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De Meulenaere, E, Bailey JB, Tezcan FA, Deheyn DD.  2017.  First biochemical and crystallographic characterization of a fast-performing ferritin from a marine invertebrate. Biochemical Journal. 474:4193-4206.   10.1042/bcj20170681   AbstractWebsite

Ferritin, a multimeric cage-like enzyme, is integral to iron metabolism across all phyla through the sequestration and storage of iron through efficient ferroxidase activity. While ferritin sequences from similar to 900 species have been identified, crystal structures from only 50 species have been reported, the majority from bacterial origin. We recently isolated a secreted ferritin from the marine invertebrate Chaetopterus sp. (parchment tube worm), which resides in muddy coastal seafloors. Here, we present the first ferritin from a marine invertebrate to be crystallized and its biochemical characterization. The initial ferroxidase reaction rate of recombinant Chaetopterus ferritin (ChF) is 8-fold faster than that of recombinant human heavy-chain ferritin (HuHF). To our knowledge, this protein exhibits the fastest catalytic performance ever described for a ferritin variant. In addition to the high-velocity ferroxidase activity, ChF is unique in that it is secreted by Chaetopterus in a bioluminescent mucus. Previous work has linked the availability of Fe2+ to this long-lived bioluminescence, suggesting a potential function for the secreted ferritin. Comparative biochemical analyses indicated that both ChF and HuHF showed similar behavior toward changes in pH, temperature, and salt concentration. Comparison of their crystal structures shows no significant differences in the catalytic sites. Notable differences were found in the residues that line both 3-fold and 4-fold pores, potentially leading to increased flexibility, reduced steric hindrance, or a more efficient pathway for Fe2+ transportation to the ferroxidase site. These suggested residues could contribute to the understanding of iron translocation through the ferritin shell to the ferroxidase site.

Hsiung, BK, Siddique RH, Stavenga DG, Otto JC, Allen MC, Liu Y, Lu YF, Deheyn DD, Shawkey MD, Blackledge TA.  2017.  Rainbow peacock spiders inspire miniature super-iridescent optics. Nature Communications. 8   10.1038/s41467-017-02451-x   AbstractWebsite

Colour produced by wavelength-dependent light scattering is a key component of visual communication in nature and acts particularly strongly in visual signalling by structurally-coloured animals during courtship. Two miniature peacock spiders (Maratus robinsoni and M. chrysomelas) court females using tiny structured scales (similar to 40 x 10 mu m(2)) that reflect the full visual spectrum. Using TEM and optical modelling, we show that the spiders' scales have 2D nanogratings on microscale 3D convex surfaces with at least twice the resolving power of a conventional 2D diffraction grating of the same period. Whereas the long optical path lengths required for light-dispersive components to resolve individual wavelengths constrain current spectrometers to bulky sizes, our nano-3D printed prototypes demonstrate that the design principle of the peacock spiders' scales could inspire novel, miniature light-dispersive components.

Weigand, WJ, Messmore A, Tu J, Morales-Sanz A, Blair DL, Deheyn DD, Urbach JS, Robertson-Anderson RM.  2017.  Active microrheology determines scale-dependent material properties of Chaetopterus mucus. Plos One. 12   10.1371/journal.pone.0176732   AbstractWebsite

We characterize the lengthscale-dependent rheological properties of mucus from the ubiquitous Chaetopterus marine worm. We use optically trapped probes (2-10 mu m) to induce microscopic strains and measure the stress response as a function of oscillation amplitude. Our results show that viscoelastic properties are highly dependent on strain scale (l), indicating three distinct lengthscale-dependent regimes at l(1)<= 4 mu m, l(2)approximate to 4-10 mu m, and l(3)>= 10 mu m. While mucus response is similar to water for l(1), suggesting that probes rarely contact the mucus mesh, the response for l(2) is distinctly more viscous and independent of probe size, indicative of continuum mechanics. Only for l(3) does the response match the macroscopic elasticity, likely due to additional stiffer constraints that strongly resist probe displacement. Our results suggest that, rather than a single lengthscale governing crossover from viscous to elastic, mucus responds as a hierarchical network with a loose biopolymer mesh coupled to a larger scaffold responsible for macroscopic gel-like mechanics.

Lowder, KB, Allen MC, Day JMD, Deheyn DD, Taylor JRA.  2017.  Assessment of ocean acidification and warming on the growth, calcification, and biophotonics of a California grass shrimp. Ices Journal of Marine Science. 74:1150-1158.   10.1093/icesjms/fsw246   AbstractWebsite

Cryptic colouration in crustaceans, important for both camouflage and visual communication, is achieved through physiological and morphological mechanisms that are sensitive to changes in environmental conditions. Consequently, ocean warming and ocean acidification can affect crustaceans' biophotonic appearance and exoskeleton composition in ways that might disrupt colouration and transparency. In the present study, we measured growth, mineralization, transparency, and spectral reflectance (colouration) of the caridean grass shrimp Hippolyte californiensis in response to pH and temperature stressors. Shrimp were exposed to ambient pH and temperature (pH 8.0, 17 degrees C), decreased pH (pH 7.5, 17 degrees C), and decreased pH/increased temperature (pH 7.5, 19 degrees C) conditions for 7 weeks. There were no differences in either Mg or Ca content in the exoskeleton across treatments nor in the transparency and spectral reflectance. There was a small but significant increase in percent growth in the carapace length of shrimp exposed to decreased pH/increased temperature. Overall, these findings suggest that growth, calcification, and colour of H. californiensis are unaffected by decreases of 0.5 pH units. This tolerance might stem from adaptation to the highly variable pH environment that these grass shrimp inhabit, highlighting the multifarious responses to ocean acidification, within the Crustacea.

Tresguerres, M, Barott K, Barron ME, Deheyn D, Kline D, Linsmayer LB.  2017.  Cell Biology of Reef-Building Corals: Ion Transport, Acid/Base Regulation, and Energy Metabolism. Acid-Base Balance and Nitrogen Excretion in Invertebrates. ( Weihrauch D, O'Donnell M, Eds.).:193-218.: Springer International Publishing   10.1007/978-3-319-39617-0_7   Abstract

Coral reefs are built by colonial cnidarians that establish a symbiotic relationship with dinoflagellate algae of the genus Symbiodinium. The processes of photosynthesis, calcification, and general metabolism require the transport of diverse ions across several cellular membranes and generate waste products that induce acid/base and oxidative stress. This chapter reviews the current knowledge on coral cell biology with a focus on ion transport and acid/base regulation while also discussing related aspects of coral energy metabolism.

Colvin, MA, Hentschel BT, Deheyn DD.  2016.  Combined effects of water flow and copper concentration on the feeding behavior, growth rate, and accumulation of copper in tissue of the infaunal polychaete Polydora cornuta. Ecotoxicology. 25:1720-1729.   10.1007/s10646-016-1705-z   AbstractWebsite

We performed an experiment in a laboratory flume to test the effects of water flow speed and the concentration of aqueaous copper on the feeding behavior, growth rate, and accumulation of copper in the tissues of juvenile polychaetes Polydora cornuta. The experiment included two flow speeds (6 or 15 cm/s) and two concentrations of added copper (0 or 85 mu g/L). Worms grew significantly faster in the faster flow and in the lower copper concentration. In the slower flow, the total time worms spent feeding decreased significantly as copper concentration increased, but copper did not significantly affect the time worms spent feeding in the faster flow. Across all treatments, there was a significant, positive relationship between the time individuals spent feeding and their relative growth rate. Worms were observed suspension feeding significantly more often in the faster flow and deposit feeding significantly more often in the slower flow, but copper concentration did not affect the proportion of time spent in either feeding mode. The addition of 85 mu g/L copper significantly increased copper accumulation in P. cornuta tissue, but the accumulation did not differ significantly due to flow speed. There was a significant interaction between copper and flow; the magnitude of the difference in copper accumulation between the 0 and 85 mu g/L treatments was greater in the faster flow than in the slower flow. In slow flows that favor deposit feeding, worms grow slowly and accumulate less copper in their tissue than in faster flows that favor suspension feeding and faster growth.

deVries, MS, Webb SJ, Tu J, Cory E, Morgan V, Sah RL, Deheyn DD, Taylor JRA.  2016.  Stress physiology and weapon integrity of intertidal mantis shrimp under future ocean conditions. Scientific Reports. 6   10.1038/srep38637   AbstractWebsite

Calcified marine organisms typically experience increased oxidative stress and changes in mineralization in response to ocean acidification and warming conditions. These effects could hinder the potency of animal weapons, such as the mantis shrimp's raptorial appendage. The mechanical properties of this calcified weapon enable extremely powerful punches to be delivered to prey and aggressors. We examined oxidative stress and exoskeleton structure, mineral content, and mechanical properties of the raptorial appendage and the carapace under long-term ocean acidification and warming conditions. The predatory appendage had significantly higher % Mg under ocean acidification conditions, while oxidative stress levels as well as the % Ca and mechanical properties of the appendage remained unchanged. Thus, mantis shrimp tolerate expanded ranges of pH and temperature without experiencing oxidative stress or functional changes to their weapons. Our findings suggest that these powerful predators will not be hindered under future ocean conditions.

Rawat, R, Deheyn DD.  2016.  Evidence that ferritin is associated with light production in the mucus of the marine worm Chaetopterus. Scientific Reports. 6   10.1038/srep36854   AbstractWebsite

The blue glow of the mucus from Chaetopterus involves a photoprotein, iron and flavins. Identity and respective role of these components remain, however, largely unresolved today, likely because of viscosity issues and inhibition of this system by oxidizers conventionally used to track bioluminescence activity. Here, we used gentle centrifugation to obtain a mucus supernatant showing no inhibition to oxidizers, allowing for further analysis. We applied conventional chromatographic techniques to isolate major proteins associated with light emission. Luminescence ability of elutriate fractions was tested with hydrogen peroxide to track photoprotein and/or protein-bound chromophore. Fractions producing light contained few major proteins, one with similarity to ferritin. Addition to the mucus of elements with inhibitory/potentiary effect on ferritin ferroxidase activity induced corresponding changes in light production, emphasizing the possible role of ferritin in the worm bioluminescence. DNA of the protein was cloned, sequenced, and expressed, confirming its identity to a Chaetopterus Ferritin (ChF). Both ferric and ferrous iron were found in the mucus, indicating the occurrence of both oxidase and reductase activity. Biochemical analysis showed ChF has strong ferroxidase activity, which could be a source of biological iron and catalytic energy for the worm bioluminescence when coupled to a reduction process with flavins.

Holzinger, A, Allen MC, Deheyn DD.  2016.  Hyperspectral imaging of snow algae and green algae from aeroterrestrial habitats. Journal of Photochemistry and Photobiology B-Biology. 162:412-420.   10.1016/j.jphotobiol.2016.07.001   AbstractWebsite

Snow algae and green algae living in aeroterrestrial habitats are ideal objects to study adaptation to high light irradiation. Here, we used a detailed description of the spectral properties as a proxy for photo-acclimation/protection in snow algae (Chlamydomonas nivalis, Chlainomonas sp. and Chloromonas sp.) and charophyte green algae (Zygnema sp., Zygogonium ericetorum and Klebsormidium crenulatum). The hyperspectral microscopic mapping and imaging technique allowed us to acquire total absorption spectra of these microalgae in the waveband of 400-900 nm. Particularly in Chlamydomonas nivalis and Chlainomonas sp., a high absorbance between 400550 nm was observed, due to naturally occurring secondary carotenoids; in Chloromonas sp. and in the charopyhte algae this high absorbance was missing, the latter being close relatives to land plants. To investigate if cellular water loss has an influence on the spectral properties, the cells were plasmolysed in sorbitol or desiccated at ambient air. While in snow algae, these treatments did hardly change the spectral properties, in the charopyhte algae the condensation of the cytoplasm and plastids increased the absorbance in the lower waveband of 400-500 nm. These changes might be ecologically relevant and photoprotective, as aeroterrestrial algae are naturally exposed to occasional water limitation, leading to desiccation, which are conditions usually occurring together with higher irradiation. (C) 2016 The Authors. Published by Elsevier B.V.

Yue, JX, Holland ND, Holland LZ, Deheyn DD.  2016.  The evolution of genes encoding for green fluorescent proteins: insights from cephalochordates (amphioxus). Scientific Reports. 6   10.1038/srep28350   AbstractWebsite

Green Fluorescent Protein (GFP) was originally found in cnidarians, and later in copepods and cephalochordates (amphioxus) (Branchiostoma spp). Here, we looked for GFP-encoding genes in Asymmetron, an early-diverged cephalochordate lineage, and found two such genes closely related to some of the Branchiostoma GFPs. Dim fluorescence was found throughout the body in adults of Asymmetron lucayanum, and, as in Branchiostoma floridae, was especially intense in the ripe ovaries. Spectra of the fluorescence were similar between Asymmetron and Branchiostoma. Lineage-specific expansion of GFP-encoding genes in the genus Branchiostoma was observed, largely driven by tandem duplications. Despite such expansion, purifying selection has strongly shaped the evolution of GFP-encoding genes in cephalochordates, with apparent relaxation for highly duplicated clades. All cephalochordate GFP-encoding genes are quite different from those of copepods and cnidarians. Thus, the ancestral cephalochordates probably had GFP, but since GFP appears to be lacking in more early-diverged deuterostomes (echinoderms, hemichordates), it is uncertain whether the ancestral cephalochordates (i.e. the common ancestor of Asymmetron and Branchiostoma) acquired GFP by horizontal gene transfer (HGT) from copepods or cnidarians or inherited it from the common ancestor of copepods and deuterostomes, i.e. the ancestral bilaterians.

Gruber, DF, Loew ER, Deheyn DD, Akkaynak D, Gaffney JP, Smith WL, Davis MP, Stern JH, Pieribone VA, Sparks JS.  2016.  Biofluorescence in catsharks (Scyliorhinidae): Fundamental description and relevance for elasmobranch visual ecology. Scientific Reports. 6   10.1038/srep24751   AbstractWebsite

Biofluorescence has recently been found to be widespread in marine fishes, including sharks. Catsharks, such as the Swell Shark (Cephaloscyllium ventriosum) from the eastern Pacific and the Chain Catshark (Scyliorhinus retifer) from the western Atlantic, are known to exhibit bright green fluorescence. We examined the spectral sensitivity and visual characteristics of these reclusive sharks, while also considering the fluorescent properties of their skin. Spectral absorbance of the photoreceptor cells in these sharks revealed the presence of a single visual pigment in each species. Cephaloscyllium ventriosum exhibited a maximum absorbance of 484 +/- 3 nm and an absorbance range at half maximum (lambda(1/2max)) of 440-540 nm, whereas for S. retifer maximum absorbance was 488 +/- 3 nm with the same absorbance range. Using the photoreceptor properties derived here, a "shark eye" camera was designed and developed that yielded contrast information on areas where fluorescence is anatomically distributed on the shark, as seen from other sharks' eyes of these two species. Phylogenetic investigations indicate that biofluorescence has evolved at least three times in cartilaginous fishes. The repeated evolution of biofluorescence in elasmobranchs, coupled with a visual adaptation to detect it; and evidence that biofluorescence creates greater luminosity contrast with the surrounding background, highlights the potential importance of biofluorescence in elasmobranch behavior and biology.

Lin, HS, Allen MC, Wu J, deGlee BM, Shin D, Cai Y, Sandhage KH, Deheyn DD, Meredith JC.  2015.  Bioenabled core/shell microparticles with tailored multimodal adhesion and optical reflectivity. Chemistry of Materials. 27:7321-7330.   10.1021/acs.chemmater.5b02782   AbstractWebsite

Nature provides remarkable examples of mass-produced microscale particles with structures and chemistries optimized by evolution for particular functions. Synthetic chemical tailoring of such sustainable biogenic particles may be used to generate new multifunctional materials. Herein, we report a facile method for the development of bioenabled core/shell microparticles consisting of surface-modified ragweed pollen with a magnetic core, for which both multimodal adhesion and optical reflectivity can be tailored. Adhesion of the magnetic-core pollen can be tuned, relative to native pollen, through the combination of tailorable short-range interactions (over similar to 5 nm, via van der Waals forces and hydrogen bonding), an intermediate-range (over several mu m) capillary force, and long-range (over similar to 1 mm) magnetic attraction. The magnetic force could be controlled by the amount of iron oxide loaded within the core of the pollen particle, while the short-range interactions and capillary force can be tuned by coating with polystyrene nanoparticles and/or a layer of viscous pollenkitt on the exine shell surface. Such coatings were also used to tailor the optical reflectance of the magnetic pollen particles; that is, the light-reflectance intensity was enhanced by coating with pollenkitt and significantly reduced by coating with polystyrene nanoparticles. This approach for generating multifunctional core/shell microparticles with tailorable adhesion and optical reflectivity may be extended to other pollen or biological particles or to synthetic biomimetic particles. Such independent control of the core and shell chemistries enabled by this approach also allows for the generation of microparticles with a variety of combination in functions tailorable to other properties.

Taylor, JRA, Gilleard JM, Allen MC, Deheyn DD.  2015.  Effects of CO2-induced pH reduction on the exoskeleton structure and biophotonic properties of the shrimp Lysmata californica. Scientific Reports. 5   10.1038/srep10608   AbstractWebsite

The anticipated effects of CO2-induced ocean acidification on marine calcifiers are generally negative, and include dissolution of calcified elements and reduced calcification rates. Such negative effects are not typical of crustaceans for which comparatively little ocean acidification research has been conducted. Crustaceans, however, depend on their calcified exoskeleton for many critical functions. Here, we conducted a short-term study on a common caridean shrimp, Lysmata californica, to determine the effect of CO2-driven reduction in seawater pH on exoskeleton growth, structure, and mineralization and animal cryptic coloration. Shrimp exposed to ambient (7.99 +/- 0.04) and reduced pH (7.53 +/- 0.06) for 21 days showed no differences in exoskeleton growth (percent increase in carapace length), but the calcium weight percent of their cuticle increased significantly in reduced pH conditions, resulting in a greater Ca:Mg ratio. Cuticle thickness did not change, indicating an increase in the mineral to matrix ratio, which may have mechanical consequences for exoskeleton function. Furthermore, there was a 5-fold decrease in animal transparency, but no change in overall shrimp coloration (red). These results suggest that even short-term exposure to CO2-induced pH reduction can significantly affect exoskeleton mineralization and shrimp biophotonics, with potential impacts on crypsis, physical defense, and predator avoidance.

Yates, KK, Turley C, Hopkinson BM, Todgham AE, Cross JN, Greening H, Williamson P, Van Hooidonk R, Deheyn DD, Johnson Z.  2015.  Transdisciplinary science: A path to understanding the interactions among ocean acidification, ecosystem, and society. Oceanography. 28:212-225.   10.5670/oceanog.2015.43   AbstractWebsite

The global nature of ocean acidification (OA) transcends habitats, ecosystems, regions, and science disciplines. The scientific community recognizes that the biggest challenge in 'improving understanding of how changing OA conditions affect ecosystems, and associated consequences for human society, requires integration of experimental, observational, and modeling approaches from many disciplines over a wide range of temporal and spatial scales. Such transdisciplinary science is the next step in providing relevant, meaningful results and optimal guidance to policymakers and coastal managers. We discuss the challenges associated with integrating ocean acidification science across funding agencies, institutions, disciplines, topical areas, and regions, and the value of unifying science objectives and activities to deliver-insights into local, regional, and global scale impacts. We identify guiding principles and strategies for developing transdisciplinary research in the ocean acidification science community.

Xiao, M, Li YW, Allen MC, Deheyn DD, Yue XJ, Zhao JZ, Gianneschi NC, Shawkey MD, Dhinojwala A.  2015.  Bio-inspired structural colors produced via self-assembly of synthetic melanin nanoparticles. Acs Nano. 9:5454-5460.   10.1021/acsnano.5b01298   AbstractWebsite

Structural colors arising from interactions of light with submicron scale periodic structures have been found in many species across all taxa, serving multiple biological functions including sexual signaling, camouflage, and aposematism. Directly inspired by the extensive use of self-assembled melanosomes to produce colors in avian feathers, we set out to synthesize and assemble polydopamine-based synthetic melanin nanoparticles in an effort to fabricate colored films. We have quantitatively demonstrated that synthetic melanin nanoparticles have a high refractive index and broad absorption spanning across the UV-visible range, similar to natural melanins. Utilizing a thin-film interference model, we demonstrated the coloration mechanism of deposited films and showed that the unique optical properties of synthetic melanin nanoparticles provide advantages for structural colors over other polymeric nanoparticles (i.e., polystyrene colloidal particles).

Shah, DU, Vollrath F, Stires J, Deheyn DD.  2015.  The biocomposite tube of a chaetopterid marine worm constructed with highly-controlled orientation of nanofilaments. Materials Science & Engineering C-Materials for Biological Applications. 48:408-415.   10.1016/j.msec.2014.12.015   AbstractWebsite

The ultrastructure of the self-constructed tube housing of the bioluminescent marine worm, Chaetopterus sp. reveals that the bio-nanocomposite tube comprises of multiple non-woven plies of multi-axially oriented organic nanofilaments (empty set 50-1100 nm) cemented together by an unstructured organic matrix binder. The thin-walled, impermeable tubes are bin-inspirational for conventional pipe technology. Orientation distribution analyses revealed that the dominant orientation angles of nanofilaments in the tube were 0 degrees, +/- 45 degrees and +/- 65 degrees, which correlate well with optimal winding angles for 'man-made' fibre reinforced composite pipes subjected to specific loading conditions. Such a use of high aspect ratio nanofilaments in multi-axial laminates would impart toughness and flexibility to the tube structure, and facilitate rapid tube growth. While the tube production mechanism is not entirely known at this stage, our time-lapse studies show that, contrary to generic assumptions in literature, the worm actively, rapidly and sporadically produces and expands the tube. (C) 2014 Elsevier B.V. All rights reserved.

Zhang, Y, Allen MC, Zhao RY, Deheyn DD, Behrens SH, Meredith JC.  2015.  Capillary foams: Stabilization and functionalization of porous liquids and solids. Langmuir. 31:2669-2676.   10.1021/la504784h   AbstractWebsite

Liquid foams are two-phase systems in which a large volume of gas is dispersed as bubbles in a continuous liquid phase. These foams are ubiquitous in nature. In addition, they are found in industrial applications, such as pharmaceutical formulation, food processing, wastewater treatment, construction, and cosmetics. Recently, we reported a new type of foam material, capillary foam, which is stabilized by the synergistic action of particles and a small amount of an immiscible secondary liquid. In this study, we explore in more detail the foam preparation routes. To illustrate some of the potential applications, we create vividly colored wet and dried foams, which are difficult to prepare using traditional methods, and load-bearing porous solids. The combined action of particles and immiscible secondary fluid confers exceptional stability to capillary foams and many options for functionalization, suggesting a wide range of possible applications.

Shah, DU, Vollrath F, Porter D, Stires J, Deheyn DD.  2014.  Housing tubes from the marine worm Chaetopterus sp.: biomaterials with exceptionally broad thermomechanical properties. Journal of the Royal Society Interface. 11   10.1098/rsif.2014.0525   AbstractWebsite

The housing tube material of the marine worm Chaetopterus sp. exhibits thermal stability up to 250 degrees C, similar to other biological materials such as mulberry silkworm cocoons. Interestingly, however, dynamic mechanical thermal analysis conducted in both air and water elucidated the lack of a glass transition in the organic tube wall material. In fact, the viscoelastic properties of the anhydrous and undried tube were remarkably stable (i.e. constant and reversible) between -75 degrees C and 200 degrees C in air, and 5 degrees C and 75 degrees C in water, respectively. Moreover, it was found that hydration and associated-water plasticization were key to the rubber-like flexible properties of the tube; dehydration transformed the material behaviour to glass-like. The tube is made of bionanocomposite fibrils in highly oriented arrangement, which we argue favours the biomaterial to be highly crystalline or cross-linked, with extensive hydrogen and/or covalent bonds. Mechanical property characterization in the longitudinal and transverse directions ascertained that the tubes were not quasi-isotropic structures. In general, the higher stiffness and strength in the transverse direction implied that there were more nanofibrils orientated at +/- 45 degrees and +/- 65 degrees than at 0 degrees to the tube axis. The order of the mechanical properties of the soft-tough tubes was similar to synthetic rubber-like elastomers and even some viscid silks. The complex structure-property relations observed indicated that the worm has evolved to produce a tubular housing structure which can (i) function stably over a broad range of temperatures, (ii) endure mechanical stresses from specific planes/axes, and (iii) facilitate rapid growth or repair.

Bomati, EK, Haley JE, Noel JP, Deheyn DD.  2014.  Spectral and structural comparison between bright and dim green fluorescent proteins in Amphioxus. Scientific Reports. 4   10.1038/srep05469   AbstractWebsite

The cephalochordate Amphioxus naturally co-expresses fluorescent proteins (FPs) with different brightness, which thus offers the rare opportunity to identify FP molecular feature/s that are associated with greater/lower intensity of fluorescence. Here, we describe the spectral and structural characteristics of green FP (bfloGFPa1) with perfect (100%) quantum efficiency yielding to unprecedentedly-high brightness, and compare them to those of co-expressed bfloGFPc1 showing extremely-dim brightness due to low (0.1%) quantum efficiency. This direct comparison of structure-function relationship indicated that in the bright bfloGFPa1, a Tyrosine (Tyr159) promotes a ring flipping of a Tryptophan (Trp157) that in turn allows a cis-trans transformation of a Proline (Pro55). Consequently, the FP chromophore is pushed up, which comes with a slight tilt and increased stability. FPs are continuously engineered for improved biochemical and/or photonic properties, and this study provides new insight to the challenge of establishing a clear mechanistic understanding between chromophore structural environment and brightness level.

Branchini, BR, Behney CE, Southworth TL, Rawat R, Deheyn DD.  2014.  Chemical analysis of the luminous slime secreted by the marine worm Chaetopterus (annelida, polychaeta). Photochemistry and Photobiology. 90:247-251.   10.1111/php.12169   AbstractWebsite

The marine annelid Chaetopterus variopedatus produces bioluminescence by an unknown and potentially novel mechanism. We have advanced the study of this fascinating phenomenon, which has not been investigated for nearly 60years after initial studies were first reported for this species. Here, we show that the luminous slime produced by the worm exhibits blue fluorescence that matches the bioluminescence emission. This result suggests that the oxyluciferin emitter is present. However, while the blue fluorescence decays over time green fluorescence is increasingly revealed that is likely associated with products of the luminescence reaction. LC/MS and fluorescence analysis of harvested luminescent material revealed riboflavin as the major green fluorescent component. Riboflavin is usually associated with the mechanism of light production in bacteria, yet luminous bacteria were not found in the worm mucus, and accordingly were not reported to be directly responsible for the light emission, which is under nervous control in the worm. We therefore propose a hypothesis in which riboflavin or a structurally related derivative serves as the emitter in the worm's light producing reaction.

Roth, MS, Fan TY, Deheyn DD.  2013.  Life History Changes in Coral Fluorescence and the Effects of Light Intensity on Larval Physiology and Settlement in Seriatopora hystrix. Plos One. 8   10.1371/journal.pone.0059476   AbstractWebsite

Fluorescence is common in both coral adult and larval stages, and is produced by fluorescent proteins that absorb higher energy light and emit lower energy light. This study investigated the changes of coral fluorescence in different life histo stages and the effects of parental light environment on larval fluorescence, larval endosymbiotic dinoflagellate abundance, larval size and settlement in the brooding coral Seriatopora hystrix. Data showed that coral fluorescence changed during development from green in larvae to cyan in adult colonies. In larvae, two green fluorescent proteins (GFPs) co-occur where the peak emission of one GFP overlaps with the peak excitation of the second GFP allowing the potential for energy transfer. Coral larvae showed great variation in GFP fluorescence, dinoflagellate abundance, and size. There was no obvious relationship between green fluorescence intensity and dirioflagellate abundance, green fluorescence intensity and larval size, or dinoflagellate abundance and larval size. Larvae of parents from high and low light treatments showed similar green fluorescence intensity, yet small but significant differences in size, dinoflagellate abundance, and settlement. The large variation in larval physiology combined with subtle effects of parental environment on larval characteristics seem to indicate that even though adult corals produce larvae with a wide range of physiological capacities, these larvae can still show small preferences for settling in similar habitats as their parents. These data highlight the importance of environmental conditions at the onset of life history and parent colony effects on coral larvae.

Gieskes, JM, Elwany H, Rasmussen L, Han S, Rathburn A, Deheyn DD.  2013.  Salinity variations in the Venice Lagoon, Italy: Results from the SIOSED Project, May 2005–February 2007. Marine Chemistry. 154:77-86.   AbstractWebsite

As a component of the Scripps Institution of Oceanography Sediment Research Project (SIOSED) in the Venice Lagoon, we studied the variability of the salinity regime with time at three principal locations in the south-central part of the Lagoon. We carried out measurements of salinity near the bottom of the Lagoon at these stations, as well as measurements of the chloride concentrations of the sedimentary pore fluids with depth into the sediments. The principal aim of these combined studies was to examine the relationship between the chloride contents of the overlying waters with those in the pore fluids. Salinity variations were measured several times over month-long periods during the SIOSED program. Occasionally these measurements overlapped with the taking of sediment cores from which pore fluids were extracted for studies of interstitial water chemistry. Generally chloride concentrations in the upper 2–4 cm of the sediments reflected the average chlorides in the overlying water column, estimated from average salinities measured over the sites of the cores, notwithstanding the short-term variability of the salinities as a function of tidal currents. Chloride concentration-depth profiles are interpreted in terms of exchange with overlying waters as well as in terms of potential influences of underlying aquifers. Though cores were taken at a higher frequency than the salinity measurements, we feel justified to use this data set together with the pore fluid data in recording the time change in chlorides of the near-bottom waters of two major SIOSED sites from May 2005 through February 2007. Results provide a better understanding of the salinity dynamics of the Venice Lagoon, and revealed that deep pore water gradients in salinity likely reflect diffusive exchange with underlying freshwater aquifers. These findings highlight the need for additional long cores, and will guide subsequent geochemical investigations of the Lagoon. Indications of the influences of aquifers on pore waters will help prevent misinterpretation of pore water trends as indications of gradual changes in the salinity of the tidal prism over time.

Deheyn, DD, Enzor LA, Dubowitz A, Urbach JS, Blair D.  2013.  Optical and physicochemical characterization of the luminous mucous secreted by the marine worm Chaetopterus sp. Physiological and Biochemical Zoology. 86:702-715.   10.1086/673869   AbstractWebsite

Bioluminescence of the marine worm Chaetopterus variopedatus was first investigated several decades ago mainly using tissue extract. Light production of the worm, however, originates from a secreted mucus only. Here, we report the optical and physicochemical properties of the luminous mucus. We show that the produced light occurs as a long glow in the blue range (455 nm), which is an unusual color for a shallow benthic invertebrate. We also show that the light originates from a photoprotein whose light production is independent of molecular oxygen yet somewhat related to the physicochemical (rheological) characteristics of the mucus itself. Indeed, the mucus seems to polymerize and become more viscous on exposure to H2O2, which in turn seems to inhibit the light production. Ferrous iron was not associated with any strong stimulatory effect. This is in contrast to past studies on worm tissues showing that the light production is strongly stimulated by H2O2 and ferrous iron. Overall, our results highlight the fact that working on the luminous mucus only (vs. worm tissues) provides the ability to study its chemical properties possibly involved in the fine control of light productionas well as its rheological propertiesand identify the possible interactions between these two properties.

Roth, MS, Deheyn DD.  2013.  Effects of cold stress and heat stress on coral fluorescence in reef-building corals. 3: Macmillan Publishers Limited. All rights reserved   10.1038/srep01421   AbstractWebsite

Widespread temperature stress has caused catastrophic coral bleaching events that have been devastating for coral reefs. Here, we evaluate whether coral fluorescence could be utilized as a noninvasive assessment for coral health. We conducted cold and heat stress treatments on the branching coral Acropora yongei, and found that green fluorescent protein (GFP) concentration and fluorescence decreased with declining coral health, prior to initiation of bleaching. Ultimately, cold-treated corals acclimated and GFP concentration and fluorescence recovered. In contrast, heat-treated corals eventually bleached but showed strong fluorescence despite reduced GFP concentration, likely resulting from the large reduction in shading from decreased dinoflagellate density. Consequently, GFP concentration and fluorescence showed distinct correlations in non-bleached and bleached corals. Green fluorescence was positively correlated with dinoflagellate photobiology, but its closest correlation was with coral growth suggesting that green fluorescence could be used as a physiological proxy for health in some corals.

Rezaie-Boroon, MH, Diaz S, Torres V, Lazzaretto T, Deheyn DD.  2013.  Coupling between the changes in co2 concentration and sediment biogeochemistry in mudflat of Salinas de San Pedro, California, USA. Journal of Environmental Protection. 4:1173-1180.   Abstract

We investigated the effects of elevated carbon dioxide (CO2) on biogeochemistry of marsh sediment including speciation of selected heavy metals in Salinas de San Pedro mudflat in California. The Salinas de San Pedro mudflat has higher carbon (C) content than the vast majority of fully-vegetated salt marshes even with the higher tidal action in the mudflat. Sources for CO2 were identified as atmospheric CO2 as well as due to local fault degassing process. We measured carbon dioxide, methane, total organic carbon, dissolved oxygen, salinity, and heavy metal concentration in various salt marsh locations. Overall, our results showed that CO2 concentration ranging from 418.7 to 436.9 (ppm), which are slightly different in various chambers but are in good agreement with some heavy metal concentrations values in mudflat at or around the same location. The selected metal concentration values (ppm) ranging from 0.003 - 0.011 (As); 0.001 - 0.005 (Cd); 0.04 - 0.02 (Cr); 0.13 - 0.38 (Cu); 0.11 - 0.38 (Pb); 0.0009 - 0.020 (Se); and 0.188 - 0.321 (Zn). The low dissolved oxygen (ppm) in the pore water sediment indicated suboxic environment. Additionally, CO2 (ppm) and loss on ignition (LOI) (%) correlated inversely; the higher CO2 content, the lower was the LOI (%); that is to say the excess CO2 causes higher rates of decomposition and therefore it leads to lower LOI (%) on the mudflat surface. It appears that the elevated CO2 makes changes in salt marsh pore water chemistry for instance the free ionic metal (Cu2+, Pb2+, etc.) speciation is one of the most reactive form because simply assimilated by the non-decayed or alive organisms in sediment of salt marsh and/or in water. This means that CO2 not only is a sign of improvement in plant productivity, but also activates microbial decomposition through increases in dissolved organic carbon availability. CO2 also increases acidification processes such as anaerobic degradation of microorganism and oxidation of reduced components. The heavy metal concentrations in sediment samples were slightly higher in suboxic layer, yet it appears that salt marsh sediments in Salinas de San Pedro act like a sink for nutrient and carbon by maximizing carbon sequestration.