Research and Publications - Department of Biological Sciences

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    Ubiquitin conjugating enzymes participate in polyglutamine protein aggregation
    (BMC, 2007) Howard, Rebecca A.; Sharma, Pratima; Hajjar, Connie; Caldwell, Kim A.; Caldwell, Guy A.; Du Breuil, Rusla; Moore, Rhonda; Boyd, Lynn; University of Alabama Huntsville; University of Alabama Tuscaloosa
    Background: Protein aggregation is a hallmark of several neurodegenerative diseases including Huntington's disease and Parkinson's disease. Proteins containing long, homopolymeric stretches of glutamine are especially prone to form aggregates. It has long been known that the small protein modifier, ubiquitin, localizes to these aggregates. In this report, nematode and cell culture models for polyglutamine aggregation are used to investigate the role of the ubiquitin pathway in protein aggregation. Results: Ubiquitin conjugating enzymes (Ubc's) were identified that affect polyglutamine aggregates in C. elegans. Specifically, RNAi knockdown of ubc-2 or ubc-22 causes a significant increase in the size of aggregates as well as a reduction in aggregate number. In contrast, RNAi of ubc-1, ubc-13, or uev-1 leads to a reduction of aggregate size and eliminates ubiquitin and proteasome localization to aggregates. In cultured human cells, shRNA knockdown of human homologs of these Ubc's (Ube2A, UbcH5b, and E2- 25K) causes similar effects indicating a conserved role for ubiquitination in polyglutamine protein aggregation. Conclusion: Results of knockdown of different Ubc enzymes indicate that at least two different and opposing ubiquitination events occur during polyglutamine aggregation. The loss of ubiquitin localization after ubc-1, ubc-13, or uev-1 knockdown suggests that these enzymes might be directly involved in ubiquitination of aggregating proteins.
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    Maple syrup urine disease: new insights from a zebrafish model
    (Company of Biologists, 2012) Roberts, Nathan B.; University of Alabama Tuscaloosa
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    Microbial Community Analysis of a Coastal Salt Marsh Affected by the Deepwater Horizon Oil Spill
    (PLOS, 2012) Beazley, Melanie J.; Martinez, Robert J.; Rajan, Suja; Powell, Jessica; Piceno, Yvette M.; Tom, Lauren M.; Andersen, Gary L.; Hazen, Terry C.; Van Nostrand, Joy D.; Zhou, Jizhong; Mortazavi, Behzad; Sobecky, Patricia A.; University of Alabama Tuscaloosa; United States Department of Energy (DOE); Lawrence Berkeley National Laboratory; University of California Berkeley; University of Tennessee Knoxville; University of Oklahoma - Norman; Dauphin Island Sea Lab
    Coastal salt marshes are highly sensitive wetland ecosystems that can sustain long-term impacts from anthropogenic events such as oil spills. In this study, we examined the microbial communities of a Gulf of Mexico coastal salt marsh during and after the influx of petroleum hydrocarbons following the Deepwater Horizon oil spill. Total hydrocarbon concentrations in salt marsh sediments were highest in June and July 2010 and decreased in September 2010. Coupled PhyloChip and GeoChip microarray analyses demonstrated that the microbial community structure and function of the extant salt marsh hydrocarbon-degrading microbial populations changed significantly during the study. The relative richness and abundance of phyla containing previously described hydrocarbon-degrading bacteria (Proteobacteria, Bacteroidetes, and Actinobacteria) increased in hydrocarbon-contaminated sediments and then decreased once hydrocarbons were below detection. Firmicutes, however, continued to increase in relative richness and abundance after hydrocarbon concentrations were below detection. Functional genes involved in hydrocarbon degradation were enriched in hydrocarbon-contaminated sediments then declined significantly (p<0.05) once hydrocarbon concentrations decreased. A greater decrease in hydrocarbon concentrations among marsh grass sediments compared to inlet sediments (lacking marsh grass) suggests that the marsh rhizosphere microbial communities could also be contributing to hydrocarbon degradation. The results of this study provide a comprehensive view of microbial community structural and functional dynamics within perturbed salt marsh ecosystems.
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    Rediscovery of Leptoxis compacta (Anthony, 1854) (Gastropoda: Cerithioidea: Pleuroceridae)
    (PLOS, 2012) Whelan, Nathan V.; Johnson, Paul D.; Harris, Phil M.; University of Alabama Tuscaloosa
    The Mobile River Basin is a hotspot of molluscan endemism, but anthropogenic activities have caused at least 47 molluscan extinctions, 37 of which were gastropods, in the last century. Nine of these suspected extinctions were in the freshwater gastropod genus Leptoxis (Cerithioidea: Pleuroceridae). Leptoxis compacta, a Cahaba River endemic, has not been collected for > 70 years and was formally declared extinct in 2000. Such gastropod extinctions underscore the imperilment of freshwater resources and the current biodiversity crisis in the Mobile River Basin. During a May 2011 gastropod survey of the Cahaba River in central Alabama, USA, L. compacta was rediscovered. The identification of snails collected was confirmed through conchological comparisons to the L. compacta lectotype, museum records, and radulae morphology of historically collected L. compacta. Through observations of L. compacta in captivity, we document for the first time that the species lays eggs in short, single lines. Leptoxis compacta is restricted to a single location in the Cahaba River, and is highly susceptible to a single catastrophic extinction event. As such, the species deserves immediate conservation attention. Artificial propagation and reintroduction of L. compacta into its native range may be a viable recovery strategy to prevent extinction from a single perturbation event.
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    Lactate-starved neurons in ALS
    (Company of Biologists, 2012) Martinez, Bryan A.; University of Alabama Tuscaloosa
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    Homeotic functions of the Teashirt transcription factor during adult Drosophila development
    (Company of Biologists, 2013) Wang, Wei; Tindell, Neil; Yan, Shun; Yoder, John H.; University of Alabama Tuscaloosa
    During Drosophila development region-specific regulation of target genes by Hox proteins is modulated by genetic interactions with various cofactors and genetic collaborators. During embryogenesis one such modulator of Hox target specificity is the zinc-finger transcription factor Teashirt (Tsh) that is expressed in the developing trunk and cooperatively functions with trunk-specific Hox proteins to promote appropriate segment fate. This embryonic function of Tsh is characterized as homeotic since loss of embryonic Tsh activity leads to transformation of trunk segments toward head identity. In addition to this embryonic homeotic role, Tsh also performs vital Hox-independent functions through patterning numerous embryonic, larval and adult structures. Here we address whether the homeotic function of Tsh is maintained throughout development by investigating its contribution to patterning the adult abdomen. We show that Tsh is expressed throughout the developing abdomen and that this expression is dependent on the three Bithorax Hox proteins Ultrabithorax, Abdominal-A and Abdominal-B. Conditional reduction of Tsh activity during pupation reveals broad homeotic roles for this transcription factor throughout the adult abdomen. Additionally we show that, as during embryogenesis, the tsh paralog tiptop (tio) plays a partially redundant role in this homeotic activity. (C) 2012. Published by The Company of Biologists Ltd.
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    Diurnal patterns of gas-exchange and metabolic pools in tundra plants during three phases of the arctic growing season
    (Wiley, 2013) Patankar, Rajit; Mortazavi, Behzad; Oberbauer, Steven F.; Starr, Gregory; University of Alabama Tuscaloosa; Dauphin Island Sea Lab; Florida International University
    Arctic tundra plant communities are subject to a short growing season that is the primary period in which carbon is sequestered for growth and survival. This period is often characterized by 24-h photoperiods for several months a year. To compensate for the short growing season tundra plants may extend their carbon uptake capacity on a diurnal basis, but whether this is true remains unknown. Here, we examined in situ diurnal patterns of physiological activity and foliar metabolites during the early, mid, and late growing season in seven arctic species under light-saturated conditions. We found clear diurnal patterns in photosynthesis and respiration, with midday peaks and midnight lulls indicative of circadian regulation. Diurnal patterns in foliar metabolite concentrations were less distinct between the species and across seasons, suggesting that metabolic pools are likely governed by proximate external factors. This understanding of diurnal physiology will also enhance the parameterization of process-based models, which will aid in better predicting future carbon dynamics for the tundra. This becomes even more critical considering the rapid changes that are occurring circumpolarly that are altering plant community structure, function, and ultimately regional and global carbon budgets.
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    Characterization of Amoeboaphelidium protococcarum, an Algal Parasite New to the Cryptomycota Isolated from an Outdoor Algal Pond Used for the Production of Biofuel
    (PLOS, 2013) Letcher, Peter M.; Lopez, Salvador; Schmieder, Robert; Lee, Philip A.; Behnke, Craig; Powell, Martha J.; McBride, Robert C.; University of Alabama Tuscaloosa; San Diego State University
    Mass culture of algae for the production of biofuels is a developing technology designed to offset the depletion of fossil fuel reserves. However, large scale culture of algae in open ponds can be challenging because of incidences of infestation with algal parasites. Without knowledge of the identity of the specific parasite and how to control these pests, algal-based biofuel production will be limited. We have characterized a eukaryotic parasite of Scenedesmus dimorphus growing in outdoor ponds used for biofuel production. We demonstrated that as the genomic DNA of parasite FD01 increases, the concentration of S. dimorphus cells decreases; consequently, this is a highly destructive pathogen. Techniques for culture of the parasite and host were developed, and the endoparasite was identified as the Aphelidea, Amoeboaphelidium protococcarum. Phylogenetic analysis of ribosomal sequences revealed that parasite FD01 placed within the recently described Cryptomycota, a poorly known phylum based on two species of Rozella and environmental samples. Transmission electron microscopy demonstrated that aplanospores of the parasite produced filose pseudopodia, which contained fine fibers the diameter of actin microfilaments. Multiple lipid globules clustered and were associated with microbodies, mitochondria and a membrane cisternae, an arrangement characteristic of the microbody-lipid globule complex of chytrid zoospores. After encystment and attachment to the host cells, the parasite injected its protoplast into the host between the host cell wall and plasma membrane. At maturity the unwalled parasite occupied the entire host cell. After cleavage of the protoplast into aplanospores, a vacuole and lipids remained in the host cell. Amoeboaphelidium protococcarum isolate FD01 is characteristic of the original description of this species and is different from strain X-5 recently characterized. Our results help put a face on the Cryptomycota, revealing that the phylum is more diverse than previously understood and include some of the Aphelidea as well as Rozella species and potentially Microsporidia.
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    The Plastid Genome of the Red Macroalga Grateloupia taiwanensis (Halymeniaceae)
    (PLOS, 2013) DePriest, Michael S.; Bhattacharya, Debashish; Lopez-Bautista, Juan M.; University of Alabama Tuscaloosa; Rutgers State University New Brunswick
    The complete plastid genome sequence of the red macroalga Grateloupia taiwanensis S.-M. Lin & H.-Y. Liang (Halymeniaceae, Rhodophyta) is presented here. Comprising 191,270 bp, the circular DNA contains 233 protein-coding genes and 29 tRNA sequences. In addition, several genes previously unknown to red algal plastids are present in the genome of G. taiwanensis. The plastid genomes from G. taiwanensis and another florideophyte, Gracilaria tenuistipitata var. liui, are very similar in sequence and share significant synteny. In contrast, less synteny is shared between G. taiwanensis and the plastid genome representatives of Bangiophyceae and Cyanidiophyceae. Nevertheless, the gene content of all six red algal plastid genomes here studied is highly conserved, and a large core repertoire of plastid genes can be discerned in Rhodophyta.
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    Intraspecific phenotypic variation in a fish predator affects multitrophic lake metacommunity structure
    (Wiley, 2013) Howeth, Jennifer G.; Weis, Jerome J.; Brodersen, Jakob; Hatton, Elizabeth C.; Post, David M.; Yale University; University of Alabama Tuscaloosa; Swiss Federal Institutes of Technology Domain; Swiss Federal Institute of Aquatic Science & Technology (EAWAG)
    Contemporary insights from evolutionary ecology suggest that population divergence in ecologically important traits within predators can generate diversifying ecological selection on local community structure. Many studies acknowledging these effects of intraspecific variation assume that local populations are situated in communities that are unconnected to similar communities within a shared region. Recent work from metacommunity ecology suggests that species dispersal among communities can also influence species diversity and composition but can depend upon the relative importance of the local environment. Here, we study the relative effects of intraspecific phenotypic variation in a fish predator and spatial processes related to plankton species dispersal on multitrophic lake plankton metacommunity structure. Intraspecific diversification in foraging traits and residence time of the planktivorous fish alewife (Alosa pseudoharengus) among coastal lakes yields lake metacommunities supporting three lake types which differ in the phenotype and incidence of alewife: lakes with anadromous, landlocked, or no alewives. In coastal lakes, plankton community composition was attributed to dispersal versus local environmental predictors, including intraspecific variation in alewives. Local and beta diversity of zooplankton and phytoplankton was additionally measured in response to intraspecific variation in alewives. Zooplankton communities were structured by species sorting, with a strong influence of intraspecific variation in A. pseudoharengus. Intraspecific variation altered zooplankton species richness and beta diversity, where lake communities with landlocked alewives exhibited intermediate richness between lakes with anadromous alewives and without alewives, and greater community similarity. Phytoplankton diversity, in contrast, was highest in lakes with landlocked alewives. The results indicate that plankton dispersal in the region supplied a migrant pool that was strongly structured by intraspecific variation in alewives. This is one of the first studies to demonstrate that intraspecific phenotypic variation in a predator can maintain contrasting patterns of multitrophic diversity in metacommunities.
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    TorsinA rescues ER-associated stress and locomotive defects in C. elegans models of ALS
    (Company of Biologists, 2014) Thompson, Michelle L.; Chen, Pan; Yan, Xiaohui; Kim, Hanna; Borom, Akeem R.; Roberts, Nathan B.; Caldwell, Kim A.; Caldwell, Guy A.; University of Alabama Tuscaloosa; University of Alabama Birmingham
    Molecular mechanisms underlying neurodegenerative diseases converge at the interface of pathways impacting cellular stress, protein homeostasis and aging. Targeting the intrinsic capacities of neuroprotective proteins to restore neuronal function and/or attenuate degeneration represents a potential means toward therapeutic intervention. The product of the human DYT1 gene, torsinA, is a member of the functionally diverse AAA+ family of proteins and exhibits robust molecular-chaperone-like activity, both in vitro and in vivo. Although mutations in DYT1 are associated with a rare form of heritable generalized dystonia, the native function of torsinA seems to be cytoprotective in maintaining the cellular threshold to endoplasmic reticulum (ER) stress. Here we explore the potential for torsinA to serve as a buffer to attenuate the cellular consequences of misfolded-protein stress as it pertains to the neurodegenerative disease amyotrophic lateral sclerosis (ALS). The selective vulnerability of motor neurons to degeneration in ALS mouse models harboring mutations in superoxide dismutase (SOD1) has been found to correlate with regional-specific ER stress in brains. Using Caenorhabditis elegans as a system to model ER stress, we generated transgenic nematodes overexpressing either wild-type or mutant human SOD1 to evaluate their relative impact on ER stress induction in vivo. These studies revealed a mutant-SOD1-specific increase in ER stress that was further exacerbated by changes in temperature, all of which was robustly attenuated by co-expression of torsinA. Moreover, through complementary behavioral analysis, torsinA was able to restore normal neuronal function in mutant G85R SOD1 animals. Furthermore, torsinA targeted mutant SOD1 for degradation via the proteasome, representing mechanistic insight on the activity that torsinA has on aggregate-prone proteins. These results expand our understanding of proteostatic mechanisms influencing neuronal dysfunction in ALS, while simultaneously highlighting the potential for torsinA as a novel target for therapeutic development.
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    Microbial Community Responses to Organophosphate Substrate Additions in Contaminated Subsurface Sediments
    (PLOS, 2014) Martinez, Robert J.; Wu, Cindy H.; Beazley, Melanie J.; Andersen, Gary L.; Conrad, Mark E.; Hazen, Terry C.; Taillefert, Martial; Sobecky, Patricia A.; University of Alabama Tuscaloosa; University of California Berkeley; United States Department of Energy (DOE); Lawrence Berkeley National Laboratory; University of Tennessee Knoxville; Georgia Institute of Technology
    Background: Radionuclide-and heavy metal-contaminated subsurface sediments remain a legacy of Cold War nuclear weapons research and recent nuclear power plant failures. Within such contaminated sediments, remediation activities are necessary to mitigate groundwater contamination. A promising approach makes use of extant microbial communities capable of hydrolyzing organophosphate substrates to promote mineralization of soluble contaminants within deep subsurface environments. Methodology/Principal Findings: Uranium-contaminated sediments from the U. S. Department of Energy Oak Ridge Field Research Center (ORFRC) Area 2 site were used in slurry experiments to identify microbial communities involved in hydrolysis of 10 mM organophosphate amendments [i.e., glycerol-2-phosphate (G2P) or glycerol-3-phosphate (G3P)] in synthetic groundwater at pH 5.5 and pH 6.8. Following 36 day (G2P) and 20 day (G3P) amended treatments, maximum phosphate (PO43-) concentrations of 4.8 mM and 8.9 mM were measured, respectively. Use of the PhyloChip 16S rRNA microarray identified 2,120 archaeal and bacterial taxa representing 46 phyla, 66 classes, 110 orders, and 186 families among all treatments. Measures of archaeal and bacterial richness were lowest under G2P (pH 5.5) treatments and greatest with G3P (pH 6.8) treatments. Members of the phyla Crenarchaeota, Euryarchaeota, Bacteroidetes, and Proteobacteria demonstrated the greatest enrichment in response to organophosphate amendments and the OTUs that increased in relative abundance by 2-fold or greater accounted for 9%-50% and 3%-17% of total detected Archaea and Bacteria, respectively. Conclusions/Significance: This work provided a characterization of the distinct ORFRC subsurface microbial communities that contributed to increased concentrations of extracellular phosphate via hydrolysis of organophosphate substrate amendments. Within subsurface environments that are not ideal for reductive precipitation of uranium, strategies that harness microbial phosphate metabolism to promote uranium phosphate precipitation could offer an alternative approach for in situ sequestration.
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    Unexpected Rarity of the Pathogen Batrachochytrium dendrobatidis in Appalachian Plethodon Salamanders: 1957-2011
    (PLOS, 2014) Muletz, Carly; Caruso, Nicholas M.; Fleischer, Robert C.; McDiarmid, Roy W.; Lips, Karen R.; University of Maryland College Park; University of Alabama Tuscaloosa; Smithsonian Institution; Smithsonian National Zoological Park & Conservation Biology Institute; United States Department of the Interior; United States Geological Survey; Smithsonian National Museum of Natural History
    Widespread population declines in terrestrial Plethodon salamanders occurred by the 1980s throughout the Appalachian Mountains, the center of global salamander diversity, with no evident recovery. We tested the hypothesis that the historic introduction and spread of the pathogenic fungus Batrachochytrium dendrobatidis (Bd) Plethodon population declines. We expected to detect elevated prevalence of Bd prior to population declines as observed for Central American plethodontids. We tested 1,498 Plethodon salamanders of 12 species (892 museum specimens, 606 wild individuals) for the presence of Bd, and tested 94 of those for Batrachochytrium salamandrivorans (Bs) and for ranavirus. Field samples were collected in 2011 from 48 field sites across a 767 km transect. Historic samples from museum specimens ere collected at five sites with the greatest number and longest duration of collection (1957-987), four of which were sampled in the field in 2011. None of the museum specimens were positive for Bd, but four P. cinereus from field surveys positive The overall Bd prevalence from 1957-2011 for 12 Plethodon species sampled across a 757 km transect was 0.2% (95% CI 0.1-0.7%). All 94 samples were negative for Bs and ranavirus. We conclude that known amphibian pathogens are unlikely causes for declines in these Plethodon populations. Furthermore, these exceptionally low levels of Bd, in a region known to harbor Bd, may indicate that Plethodon specific traits limit Bd infection.
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    USBombus, a database of contemporary survey data for North American Bumble Bees (Hymenoptera, Apidae, Bombus) distributed in the United States
    (Pensoft, 2015) Koch, Jonathan B.; Lozier, Jeffrey; Strange, James P.; Ikerd, Harold; Griswold, Terry; Cordes, Nils; Solter, Leellen; Stewart, Isaac; Cameron, Sydney A.; Utah State University; United States Department of Agriculture (USDA); University of Alabama Tuscaloosa; University of Bielefeld; University of Illinois Urbana-Champaign
    Background Bumble bees (Hymenoptera: Apidae, Bombus) are pollinators of wild and economically important flowering plants. However, at least four bumble bee species have declined significantly in population abundance and geographic range relative to historic estimates, and one species is possibly extinct. While a wealth of historic data is now available for many of the North American species found to be in decline in online databases, systematic survey data of stable species is still not publically available. The availability of contemporary survey data is critically important for the future monitoring of wild bumble bee populations. Without such data, the ability to ascertain the conservation status of bumble bees in the United States will remain challenging. New information This paper describes USBombus, a large database that represents the outcomes of one of the largest standardized surveys of bumble bee pollinators (Hymenoptera, Apidae, Bombus) globally. The motivation to collect live bumble bees across the United States was to examine the decline and conservation status of Bombus affinis, B. occidentalis, B. pensylvanicus, and B. terricola. Prior to our national survey of bumble bees in the United States from 2007 to 2010, there have only been regional accounts of bumble bee abundance and richness. In addition to surveying declining bumble bees, we also collected and documented a diversity of co-occuring bumble bees. However we have not yet completely reported their distribution and diversity onto a public online platform. Now, for the first time, we report the geographic distribution of bumble bees reported to be in decline (Cameron et al. 2011), as well as bumble bees that appeared to be stable on a large geographic scale in the United States (not in decline). In this database we report a total of 17,930 adult occurrence records across 397 locations and 39 species of Bombus detected in our national survey. We summarize their abundance and distribution across the United States and association to different ecoregions. The geospatial coverage of the dataset extends across 41 of the 50 US states, and from 0 to 3500 m a.s.l. Authors and respective field crews spent a total of 512 hours surveying bumble bees from 2007 to 2010. The dataset was developed using SQL server 2008 r2. For each specimen, the following information is generally provided: species, name, sex, caste, temporal and geospatial details, Cartesian coordinates, data collector(s), and when available, host plants. This database has already proven useful for a variety of studies on bumble bee ecology and conservation. However it is not publicly available. Considering the value of pollinators in agriculture and wild ecosystems, this large database of bumble bees will likely prove useful for investigations of the effects of anthropogenic activities on pollinator community composition and conservation status.
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    How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model
    (Wiley, 2015) Boulton, Kay; Couto, Elsa; Grimmer, Andrew J.; Earley, Ryan L.; Canario, Adelino V. M.; Wilson, Alastair J.; Walling, Craig A.; University of Edinburgh; Universidade do Algarve; University of Exeter; University of Alabama Tuscaloosa
    It is widely expected that physiological and behavioral stress responses will be integrated within divergent stress-coping styles (SCS) and that these may represent opposite ends of a continuously varying reactive-proactive axis. If such a model is valid, then stress response traits should be repeatable and physiological and behavioral responses should also change in an integrated manner along a major axis of among-individual variation. While there is some evidence of association between endocrine and behavioral stress response traits, few studies incorporate repeated observations of both. To test this model, we use a multivariate, repeated measures approach in a captive-bred population of Xiphophorus birchmanni. We quantify among-individual variation in behavioral stress response to an open field trial (OFT) with simulated predator attack (SPA) and measure waterborne steroid hormone levels (cortisol, 11-ketotestosterone) before and after exposure. Under the mild stress stimulus (OFT), (multivariate) behavioral variation among individuals was consistent with a strong axis of personality (shy-bold) or coping style (reactive-proactive) variation. However, behavioral responses to a moderate stressor (SPA) were less repeatable, and robust statistical support for repeatable endocrine state over the full sampling period was limited to 11-ketotestosterone. Although post hoc analysis suggested cortisol expression was repeatable over short time periods, qualitative relationships between behavior and glucocorticoid levels were counter to our a priori expectations. Thus, while our results clearly show among-individual differences in behavioral and endocrine traits associated with stress response, the correlation structure between these is not consistent with a simple proactive-reactive axis of integrated stress-coping style. Additionally, the low repeatability of cortisol suggests caution is warranted if single observations (or indeed repeat measures over short sampling periods) of glucocorticoid traits are used in ecological or evolutionary studies focussed at the individual level.
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    Drought-induced changes in flow regimes lead to long-term losses in mussel-provided ecosystem services
    (Wiley, 2015) Vaughn, Caryn C.; Atkinson, Carla L.; Julian, Jason P.; University of Oklahoma - Norman; University of Alabama Tuscaloosa; Texas State University San Marcos
    Extreme hydro-meteorological events such as droughts are becoming more frequent, intense, and persistent. This is particularly true in the south central USA, where rapidly growing urban areas are running out of water and human-engineered water storage and management are leading to broad-scale changes in flow regimes. The Kiamichi River in southeastern Oklahoma, USA, has high fish and freshwater mussel biodiversity. However, water from this rural river is desired by multiple urban areas and other entities. Freshwater mussels are large, long-lived filter feeders that provide important ecosystem services. We ask how observed changes in mussel biomass and community composition resulting from drought-induced changes in flow regimes might lead to changes in river ecosystem services. We sampled mussel communities in this river over a 20-year period that included two severe droughts. We then used laboratory-derived physiological rates and river-wide estimates of species-specific mussel biomass to estimate three aggregate ecosystem services provided by mussels over this time period: biofiltration, nutrient recycling (nitrogen and phosphorus), and nutrient storage (nitrogen, phosphorus, and carbon). Mussel populations declined over 60%, and declines were directly linked to drought-induced changes in flow regimes. All ecosystem services declined over time and mirrored biomass losses. Mussel declines were exacerbated by human water management, which has increased the magnitude and frequency of hydrologic drought in downstream reaches of the river. Freshwater mussels are globally imperiled and declining around the world. Summed across multiple streams and rivers, mussel losses similar to those we document here could have considerable consequences for downstream water quality although lost biofiltration and nutrient retention. While we cannot control the frequency and severity of climatological droughts, water releases from reservoirs could be used to augment stream flows and prevent compounded anthropogenic stressors.
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    The Complete Chloroplast and Mitochondrial Genomes of the Green Macroalga Ulva sp UNA00071828 (Ulvophyceae, Chlorophyta)
    (PLOS, 2015) Melton, James T., III; Leliaert, Frederik; Tronholm, Ana; Lopez-Bautista, Juan M.; University of Alabama Tuscaloosa; Ghent University; Smithsonian Institution; Smithsonian National Museum of Natural History
    Sequencing mitochondrial and chloroplast genomes has become an integral part in understanding the genomic machinery and the phylogenetic histories of green algae. Previously, only three chloroplast genomes (Oltmannsiellopsis viridis, Pseudendoclonium akinetum, and Bryopsis hypnoides) and two mitochondrial genomes (O. viridis and P. akinetum) from the class Ulvophyceae have been published. Here, we present the first chloroplast and mitochondrial genomes from the ecologically and economically important marine, green algal genus Ulva. The chloroplast genome of Ulva sp. was 99,983 bp in a circular-mapping molecule that lacked inverted repeats, and thus far, was the smallest ulvophycean plastid genome. This cpDNA was a highly compact, AT-rich genome that contained a total of 102 identified genes (71 protein-coding genes, 28 tRNA genes, and three ribosomal RNA genes). Additionally, five introns were annotated in four genes: atpA (1), petB (1), psbB (2), and rrl (1). The circular-mapping mitochondrial genome of Ulva sp. was 73,493 bp and follows the expanded pattern also seen in other ulvophyceans and trebouxiophyceans. The Ulva sp. mtDNA contained 29 protein-coding genes, 25 tRNA genes, and two rRNA genes for a total of 56 identifiable genes. Ten introns were annotated in this mtDNA: cox1 (4), atp1 (1), nad3 (1), nad5 (1), and rrs (3). Double-cut-and-join (DCJ) values showed that organellar genomes across Chlorophyta are highly rearranged, in contrast to the highly conserved organellar genomes of the red algae (Rhodophyta). A phylogenomic investigation of 51 plastid protein-coding genes showed that Ulvophyceae is not monophyletic, and also placed Oltmannsiellopsis (Oltmannsiellopsidales) and Tetraselmis (Chlorodendrophyceae) closely to Ulva (Ulvales) and Pseudendoclonium (Ulothrichales).
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    Mutant human torsinA, responsible for early-onset dystonia, dominantly suppresses GTPCH expression, dopamine levels and locomotion in Drosophila melanogaster
    (Company of Biologists, 2015) Wakabayashi-Ito, Noriko; Ajjuri, Rami R.; Henderson, Benjamin W.; Doherty, Olugbenga M.; Breakefield, Xandra O.; O'Donnell, Janis M.; Ito, Naoto; Harvard University; Massachusetts General Hospital; Harvard Medical School; University of Alabama Tuscaloosa
    Dystonia represents the third most common movement disorder in humans with over 20 genetic loci identified. TOR1A (DYT1), the gene responsible for the most common primary hereditary dystonia, encodes torsinA, an AAA ATPase family protein. Most cases of DYT1 dystonia are caused by a 3 bp (Delta GAG) deletion that results in the loss of a glutamic acid residue (Delta E302/303) in the carboxyl terminal region of torsinA. This torsinA Delta E mutant protein has been speculated to act in a dominant-negative manner to decrease activity of wild type torsinA. Drosophila melanogaster has a single torsin-related gene, dtorsin. Null mutants of dtorsin exhibited locomotion defects in third instar larvae. Levels of dopamine and GTP cyclohydrolase (GTPCH) proteins were severely reduced in dtorsin-null brains. Further, the locomotion defect was rescued by the expression of human torsinA or feeding with dopamine. Here, we demonstrate that human torsinA Delta E dominantly inhibited locomotion in larvae and adults when expressed in neurons using a pan-neuronal promoter Elav. Dopamine and tetrahydrobiopterin (BH4) levels were significantly reduced in larval brains and the expression level of GTPCH protein was severely impaired in adult and larval brains. When human torsinA and torsinA Delta E were co-expressed in neurons in dtorsin-null larvae and adults, the locomotion rates and the expression levels of GTPCH protein were severely reduced. These results support the hypothesis that torsinA Delta E inhibits wild type torsinA activity. Similarly, neuronal expression of a Drosophila Dtorsin Delta E equivalent mutation dominantly inhibited larval locomotion and GTPCH protein expression. These results indicate that both torsinA Delta E and DtorsinDE act in a dominant-negative manner. We also demonstrate that Dtorsin regulates GTPCH expression at the post-transcriptional level. This Drosophila model of DYT1 dystonia provides an important tool for studying the differences in the molecular function between the wild type and the mutant torsin proteins.
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    Population Dynamics and Parasite Load of a Foraminifer on Its Antarctic Scallop Host with Their Carbonate Biomass Contributions
    (PLOS, 2015) Hancock, Leanne G.; Walker, Sally E.; Perez-Huerta, Alberto; Bowser, Samuel S.; University of Georgia; University of Alabama Tuscaloosa; Wadsworth Center
    We studied the population dynamics and parasite load of the foraminifer Cibicides antarcticus on its host the Antarctic scallop Adamussium colbecki from three localities differing by sea ice cover within western McMurdo Sound, Ross Sea, Antarctica: Explorers Cove, Bay of Sails and Herbertson Glacier. We also estimated CaCO3 biomass and annual production for both species. Cibicides populations varied by locality, valve type, and depth. Explorers Cove with multiannual sea ice had larger populations than the two annual sea ice localities, likely related to differences in nutrients. Populations were higher on Adamussium top valves, a surface that is elevated above the sediment. Depth did not affect Cibicides distributions except at Bay of Sails. Cibicides parasite load (the number of complete boreholes in Adamussium valves) varied by locality between 2% and 50%. For most localities the parasite load was < 20%, contrary to a previous report that similar to 50% of Cibicides were parasitic. The highest and lowest parasite load occurred at annual sea ice localities, suggesting that sea ice condition is not important. Rather, the number of adults that are parasitic could account for these differences. Cibicides bioerosion traces were categorized into four ontogenetic stages, ranging from newly attached recruits to parasitic adults. These traces provide an excellent proxy for population structure, revealing that Explorers Cove had a younger population than Bay of Sails. Both species are important producers of CaCO3. Cibicides CaCO3 biomass averaged 47-73 kg ha(-1) and Adamussium averaged 4987-6806 kg ha(-1) by locality. Annual production rates were much higher. Moreover, Cibicides represents 1.0-2.3% of the total host-parasite CaCO3 biomass. Despite living in the coldest waters on Earth, these species can contribute a substantial amount of CaCO3 to the Ross Sea and need to be incorporated into food webs, ecosystem models, and carbonate budgets for Antarctica.
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    Mitochondrial Haplotypes Influence Metabolic Traits in Porcine Transmitochondrial Cybrids
    (Nature Portfolio, 2015) Yu, Guanghui; Xiang, Hai; Tian, Jianhui; Yin, Jingdong; Pinkert, Carl A.; Li, Qiuyan; Zhao, Xingbo; Ministry of Agriculture & Rural Affairs; China Agricultural University; Auburn University; University of Alabama Tuscaloosa
    In farm animals, mitochondrial DNA mutations exist widely across breeds and individuals. In order to identify differences among mtDNA haplotypes, two porcine transmitochondrial cybrids were generated by fusion of a Lantang pig cell line devoid of mitochondrial DNA with enucleated cytoplasm from either a Large White pig or a Xiang pig harboring potentially divergent mitochondrial haplotypes. These cybrid cells were subjected to mitochondrial genome sequencing, copy number detecting and analysis of biochemical traits including succinate dehydrogenase (SDH) activity, ATP content and susceptibility to reactive oxygen species (ROS). The Lantang and Xiang mitochondrial genomes were highly homologous with only 18 polymorphic sites, and differed radically from the Large White with 201 and 198 mutations respectively. The Large White and Xiang cybrids exhibited similar mtDNA copy numbers and different values among biochemical traits, generated greater ROS production (P < 0.05) and less SDH activity (P < 0.05) and a lesser ATP content (P < 0.05). The results show that functional differences exist between cybrid cells which differ in mitochondrial genomic background. In conclusion, transmitochondrial cybrids provide the first direct evidence on pig biochemical traits linking different mitochondrial genome haplotypes.