BioSciences Publications

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https://hdl.handle.net/1911/78269

BioSciences faculty publications. For works published before Summer 2014, please see the Biochemistry & Cell Biology and Ecology & Evolutionary Biology collections.

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Cell behaviors underlying Myxococcus xanthus aggregate dispersal
(American Society for Microbiology, 2023) Murphy, Patrick; Comstock, Jessica; Khan, Trosporsha; Zhang, Jiangguo; Welch, Roy; Igoshin, Oleg A.; Center for Theoretical Physical Biology
The soil bacterium Myxococcus xanthus is a model organism with a set of diverse behaviors. These behaviors include the starvation-induced multicellular development program, in which cells move collectively to assemble multicellular aggregates. After initial aggregates have formed, some will disperse, with smaller aggregates having a higher chance of dispersal. Initial aggregation is driven by two changes in cell behavior: cells slow down inside of aggregates and bias their motion by reversing direction less frequently when moving toward aggregates. However, the cell behaviors that drive dispersal are unknown. Here, we use fluorescent microscopy to quantify changes in cell behavior after initial aggregates have formed. We observe that after initial aggregate formation, cells adjust the bias in reversal timings by initiating reversals more rapidly when approaching unstable aggregates. Using agent-based modeling, we then show dispersal is predominantly generated by this change in bias, which is strong enough to overcome slowdown inside aggregates. Notably, the change in reversal bias is correlated with the nearest aggregate size, connecting cellular activity to previously observed correlations between aggregate size and fate. To determine if this connection is consistent across strains, we analyze a second M. xanthus strain with reduced levels of dispersal. We find that far fewer cells near smaller aggregates modified their bias. This implies that aggregate dispersal is under genetic control, providing a foundation for further investigations into the role it plays in the life cycle of M. xanthus.
Regulation of Syntaxin3B-Mediated Membrane Fusion by T14, Munc18, and Complexin
(MDPI, 2023) Nishad, Rajkishor; Betancourt-Solis, Miguel; Dey, Himani; Heidelberger, Ruth; McNew, James A.
Retinal neurons that form ribbon-style synapses operate over a wide dynamic range, continuously relaying visual information to their downstream targets. The remarkable signaling abilities of these neurons are supported by specialized presynaptic machinery, one component of which is syntaxin3B. Syntaxin3B is an essential t-SNARE protein of photoreceptors and bipolar cells that is required for neurotransmitter release. It has a light-regulated phosphorylation site in its N-terminal domain at T14 that has been proposed to modulate membrane fusion. However, a direct test of the latter has been lacking. Using a well-controlled in vitro fusion assay, we found that a phosphomimetic T14 syntaxin3B mutation leads to a small but significant enhancement of SNARE-mediated membrane fusion following the formation of the t-SNARE complex. While the addition of Munc18a had only a minimal effect on membrane fusion mediated by SNARE complexes containing wild-type syntaxin3B, a more significant enhancement was observed in the presence of Munc18a when the SNARE complexes contained a syntaxin3B T14 phosphomimetic mutant. Finally, we showed that the retinal-specific complexins (Cpx III and Cpx IV) inhibited membrane fusion mediated by syntaxin3B-containing SNARE complexes in a dose-dependent manner. Collectively, our results establish that membrane fusion mediated by syntaxin3B-containing SNARE complexes is regulated by the T14 residue of syntaxin3B, Munc18a, and Cpxs III and IV.
Environment and shipping drive environmental DNA beta-diversity among commercial ports
(Wiley, 2023) Andrés, Jose; Czechowski, Paul; Grey, Erin; Saebi, Mandana; Andres, Kara; Brown, Christopher; Chawla, Nitesh; Corbett, James J.; Brys, Rein; Cassey, Phillip; Correa, Nancy; Deveney, Marty R.; Egan, Scott P.; Fisher, Joshua P.; vanden Hooff, Rian; Knapp, Charles R.; Leong, Sandric Chee Yew; Neilson, Brian J.; Paolucci, Esteban M.; Pfrender, Michael E.; Pochardt, Meredith R.; Prowse, Thomas A. A.; Rumrill, Steven S.; Scianni, Chris; Sylvester, Francisco; Tamburri, Mario N.; Therriault, Thomas W.; Yeo, Darren C. J.; Lodge, David M.
The spread of nonindigenous species by shipping is a large and growing global problem that harms coastal ecosystems and economies and may blur coastal biogeographical patterns. This study coupled eukaryotic environmental DNA (eDNA) metabarcoding with dissimilarity regression to test the hypothesis that ship-borne species spread homogenizes port communities. We first collected and metabarcoded water samples from ports in Europe, Asia, Australia and the Americas. We then calculated community dissimilarities between port pairs and tested for effects of environmental dissimilarity, biogeographical region and four alternative measures of ship-borne species transport risk. We predicted that higher shipping between ports would decrease community dissimilarity, that the effect of shipping would be small compared to that of environment dissimilarity and shared biogeography, and that more complex shipping risk metrics (which account for ballast water and stepping-stone spread) would perform better. Consistent with our hypotheses, community dissimilarities increased significantly with environmental dissimilarity and, to a lesser extent, decreased with ship-borne species transport risks, particularly if the ports had similar environments and stepping-stone risks were considered. Unexpectedly, we found no clear effect of shared biogeography, and that risk metrics incorporating estimates of ballast discharge did not offer more explanatory power than simpler traffic-based risks. Overall, we found that shipping homogenizes eukaryotic communities between ports in predictable ways, which could inform improvements in invasive species policy and management. We demonstrated the usefulness of eDNA metabarcoding and dissimilarity regression for disentangling the drivers of large-scale biodiversity patterns. We conclude by outlining logistical considerations and recommendations for future studies using this approach.
Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins
(Oxford University Press, 2023) Howe-Kerr, Lauren I.; Knochel, Anna M.; Meyer, Matthew D.; Sims, Jordan A.; Karrick, Carly E.; Grupstra, Carsten G. B.; Veglia, Alex J.; Thurber, Andrew R.; Vega Thurber, Rebecca L.; Correa, Adrienne M. S.
Filamentous viruses are hypothesized to play a role in stony coral tissue loss disease (SCTLD) through infection of the endosymbiotic dinoflagellates (Family Symbiodiniaceae) of corals. To evaluate this hypothesis, it is critical to understand the global distribution of filamentous virus infections across the genetic diversity of Symbiodiniaceae hosts. Using transmission electron microscopy, we demonstrate that filamentous virus-like particles (VLPs) are present in over 60% of Symbiodiniaceae cells (genus Cladocopium) within Pacific corals (Acropora hyacinthus, Porites c.f. lobata); these VLPs are more prevalent in Symbiodiniaceae of in situ colonies experiencing heat stress. Symbiodiniaceae expelled from A. hyacinthus also contain filamentous VLPs, and these cells are more degraded than their in hospite counterparts. Similar to VLPs reported from SCTLD-affected Caribbean reefs, VLPs range from ~150 to 1500 nm in length and 16–37 nm in diameter and appear to constitute various stages in a replication cycle. Finally, we demonstrate that SCTLD-affected corals containing filamentous VLPs are dominated by diverse Symbiodiniaceae lineages from the genera Breviolum, Cladocopium, and Durusdinium. Although this study cannot definitively confirm or refute the role of filamentous VLPs in SCTLD, it demonstrates that filamentous VLPs are not solely observed in SCTLD-affected corals or reef regions, nor are they solely associated with corals dominated by members of a particular Symbiodiniaceae genus. We hypothesize that filamentous viruses are a widespread, common group that infects Symbiodiniaceae. Genomic characterization of these viruses and empirical tests of the impacts of filamentous virus infection on Symbiodiniaceae and coral colonies should be prioritized.
Cooperative assembly confers regulatory specificity and long-term genetic circuit stability
(Elsevier, 2023) Bragdon, Meghan D. J.; Patel, Nikit; Chuang, James; Levien, Ethan; Bashor, Caleb J.; Khalil, Ahmad S.
A ubiquitous feature of eukaryotic transcriptional regulation is cooperative self-assembly between transcription factors (TFs) and DNA cis-regulatory motifs. It is thought that this strategy enables specific regulatory connections to be formed in gene networks between otherwise weakly interacting, low-specificity molecular components. Here, using synthetic gene circuits constructed in yeast, we find that high regulatory specificity can emerge from cooperative, multivalent interactions among artificial zinc-finger-based TFs. We show that circuits “wired” using the strategy of cooperative TF assembly are effectively insulated from aberrant misregulation of the host cell genome. As we demonstrate in experiments and mathematical models, this mechanism is sufficient to rescue circuit-driven fitness defects, resulting in genetic and functional stability of circuits in long-term continuous culture. Our naturally inspired approach offers a simple, generalizable means for building high-fidelity, evolutionarily robust gene circuits that can be scaled to a wide range of host organisms and applications.
High-temperature electrothermal remediation of multi-pollutants in soil
(Springer Nature, 2023) Deng, Bing; Carter, Robert A.; Cheng, Yi; Liu, Yuan; Eddy, Lucas; Wyss, Kevin M.; Ucak-Astarlioglu, Mine G.; Luong, Duy Xuan; Gao, Xiaodong; JeBailey, Khalil; Kittrell, Carter; Xu, Shichen; Jana, Debadrita; Torres, Mark Albert; Braam, Janet; Tour, James M.; NanoCarbon Center and the Rice Advanced Materials Institute; Smalley-Curl Institute
Soil contamination is an environmental issue due to increasing anthropogenic activities. Existing processes for soil remediation suffer from long treatment time and lack generality because of different sources, occurrences, and properties of pollutants. Here, we report a high-temperature electrothermal process for rapid, water-free remediation of multiple pollutants in soil. The temperature of contaminated soil with carbon additives ramps up to 1000 to 3000 °C as needed within seconds via pulsed direct current input, enabling the vaporization of heavy metals like Cd, Hg, Pb, Co, Ni, and Cu, and graphitization of persistent organic pollutants like polycyclic aromatic hydrocarbons. The rapid treatment retains soil mineral constituents while increases infiltration rate and exchangeable nutrient supply, leading to soil fertilization and improved germination rates. We propose strategies for upscaling and field applications. Techno-economic analysis indicates the process holds the potential for being more energy-efficient and cost-effective compared to soil washing or thermal desorption.
Heterogeneity in M. tuberculosis β-lactamase inhibition by Sulbactam
(Springer Nature, 2023) Malla, Tek Narsingh; Zielinski, Kara; Aldama, Luis; Bajt, Sasa; Feliz, Denisse; Hayes, Brendon; Hunter, Mark; Kupitz, Christopher; Lisova, Stella; Knoska, Juraj; Martin-Garcia, Jose Manuel; Mariani, Valerio; Pandey, Suraj; Poudyal, Ishwor; Sierra, Raymond G.; Tolstikova, Alexandra; Yefanov, Oleksandr; Yoon, Chung Hong; Ourmazd, Abbas; Fromme, Petra; Schwander, Peter; Barty, Anton; Chapman, Henry N.; Stojkovic, Emina A.; Batyuk, Alexander; Boutet, Sébastien; Phillips, George N.; Pollack, Lois; Schmidt, Marius
For decades, researchers have elucidated essential enzymatic functions on the atomic length scale by tracing atomic positions in real-time. Our work builds on possibilities unleashed by mix-and-inject serial crystallography (MISC) at X-ray free electron laser facilities. In this approach, enzymatic reactions are triggered by mixing substrate or ligand solutions with enzyme microcrystals. Here, we report in atomic detail (between 2.2 and 2.7 Å resolution) by room-temperature, time-resolved crystallography with millisecond time-resolution (with timepoints between 3 ms and 700 ms) how the Mycobacterium tuberculosis enzyme BlaC is inhibited by sulbactam (SUB). Our results reveal ligand binding heterogeneity, ligand gating, cooperativity, induced fit, and conformational selection all from the same set of MISC data, detailing how SUB approaches the catalytic clefts and binds to the enzyme noncovalently before reacting to a trans-enamine. This was made possible in part by the application of singular value decomposition to the MISC data using a program that remains functional even if unit cell parameters change up to 3 Å during the reaction.
A portable regulatory RNA array design enables tunable and complex regulation across diverse bacteria
(Springer Nature, 2023) Liu, Baiyang; Samaniego, Christian Cuba; Bennett, Matthew R.; Franco, Elisa; Chappell, James
A lack of composable and tunable gene regulators has hindered efforts to engineer non-model bacteria and consortia. Toward addressing this, we explore the broad-host potential of small transcription activating RNA (STAR) and propose a design strategy to achieve tunable gene control. First, we demonstrate that STARs optimized for E. coli function across different Gram-negative species and can actuate using phage RNA polymerase, suggesting that RNA systems acting at the level of transcription are portable. Second, we explore an RNA design strategy that uses arrays of tandem and transcriptionally fused RNA regulators to precisely alter regulator concentration from 1 to 8 copies. This provides a simple means to predictably tune output gain across species and does not require access to large regulatory part libraries. Finally, we show RNA arrays can be used to achieve tunable cascading and multiplexing circuits across species, analogous to the motifs used in artificial neural networks.
Human astrovirus capsid protein releases a membrane lytic peptide upon trypsin maturation
(American Society for Microbiology, 2023) Ykema, Matthew; Ye, Kai; Xun, Meng; Harper, Justin; Betancourt-Solis, Miguel A.; Arias, Carlos F.; McNew, James A.; Tao, Yizhi Jane
The human astrovirus (HAstV) is a non-enveloped, single-stranded RNA virus that is a common cause of gastroenteritis. Most non-enveloped viruses use membrane disruption to deliver the viral genome into a host cell after virus uptake. The virus–host factors that allow for HAstV cell entry are currently unknown but thought to be associated with the host-protease-mediated viral maturation. Using in vitro liposome disruption analysis, we identified a trypsin-dependent lipid disruption activity in the capsid protein of HAstV serotype 8. This function was further localized to the P1 domain of the viral capsid core, which was both necessary and sufficient for membrane disruption. Site-directed mutagenesis identified a cluster of four trypsin cleavage sites necessary to retain the lipid disruption activity, which is likely attributed to a short stretch of sequence ending at arginine 313 based on mass spectrometry of liposome-associated peptides. The membrane disruption activity was conserved across several other HAstVs, including the emerging VA2 strain, and effective against a wide range of lipid identities. This work provides key functional insight into the protease maturation process essential to HAstV infectivity and presents a method to investigate membrane penetration by non-enveloped viruses in vitro.
Pattern of seasonal variation in rates of predation between spider families is temporally stable in a food web with widespread intraguild predation
(Public Library of Science, 2023) Wise, David H.; Mores, Robin M.; O, Jennifer M. Pajda-De La; McCary, Matthew A.
Intraguild predation (IGP)–predation between generalist predators (IGPredator and IGPrey) that potentially compete for a shared prey resource–is a common interaction module in terrestrial food webs. Understanding temporal variation in webs with widespread IGP is relevant to testing food web theory. We investigated temporal constancy in the structure of such a system: the spider-focused food web of the forest floor. Multiplex PCR was used to detect prey DNA in 3,300 adult spiders collected from the floor of a deciduous forest during spring, summer, and fall over four years. Because only spiders were defined as consumers, the web was tripartite, with 11 consumer nodes (spider families) and 22 resource nodes: 11 non-spider arthropod taxa (order- or family-level) and the 11 spider families. Most (99%) spider-spider predation was on spider IGPrey, and ~90% of these interactions were restricted to spider families within the same broadly defined foraging mode (cursorial or web-spinning spiders). Bootstrapped-derived confidence intervals (BCI’s) for two indices of web structure, restricted connectance and interaction evenness, overlapped broadly across years and seasons. A third index, % IGPrey (% IGPrey among all prey of spiders), was similar across years (~50%) but varied seasonally, with a summer rate (65%) ~1.8x higher than spring and fall. This seasonal pattern was consistent across years. Our results suggest that extensive spider predation on spider IGPrey that exhibits consistent seasonal variation in frequency, and that occurs primarily within two broadly defined spider-spider interaction pathways, must be incorporated into models of the dynamics of forest-floor food webs.
Protein target highlights in CASP15: Analysis of models by structure providers
(Wiley, 2023) Alexander, Leila T.; Durairaj, Janani; Kryshtafovych, Andriy; Abriata, Luciano A.; Bayo, Yusupha; Bhabha, Gira; Breyton, Cécile; Caulton, Simon G.; Chen, James; Degroux, Séraphine; Ekiert, Damian C.; Erlandsen, Benedikte S.; Freddolino, Peter L.; Gilzer, Dominic; Greening, Chris; Grimes, Jonathan M.; Grinter, Rhys; Gurusaran, Manickam; Hartmann, Marcus D.; Hitchman, Charlie J.; Keown, Jeremy R.; Kropp, Ashleigh; Kursula, Petri; Lovering, Andrew L.; Lemaitre, Bruno; Lia, Andrea; Liu, Shiheng; Logotheti, Maria; Lu, Shuze; Markússon, Sigurbjörn; Miller, Mitchell D.; Minasov, George; Niemann, Hartmut H.; Opazo, Felipe; Phillips Jr, George N.; Davies, Owen R.; Rommelaere, Samuel; Rosas-Lemus, Monica; Roversi, Pietro; Satchell, Karla; Smith, Nathan; Wilson, Mark A.; Wu, Kuan-Lin; Xia, Xian; Xiao, Han; Zhang, Wenhua; Zhou, Z. Hong; Fidelis, Krzysztof; Topf, Maya; Moult, John; Schwede, Torsten
We present an in-depth analysis of selected CASP15 targets, focusing on their biological and functional significance. The authors of the structures identify and discuss key protein features and evaluate how effectively these aspects were captured in the submitted predictions. While the overall ability to predict three-dimensional protein structures continues to impress, reproducing uncommon features not previously observed in experimental structures is still a challenge. Furthermore, instances with conformational flexibility and large multimeric complexes highlight the need for novel scoring strategies to better emphasize biologically relevant structural regions. Looking ahead, closer integration of computational and experimental techniques will play a key role in determining the next challenges to be unraveled in the field of structural molecular biology.
High-speed AFM imaging reveals DNA capture and loop extrusion dynamics by cohesin-NIPBL
(Elsevier, 2023) Kaur, Parminder; Lu, Xiaotong; Xu, Qi; Irvin, Elizabeth Marie; Pappas, Colette; Zhang, Hongshan; Finkelstein, Ilya J.; Shi, Zhubing; Tao, Yizhi Jane; Yu, Hongtao; Wang, Hong
3D chromatin organization plays a critical role in regulating gene expression, DNA replication, recombination, and repair. While initially discovered for its role in sister chromatid cohesion, emerging evidence suggests that the cohesin complex (SMC1, SMC3, RAD21, and SA1/SA2), facilitated by NIPBL, mediates topologically associating domains and chromatin loops through DNA loop extrusion. However, information on how conformational changes of cohesin-NIPBL drive its loading onto DNA, initiation, and growth of DNA loops is still lacking. In this study, high-speed atomic force microscopy imaging reveals that cohesin-NIPBL captures DNA through arm extension, assisted by feet (shorter protrusions), and followed by transfer of DNA to its lower compartment (SMC heads, RAD21, SA1, and NIPBL). While binding at the lower compartment, arm extension leads to the capture of a second DNA segment and the initiation of a DNA loop that is independent of ATP hydrolysis. The feet are likely contributed by the C-terminal domains of SA1 and NIPBL and can transiently bind to DNA to facilitate the loading of the cohesin complex onto DNA. Furthermore, high-speed atomic force microscopy imaging reveals distinct forward and reverse DNA loop extrusion steps by cohesin-NIPBL. These results advance our understanding of cohesin by establishing direct experimental evidence for a multistep DNA-binding mechanism mediated by dynamic protein conformational changes.
Impacts of habitat connectivity on grassland arthropod metacommunity structure: A field-based experimental test of theory
(Wiley, 2023) Bertellotti, Franklin; Sommer, Nathalie R.; Schmitz, Oswald J.; McCary, Matthew A.
Metacommunity theory has advanced scientific understanding of how species interactions and spatial processes influence patterns of biodiversity and community structure across landscapes. While the central tenets of metacommunity theory have been promoted as pivotal considerations for conservation management, few field experiments have tested the validity of metacommunity predictions. Here, we tested one key prediction of metacommunity theory—that decreasing habitat connectivity should erode metacommunity structure by hindering species movement between patches. For 2 years, we manipulated an experimental old-field grassland ecosystem via mowing to represent four levels of habitat connectivity: (1) open control, (2) full connectivity, (3) partial connectivity, and (4) no connectivity. Within each treatment plot (10 × 10 m, n = 4 replicates), we measured the abundance and diversity (i.e., alpha and beta) of both flying and ground arthropods using sticky and pitfall traps, respectively. We found that the abundance and diversity of highly mobile flying arthropods were unaffected by habitat connectivity, whereas less mobile ground arthropods were highly impacted. The mean total abundance of ground arthropods was 2.5× and 2× higher in the control and partially connected plots compared to isolated patches, respectively. We also reveal that habitat connectivity affected the trophic interactions of ground arthropods, with predators (e.g., wolf spiders, ground spiders) being highly positively correlated with micro-detritivores (springtails, mites) but not macro-detritivores (millipedes, isopods) as habitat connectivity increased. Together these findings indicate that changes in habitat connectivity can alter the metacommunity structure for less mobile organisms such as ground arthropods. Because of their essential roles in terrestrial ecosystem functioning and services, we recommend that conservationists, restoration practitioners, and land managers include principles of habitat connectivity for ground arthropods when designing biodiversity management programs.
Infrastructure to factorially manipulate the mean and variance of precipitation in the field
(Wiley, 2023) Rudgers, Jennifer A.; Luketich, Anthony; Bacigalupa, Melissa; Baur, Lauren E.; Collins, Scott L.; Hall, Kristofer M.; Hou, Enqing; Litvak, Marcy E.; Luo, Yiqi; Miller, Tom E. X.; Newsome, Seth D.; Pockman, William T.; Richardson, Andrew D.; Rinehart, Alex; Villatoro-Castañeda, Melissa; Wainwright, Brooke E.; Watson, Samantha J.; Yogi, Purbendra; Zhou, Yu
Extensive ecological research has investigated extreme climate events or long-term changes in average climate variables, but changes in year-to-year (interannual) variability may also cause important biological responses, even if the mean climate is stable. The environmental stochasticity that is a hallmark of climate variability can trigger unexpected biological responses that include tipping points and state transitions, and large differences in weather between consecutive years can also propagate antecedent effects, in which current biological responses depend on responsiveness to past perturbations. However, most studies to date cannot predict ecological responses to rising variance because the study of interannual variance requires empirical platforms that generate long time series. Furthermore, the ecological consequences of increases in climate variance could depend on the mean climate in complex ways; therefore, effective ecological predictions will require determining responses to both nonstationary components of climate distributions: the mean and the variance. We introduce a new design to resolve the relative importance of, and interactions between, a drier mean climate and greater climate variance, which are dual components of ongoing climate change in the southwestern United States. The Mean × Variance Experiment (MVE) adds two novel elements to prior field infrastructure methods: (1) factorial manipulation of variance together with the climate mean and (2) the creation of realistic, stochastic precipitation regimes. Here, we demonstrate the efficacy of the experimental design, including sensor networks and PhenoCams to automate monitoring. We replicated MVE across ecosystem types at the northern edge of the Chihuahuan Desert biome as a central component of the Sevilleta Long-Term Ecological Research Program. Soil sensors detected significant treatment effects on both the mean and interannual variability in soil moisture, and PhenoCam imagery captured change in vegetation cover. Our design advances field methods to newly compare the sensitivities of populations, communities, and ecosystem processes to climate mean × variance interactions.
A deep learning solution for crystallographic structure determination
(International Union of Crystallography, 2023) Pan, T.; Jin, S.; Miller, M. D.; Kyrillidis, A.; Phillips, G. N.
The general de novo solution of the crystallographic phase problem is difficult and only possible under certain conditions. This paper develops an initial pathway to a deep learning neural network approach for the phase problem in protein crystallography, based on a synthetic dataset of small fragments derived from a large well curated subset of solved structures in the Protein Data Bank (PDB). In particular, electron-density estimates of simple artificial systems are produced directly from corresponding Patterson maps using a convolutional neural network architecture as a proof of concept.
Endogenous viral elements reveal associations between a non-retroviral RNA virus and symbiotic dinoflagellate genomes
(Springer Nature, 2023) Veglia, Alex J.; Bistolas, Kalia S. I.; Voolstra, Christian R.; Hume, Benjamin C. C.; Ruscheweyh, Hans-Joachim; Planes, Serge; Allemand, Denis; Boissin, Emilie; Wincker, Patrick; Poulain, Julie; Moulin, Clémentine; Bourdin, Guillaume; Iwankow, Guillaume; Romac, Sarah; Agostini, Sylvain; Banaigs, Bernard; Boss, Emmanuel; Bowler, Chris; de Vargas, Colomban; Douville, Eric; Flores, Michel; Forcioli, Didier; Furla, Paola; Galand, Pierre E.; Gilson, Eric; Lombard, Fabien; Pesant, Stéphane; Reynaud, Stéphanie; Sunagawa, Shinichi; Thomas, Olivier P.; Troublé, Romain; Zoccola, Didier; Correa, Adrienne M. S.; Vega Thurber, Rebecca L.
Endogenous viral elements (EVEs) offer insight into the evolutionary histories and hosts of contemporary viruses. This study leveraged DNA metagenomics and genomics to detect and infer the host of a non-retroviral dinoflagellate-infecting +ssRNA virus (dinoRNAV) common in coral reefs. As part of the Tara Pacific Expedition, this study surveyed 269 newly sequenced cnidarians and their resident symbiotic dinoflagellates (Symbiodiniaceae), associated metabarcodes, and publicly available metagenomes, revealing 178 dinoRNAV EVEs, predominantly among hydrocoral-dinoflagellate metagenomes. Putative associations between Symbiodiniaceae and dinoRNAV EVEs were corroborated by the characterization of dinoRNAV-like sequences in 17 of 18 scaffold-scale and one chromosome-scale dinoflagellate genome assembly, flanked by characteristically cellular sequences and in proximity to retroelements, suggesting potential mechanisms of integration. EVEs were not detected in dinoflagellate-free (aposymbiotic) cnidarian genome assemblies, including stony corals, hydrocorals, jellyfish, or seawater. The pervasive nature of dinoRNAV EVEs within dinoflagellate genomes (especially Symbiodinium), as well as their inconsistent within-genome distribution and fragmented nature, suggest ancestral or recurrent integration of this virus with variable conservation. Broadly, these findings illustrate how +ssRNA viruses may obscure their genomes as members of nested symbioses, with implications for host evolution, exaptation, and immunity in the context of reef health and disease.
Stony coral tissue loss disease induces transcriptional signatures of in situ degradation of dysfunctional Symbiodiniaceae
(Springer Nature, 2023) Beavers, Kelsey M.; Van Buren, Emily W.; Rossin, Ashley M.; Emery, Madison A.; Veglia, Alex J.; Karrick, Carly E.; MacKnight, Nicholas J.; Dimos, Bradford A.; Meiling, Sonora S.; Smith, Tyler B.; Apprill, Amy; Muller, Erinn M.; Holstein, Daniel M.; Correa, Adrienne M. S.; Brandt, Marilyn E.; Mydlarz, Laura D.
Stony coral tissue loss disease (SCTLD), one of the most pervasive and virulent coral diseases on record, affects over 22 species of reef-building coral and is decimating reefs throughout the Caribbean. To understand how different coral species and their algal symbionts (family Symbiodiniaceae) respond to this disease, we examine the gene expression profiles of colonies of five species of coral from a SCTLD transmission experiment. The included species vary in their purported susceptibilities to SCTLD, and we use this to inform gene expression analyses of both the coral animal and their Symbiodiniaceae. We identify orthologous coral genes exhibiting lineage-specific differences in expression that correlate to disease susceptibility, as well as genes that are differentially expressed in all coral species in response to SCTLD infection. We find that SCTLD infection induces increased expression of rab7, an established marker of in situ degradation of dysfunctional Symbiodiniaceae, in all coral species accompanied by genus-level shifts in Symbiodiniaceae photosystem and metabolism gene expression. Overall, our results indicate that SCTLD infection induces symbiophagy across coral species and that the severity of disease is influenced by Symbiodiniaceae identity.
How to tuna fish: constraint, convergence, and integration in the neurocranium of pelagiarian fishes
(Oxford University Press, 2023) Knapp, Andrew; Rangel-de Lázaro, Gizéh; Friedman, Matt; Johanson, Zerina; Evans, Kory M; Giles, Sam; Beckett, Hermione T; Goswami, Anjali
Morphological evolution of the vertebrate skull has been explored across a wide range of tetrapod clades using geometric morphometrics, but the application of these methods to teleost fishes, accounting for roughly half of all vertebrate species, has been limited. Here we present the results of a study investigating 3D morphological evolution of the neurocranium across 114 species of Pelagiaria, a diverse clade of open-ocean teleost fishes that includes tuna and mackerel. Despite showing high shape disparity overall, taxa from all families fall into three distinct morphological clusters. Convergence in shape within clusters is high, and phylogenetic signal in shape data is significant but low. Neurocranium shape is significantly correlated with body elongation and significantly but weakly correlated with size. Diet and habitat depth are weakly correlated with shape, and nonsignificant after accounting for phylogeny. Evolutionary integration in the neurocranium is high, suggesting that convergence in skull shape and the evolution of extreme morphologies are associated with the correlated evolution of neurocranial elements. These results suggest that shape evolution in the pelagiarian neurocranium reflects the extremes in elongation found in body shape but is constrained along relatively few axes of variation, resulting in repeated evolution toward a restricted range of morphologies.
Building consensus around the assessment and interpretation of Symbiodiniaceae diversity
(PeerJ, Inc, 2023) Davies, Sarah W.; Gamache, Matthew H.; Howe-Kerr, Lauren I.; Kriefall, Nicola G.; Baker, Andrew C.; Banaszak, Anastazia T.; Bay, Line Kolind; Bellantuono, Anthony J.; Bhattacharya, Debashish; Chan, Cheong Xin; Claar, Danielle C.; Coffroth, Mary Alice; Cunning, Ross; Davy, Simon K.; Campo, Javier del; Díaz-Almeyda, Erika M.; Frommlet, Jörg C.; Fuess, Lauren E.; González-Pech, Raúl A.; Goulet, Tamar L.; Hoadley, Kenneth D.; Howells, Emily J.; Hume, Benjamin C. C.; Kemp, Dustin W.; Kenkel, Carly D.; Kitchen, Sheila A.; LaJeunesse, Todd C.; Lin, Senjie; McIlroy, Shelby E.; McMinds, Ryan; Nitschke, Matthew R.; Oakley, Clinton A.; Peixoto, Raquel S.; Prada, Carlos; Putnam, Hollie M.; Quigley, Kate; Reich, Hannah G.; Reimer, James Davis; Rodriguez-Lanetty, Mauricio; Rosales, Stephanie M.; Saad, Osama S.; Sampayo, Eugenia M.; Santos, Scott R.; Shoguchi, Eiichi; Smith, Edward G.; Stat, Michael; Stephens, Timothy G.; Strader, Marie E.; Suggett, David J.; Swain, Timothy D.; Tran, Cawa; Traylor-Knowles, Nikki; Voolstra, Christian R.; Warner, Mark E.; Weis, Virginia M.; Wright, Rachel M.; Xiang, Tingting; Yamashita, Hiroshi; Ziegler, Maren; Correa, Adrienne M. S.; Parkinson, John Everett
Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.
SARS-CoV-2 Exposure in Norway Rats (Rattus norvegicus) from New York City
(American Society for Microbiology, 2023) Wang, Yang; Lenoch, Julianna; Kohler, Dennis; DeLiberto, Thomas J.; Tang, Cynthia Y.; Li, Tao; Tao, Yizhi Jane; Guan, Minhui; Compton, Susan; Zeiss, Caroline; Hang, Jun; Wan, Xiu-Feng
Millions of Norway rats (Rattus norvegicus) inhabit New York City (NYC), presenting the potential for transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) from humans to rats. We evaluated SARS-CoV-2 exposure among 79 rats captured from NYC during the fall of 2021. Our results showed that 13 of the 79 rats (16.5%) tested IgG- or IgM-positive, and partial SARS-CoV-2 genomes were recovered from all 4 rats that were qRT-PCR (reverse transcription-quantitative PCR)-positive. Genomic analyses suggest these viruses were associated with genetic lineage B, which was predominant in NYC in the spring of 2020 during the early pandemic period. To further investigate rat susceptibility to SARS-CoV-2 variants, we conducted a virus challenge study and showed that Alpha, Delta, and Omicron variants can cause infections in wild-type Sprague Dawley (SD) rats, including high replication levels in the upper and lower respiratory tracts and induction of both innate and adaptive immune responses. Additionally, the Delta variant resulted in the highest infectivity. In summary, our results indicate that rats are susceptible to infection with Alpha, Delta, and Omicron variants, and wild Norway rats in the NYC municipal sewer systems have been exposed to SARS-CoV-2. Our findings highlight the need for further monitoring of SARS-CoV-2 in urban rat populations and for evaluating the potential risk of secondary zoonotic transmission from these rat populations back to humans. IMPORTANCE The host tropism expansion of SARS-CoV-2 raises concern for the potential risk of reverse-zoonotic transmission of emerging variants into rodent species, including wild rat species. In this study, we present both genetic and serological evidence for SARS-CoV-2 exposure to the New York City wild rat population, and these viruses may be linked to the viruses that were circulating during the early stages of the pandemic. We also demonstrated that rats are susceptible to additional variants (i.e., Alpha, Delta, and Omicron) that have been predominant in humans and that susceptibility to infection varies by variant. Our findings highlight the reverse zoonosis of SARS-CoV-2 to urban rats and the need for further monitoring of SARS-CoV-2 in rat populations for potential secondary zoonotic transmission to humans.

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