Evidence From Nitrogen Isotopes in a Six-Hundred-Year-Old Crustose Coralline Alga.” Paleoceanography and Paleoclimatology, vol. 36, issue 5, 2021, e2020PA004149.
Abstract: The impacts of climate change on north Atlantic nutrient chemistry remain poorly understood, as there exist a multitude of rapidly changing biological and physical drivers of nutrient conditions throughout the region. Here, we present nitrogen isotope measurements derived from a six-hundred-year-old crustose coralline alga (δ15Nalgal) to elucidate historical and contemporary trends in nitrate utilization and circulation patterns along the Labrador Shelf. Prior to the early 1900s, we argue that intervals during which utilization approached completion were controlled by reduced nitrate advection linked to an increased proportion of nitrate-poor polar waters and subdued Atlantic influence, as expected from concurrent negative modes of the Atlantic multidecadal oscillation. While nitrate conditions should have recovered in recent years, our record suggests that high utilization persisted since ∼1870, which we also attribute to reduced Atlantic advection, likely associated with the twentieth-century anthropogenic weakening of the Atlantic meridional overturning circulation. These results highlight the role of ongoing climate-induced circulation changes in modulating nutrient distributions throughout the subpolar north Atlantic, which may have implications for other environmental phenomena such as fisheries and oceanic carbon storage.
Williams, Branwen, Phoebe T.W. Chan, Jochen Halfar, Kathryn Hargan, and Walter Adey. “Arctic Crustose Coralline Alga Resilient to Recent Environmental Change.” Limnology and Oceanography, vol. 66, issue S1, 2021, pp. S246-S258.
Abstract: Rising atmospheric carbon dioxide is warming Arctic seawater at a rate twice the global average due to multiple positive feedbacks. Thus, warming is disproportionately influencing data‐poor Arctic marine ecosystems. Subarctic flora are an important component of these ecosystems, along with the less biodiverse flora endemic to the Arctic. Warming will likely lead to an increasing dominance of subarctic flora that will be initially successful due to a shorter sea ice period. Benthic crustose coralline algae presently flourishes in subarctic regions where they are key substrate builders that influence community structure through provision of habitat for a variety of benthic organisms. Here we evaluate changes in the skeletal resilience of long‐lived subarctic crustose coralline alga Clathromorphum compactum to variability in seawater temperature and sea ice (the later which influences salinity and solar irradiance reaching the seafloor) across latitudes in the northwest Atlantic and Arctic Oceans. We demonstrate that average growth and calcification rate significantly decreases in C. compactum toward higher latitudes due to colder temperatures and more fresh waters. Skeletal density also declines toward higher latitudes but displays specimen‐specific variability. However, through a common growth period (1984–2001), density increased at all locations which we interpret to be a response to warmer and more well‐lit benthic environments. At the most northerly site, growth and calcification also increased with density, suggesting warming and declining Arctic sea ice in the spring may benefit this species at its upper latitudinal limits. As a result, continued warming may enhance the presence of C. compactum in Arctic regions.
Williams, Branwen, Phoebe Chan, Issac Westfield, Douglas Rasher, and Justin Ries. “Ocean Acidification Reduces Skeletal Density of Hardground-Forming High-Latitude Crustose Coralline Algae.” Geophysical Research Letters, vol. 48, issue 5, 2021, e2020GL091499.
Abstract: Crustose coralline algae (CCA) function as foundation species by creating marine carbonate hardground habitats. High-latitude species may be vulnerable to regional warming and acidification. Here, we report the results of an experiment investigating the impacts of CO2-induced acidification (pCO2 ∼350, 490, 890, 3,200 µatm) and temperature (∼6.5°C, 8.5°C, 12.5°C) on the skeletal density of two species of high-latitude CCA: Clathromorphum compactum and Clathromorphum nereostratum (CN). Skeletal density of both species significantly declined with pCO2. In CN, the density of previously deposited skeleton declined in the highest pCO2 treatment. This species was also unable to precipitate new skeleton at 12.5°C, suggesting that CN will be particularly sensitive to future warming and acidification. The decline in skeletal density exhibited by both species under future pCO2 conditions could reduce their skeletal strength, potentially rendering them more vulnerable to disturbance, and impairing their production of critical habitat in high-latitude systems.
Williams, Sierra J., Clare S. Hwang, and Jennifer A. Prescher. “Orthogonal Bioluminescent Probes from Disubstituted Luciferins.” Biochemistry, vol. 60, issue 8, 2021, pp. 563-572.
Abstract: Bioluminescence imaging with luciferase–luciferin pairs is routinely used to monitor cellular functions. Multiple targets can be visualized in tandem using luciferases that process unique substrates, but only a handful of such orthogonal probes are known. Multiplexed studies require additional robust, light-emitting molecules. In this work, we report new luciferins for orthogonal imaging that comprise disubstituted cores. These probes were found to be bright emitters with various engineered luciferases. The unique patterns of light output also provided insight into enzyme–substrate interactions necessary for productive emission. Screening studies identified mutant luciferases that could preferentially process the disubstituted analogues, enabling orthogonal imaging with existing bioluminescent reporters. Further mutational analyses revealed the origins of substrate selectivity. Collectively, this work provides insights into luciferase–luciferin features relevant to bioluminescence and expands the number of probes for multicomponent tracking.