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ArticleOptimizing seaweed biomass production—A two kelp solution(Springer, 2024-07-02)Interest in farming kelps has grown beyond using kelp for food, feed or biofuels. There is considerable interest in generating biomass from seaweed for use in bioplastics and other products that would substitute for petroleum-derived products. For these uses to be viable, large amounts of biomass are needed. Very large kelp farms can be expensive to build and maintain, leading to the need to optimize the biomass per unit area. Although close spacing of growlines can lead to poor growth, a viable approach may be to grow two species of kelps together: one that hangs down and one that is buoyant, growing up. This system would increase the spacing in three dimensions. In Alaska, Saccharina latissima is commonly grown hanging down from longlines. One of the buoyant Alaskan kelps is Nereocystis luetkeana. Because there are commercial uses for wild-harvested Nereocystis in Alaska, we undertook a preliminary trial in Kodiak, Alaska, that grew both Saccharina and Nereocystis in the same longline array. Closely spaced lines were seeded the first week of February 2023 and set at 3 m below the surface. The arrays were harvested in late June 2023. Total yields were greatest on the combined arrays, followed by the Nereocystis only and Saccharina only arrays. Despite having 45% fewer grow-lines, the total yield of the Nereocystis on the combined arrays was statistically similar to the Nereocystis only arrays. These results may have significance for large scale macroalgal production.
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ArticleAcute introduction of phosphoserine-129 α-synuclein induces severe swelling of mitochondria at lamprey synapses(Caltech Library, 2024-05-23)Abnormal synaptic aggregation of α-synuclein is linked to cognitive deficits in Parkinson’s disease (PD). While the impacts of excess α-synuclein on synaptic function are well established, comparatively less is known about the effects on local mitochondria. Here, we examined morphological features of synaptic mitochondria treated with wild type (WT) or phosphoserine 129 (pS129) α-synuclein, a variant with prominent synaptic accumulation in PD. Acute introduction of pS129 α-synuclein to lamprey synapses caused an activity-dependent swelling and bursting of mitochondria, which did not occur with WT α-synuclein. These pS129-induced effects on mitochondria likely contribute to the synaptic deficits observed in PD.
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ArticleLarval development of Holothuria tubulosa, a new tractable system for evo-devo(Frontiers Media, 2024-05-24)To explore animal diversity, new experimentally tractable organisms must be established. Echinoderms include five groups of marine animals that have been used as developmental models for over a century thanks to their low costs, high fecundity, optically clear larvae and genetic tractability. An additional advantage of echinoderms is that their larval forms display diverse morphologies. This rich diversity enables comparative studies to investigate the evolutionary relationships among cell types, tissues, and organs. However, reproducible protocols to obtain gametes, detailed information on embryogenesis, and genomic tools have been optimized only for selected species of sea urchins and sea stars. To address this gap, we established the abundant Mediterranean sea cucumber Holothuria tubulosa as a new experimental system. Here we describe a method to reliably obtain gametes and make embryonic cultures multiple times from the same animal and characterize unique larval tissues combining immunohistochemistry and high-resolution microscopy. This work represents a step forward in our understanding of holothurian development and establishes H. tubulosa as an emerging experimental system for evo-devo and other biological disciplines.
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ArticleStudying regeneration through history as a way of looking forward(Springer, 2024-03-19)2024 is a good year for celebrating history of science. First comes the 100th year of the History of Science Society (HSS). Historian of Science George Sarton played a major role in establishing the Society, and he had clear views about what the field should include. He insisted that “the chief requisite for the making of a good chicken pie is chicken; nay, no amount of culinary legerdemain can make up for the lack of chicken. In the same way, the chief requisite for the history of science is intimate scientific knowledge; no amount of philosophic legerdemain can make up for its absence” (Sarton 1918, p. 194). From the beginning of the HSS, then, science played a central role. When one of us (Maienschein) served as HSS president in 2008–2009, she worked to include science and scientists in committees and activities, and the following president Paul Farber did as well. 2024 is also a new beginning for the Journal of the History of Biology (JHB), with editors Betty Smocovitis and Nic Rasmussen at the helm since 2023. This journal, begun by Everett Mendelsohn and supported by Ernst Mayr, was always steeped in science. Mendelsohn explained that he started the journal and remained editor for 31 years to provide a place for historians of biology, with their interests in the ideas and practices of biological sciences, to publish (Mendelsohn 1968). Smocovitis and Rasmussen are carrying on the tradition of embedding the history with the science, so that the historical work the journal publishes is useful to both historians and biologists. Shortly before he died early in 2023, Mendelsohn told Maienschein that he was pleased with the continued emphasis on science along with history. We may also point to the International Society for the History, Philosophy, and Social Studies of Biology (fondly known as Ishkabibble, or ISH for short) as a conjunction for history and science, along with its complementary fields. In 2024, JHB co-editor-in chief Smocovitis has become the president of ISH, MacCord is the program co-chair, and Maienschein is proud to have served as the first president for this organization and its embrace of science and the several fields that study it. At this time when science is under attack politically, and history is often (falsely) considered irrelevant to current pressing issues, it is all the more important that we look at ways that history and science can work together. They can nudge each other to ask new questions, explore new areas, and thereby enhance and enrich both domains. History can be at once for science, with science, about science, and part of science, as we explain in the context of one particular example below. Looking at history and science simultaneously helps us look forward with perspective and reflection.
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ArticleOrientation-independent-DIC imaging reveals that a transient rise in depletion attraction contributes to mitotic chromosome condensation(National Academy of Sciences, 2024-08-27)Genomic information must be faithfully transmitted into two daughter cells during mitosis. To ensure the transmission process, interphase chromatin is further condensed into mitotic chromosomes. Although protein factors like condensins and topoisomerase IIα are involved in the assembly of mitotic chromosomes, the physical bases of the condensation process remain unclear. Depletion attraction/macromolecular crowding, an effective attractive force that arises between large structures in crowded environments around chromosomes, may contribute to the condensation process. To approach this issue, we investigated the “chromosome milieu” during mitosis of living human cells using an orientation-independent-differential interference contrast module combined with a confocal laser scanning microscope, which is capable of precisely mapping optical path differences and estimating molecular densities. We found that the molecular density surrounding chromosomes increased with the progression from prophase to anaphase, concurring with chromosome condensation. However, the molecular density went down in telophase, when chromosome decondensation began. Changes in the molecular density around chromosomes by hypotonic or hypertonic treatment consistently altered the condensation levels of chromosomes. In vitro, native chromatin was converted into liquid droplets of chromatin in the presence of cations and a macromolecular crowder. Additional crowder made the chromatin droplets stiffer and more solid-like. These results suggest that a transient rise in depletion attraction, likely triggered by the relocation of macromolecules (proteins, RNAs, and others) via nuclear envelope breakdown and by a subsequent decrease in cell volumes, contributes to mitotic chromosome condensation, shedding light on a different aspect of the condensation mechanism in living human cells.
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ArticleLRRK2 kinase activity is necessary for development and regeneration in Nematostella vectensis(BMC, 2024-08-08)The starlet sea anemone, Nematostella vectensis, is an emerging model organism with a high regenerative capacity, which was recently found to possess an orthologue to the human Leucine Rich Repeat Kinase 2 (LRRK2) gene. Mutations in this gene are the most common cause of inherited Parkinson’s Disease (PD), highlighting the importance of understanding its function. Despite two decades of research, however, the function of LRRK2 is not well established. To investigate the function of LRRKs in Nematostella vectensis, we applied small molecule inhibitors targeting the kinase activity of LRRK2 to examine its function in development, homeostasis and regeneration in Nematostella vectensis. In vivo analyses inhibiting the kinase function of this enzyme demonstrated a role of nvLRRK2 in development and regeneration of N. vectensis. These findings implicate a developmental role of LRRK2 in Nematostella, adding to the expanding knowledge of its physiological function. Our work introduces a new model organism with which to study LRRK biology. We report that LRRK kinase activity is necessary for the development and regeneration of Nematostella. Given the short generation time, genetic trackability and in vivo imaging capabilities, this work introduces Nematostella vectensis as a new model in which to study genes linked to neurodegenerative diseases such as Parkinson’s.
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ArticleSall4 regulates downstream patterning genes during limb regeneration(Elsevier, 2024-07-25)Many salamanders can completely regenerate a fully functional limb. Limb regeneration is a carefully coordinated process involving several defined stages. One key event during the regeneration process is the patterning of the blastema to inform cells of what they must differentiate into. Although it is known that many genes involved in the initial development of the limb are re-used during regeneration, the exact molecular circuitry involved in this process is not fully understood. Several large-scale transcriptional profiling studies of axolotl limb regeneration have identified many transcription factors that are up-regulated after limb amputation. Sall4 is a transcription factor that has been identified to play essential roles in maintaining cells in an undifferentiated state during development and also plays a unique role in limb development. Inactivation of Sall4 during limb bud development results in defects in anterior-posterior patterning of the limb. Sall4 has been found to be up-regulated during limb regeneration in both Xenopus and salamanders, but to date it function has been untested. We confirmed that Sall4 is up-regulated during limb regeneration in the axolotl using qRT-PCR and identified that it is present in the skin cells and also in cells within the blastema. Using CRISPR technology we microinjected gRNAs specific for Sall4 complexed with cas9 protein into the blastema to specifically knockout Sall4 in blastema cells only. This resulted in limb regenerate defects, including missing digits, fusion of digit elements, and defects in the radius and ulna. This suggests that during regeneration Sall4 may play a similar role in regulating the specification of anterior-proximal skeletal elements.
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ArticleVitelloTag: A tool for high-throughput cargo delivery into oocytes(The Company of Biologists, 2024-09-14)Delivering molecular tools into oocytes is essential for developmental and reproductive biology. Microinjection, the conventional method, is equipment intensive, often technically challenging and has a low yield, and is impractical in species with delicate oocytes or restricted spawning seasons. To overcome these limitations, we developed VitelloTag, a cost-effective, high-throughput system using vitellogenin-derived fusion proteins to enable efficient cargo delivery via receptor-mediated endocytosis. We demonstrate its utility by delivering Cas9/sgRNA complexes in two distantly related species for gene knockout.
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ArticleFrom pipette to palette: Bridging science and art at MBoC(American Society for Cell Biology, 2024-05-28)Science and art evoke two different worlds, with science thought of as objective and data driven, and art as subjective and expressive. Yet the practice and process of science and art bear many similarities. Both are centered on observation and description, and both involve experimentation to achieve tangible results. Molecular Biology of the Cell (MBoC) has recently initiated a project to bridge the worlds of science and art to generate a series of cover images for the journal.
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ArticleAnnelid adult cell type diversity and their pluripotent cellular origins(Nature Research, 2024-04-12)Many annelids can regenerate missing body parts or reproduce asexually, generating all cell types in adult stages. However, the putative adult stem cell populations involved in these processes, and the diversity of cell types generated by them, are still unknown. To address this, we recover 75,218 single cell transcriptomes of the highly regenerative and asexually-reproducing annelid Pristina leidyi. Our results uncover a rich cell type diversity including annelid specific types as well as novel types. Moreover, we characterise transcription factors and gene networks that are expressed specifically in these populations. Finally, we uncover a broadly abundant cluster of putative stem cells with a pluripotent signature. This population expresses well-known stem cell markers such as vasa, piwi and nanos homologues, but also shows heterogeneous expression of differentiated cell markers and their transcription factors. We find conserved expression of pluripotency regulators, including multiple chromatin remodelling and epigenetic factors, in piwi+ cells. Finally, lineage reconstruction analyses reveal computational differentiation trajectories from piwi+ cells to diverse adult types. Our data reveal the cell type diversity of adult annelids by single cell transcriptomics and suggest that a piwi+ cell population with a pluripotent stem cell signature is associated with adult cell type differentiation.
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ArticleManaging offshore multi-use settings: use of conceptual mapping to reduce uncertainty of co-locating seaweed aquaculture and wind farms(Elsevier, 2024-04-12)The offshore Multi-use Setting (MUS) is a concept that aims to co-locate marine industrial activities, including wind farms and aquaculture. MUS is considered an innovative approach to promoting efficiency in space and resource use whilst contributing global policy priorities. However, the impacts of MUS development across social, economic, and environmental domains are uncertain, hindering the commercialisation of the concept. In this study, we initially demonstrate the potential consequences of co-locating seaweed aquaculture and a wind farm as a step towards MUS. Using a hypothetical case study and modified Delphi methodology, 14 subject matter experts predicted potential outcomes across social and environmental objectives. Five Cognitive maps and impact tables of 58 potential consequences were generated based on experts' perspective on co-locating seaweed aquaculture and a wind farm. The findings highlight the potential to exasperate pressures in the area, including those already attributed to wind farm operations, such as species mortality and stakeholder conflict. However, it may also enhance social-ecological conditions, such as resource provisioning and promoting habitat functionality in the region, through the addition of seaweed aquaculture. The cognitive maps demonstrate the complexity of managing MUS implementation, where high degree of variability and uncertainty about the outcomes is present. The findings of this study provide the vital entry point to performing further integrative assessment and modelling approaches, such as probabilistic analysis and simulations, in support of MUS decision-making. The research also strongly recommends alternative strategies in the pursuit of combining seaweed production and wind farms to avoid significant financial (among many other) trade-offs and risks. More broadly, we have found that our approach's ability to visually represent a complex situation while considering multiple objectives could be immensely valuable for other bioeconomy innovations or nature-based solutions. It helps mitigate the potential for expensive investments without a comprehensive evaluation of the associated risks and negative impacts, as necessitated by the principles of sustainability in decision-making.
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ArticleSea cucumbers: an emerging system in evo-devo(BMC, 2024-02-17)A challenge for evolutionary developmental (evo-devo) biology is to expand the breadth of research organisms used to investigate how animal diversity has evolved through changes in embryonic development. New experimental systems should couple a relevant phylogenetic position with available molecular tools and genomic resources. As a phylum of the sister group to chordates, echinoderms extensively contributed to our knowledge of embryonic patterning, organ development and cell-type evolution. Echinoderms display a variety of larval forms with diverse shapes, making them a suitable group to compare the evolution of embryonic developmental strategies. However, because of the laboratory accessibility and the already available techniques, most studies focus on sea urchins and sea stars mainly. As a comparative approach, the field would benefit from including information on other members of this group, like the sea cucumbers (holothuroids), for which little is known on the molecular basis of their development. Here, we review the spawning and culture methods, the available morphological and molecular information, and the current state of genomic and transcriptomic resources on sea cucumbers. With the goal of making this system accessible to the broader community, we discuss how sea cucumber embryos and larvae can be a powerful system to address the open questions in evo-devo, including understanding the origins of bilaterian structures.
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ArticleInjury-induced cooperation of InhibinβA and JunB is essential for cell proliferation in Xenopus tadpole tail regeneration(Nature Research, 2024-02-14)In animal species that have the capability of regenerating tissues and limbs, cell proliferation is enhanced after wound healing and is essential for the reconstruction of injured tissue. Although the ability to induce cell proliferation is a common feature of such species, the molecular mechanisms that regulate the transition from wound healing to regenerative cell proliferation remain unclear. Here, we show that upon injury, InhibinβA and JunB cooperatively function for this transition during Xenopus tadpole tail regeneration. We found that the expression of inhibin subunit beta A (inhba) and junB proto-oncogene (junb) is induced by injury-activated TGF-β/Smad and MEK/ERK signaling in regenerating tails. Similarly to junb knockout (KO) tadpoles, inhba KO tadpoles show a delay in tail regeneration, and inhba/junb double KO (DKO) tadpoles exhibit severe impairment of tail regeneration compared with either inhba KO or junb KO tadpoles. Importantly, this impairment is associated with a significant reduction of cell proliferation in regenerating tissue. Moreover, JunB regulates tail regeneration via FGF signaling, while InhibinβA likely acts through different mechanisms. These results demonstrate that the cooperation of injury-induced InhibinβA and JunB is critical for regenerative cell proliferation, which is necessary for re-outgrowth of regenerating Xenopus tadpole tails.
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ArticleExcess phosphoserine-129 α-Synuclein induces synaptic vesicle trafficking and declustering defects at a Vertebrate Synapse(American Society for Cell Biology, 2023-11-22)α-Synuclein is a presynaptic protein that regulates synaptic vesicle (SV) trafficking. In Parkinson’s disease (PD) and dementia with Lewy bodies (DLB), α-synuclein aberrantly accumulates throughout neurons, including at synapses. During neuronal activity, α-synuclein is reversibly phosphorylated at serine 129 (pS129). While pS129 comprises ∼4% of total α-synuclein under physiological conditions, it dramatically increases in PD and DLB brains. The impacts of excess pS129 on synaptic function are currently unknown. We show here that compared with wild-type (WT) α-synuclein, pS129 exhibits increased binding and oligomerization on synaptic membranes and enhanced vesicle “microclustering” in vitro. Moreover, when acutely injected into lamprey reticulospinal axons, excess pS129 α-synuclein robustly localized to synapses and disrupted SV trafficking in an activity-dependent manner, as assessed by ultrastructural analysis. Specifically, pS129 caused a declustering and dispersion of SVs away from the synaptic vicinity, leading to a significant loss of total synaptic membrane. Live imaging further revealed altered SV cycling, as well as microclusters of recently endocytosed SVs moving away from synapses. Thus, excess pS129 caused an activity-dependent inhibition of SV trafficking via altered vesicle clustering/reclustering. This work suggests that accumulation of pS129 at synapses in diseases like PD and DLB could have profound effects on SV dynamics.
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ArticlePVC pellet leachates affect adult immune system and embryonic development but not reproductive capacity in the sea urchin Paracentrotus lividus(Elsevier, 2023-10-10)Microplastic pollution is a major concern of our age, eliciting a range of effects on organisms including during embryonic development. Plastic preproduction pellets stunt the development of sea urchins through the leaching of teratogenic compounds. However, the effect of these leachates on adult sea urchins and their fertility is unknown. Here we investigate the effect of PVC leachates on the capacity to produce normal embryos, and demonstrate that adults kept in contaminated water still produce viable offspring. However, we observe a cumulative negative effect by continued exposure to highly polluted water: adult animals had lower counts and disturbed morphological profiles of immune cells, were under increased oxidative stress, and produced embryos less tolerant of contaminated environments. Our findings suggest that even in highly polluted areas, sea urchins are fertile, but that sublethal effects seen in the adults may lead to transgenerational effects that reduce developmental robustness of the embryos.
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ArticleExploring the effect of age on the reproductive and stress physiology of octopus bimaculoides using dermal hormones(MDPI, 2023-10-06)Our goal was to validate the use of dermal swabs to evaluate both reproductive and stress physiology in the California two-spot octopus, Octopus bimaculoides. Our objectives were to (1) use dermal swabs to evaluate glucocorticoids and reproductive hormones of O. bimaculoides; (2) determine the influence of life stage on hormone production (glucocorticoids in all individuals; testosterone, estrogen, and progesterone in females; and testosterone in males) of reproductive (n = 4) and senescent (n = 8) individuals to determine the effect of age on hormonal patterns; and (3) determine whether these hormones change significantly in response to an acute stressor. For the stress test, individuals were first swabbed for a baseline and then chased around the aquarium with a net for 5 min. Afterward, individuals were swabbed for 2 h at 15 min intervals to compare to the pre-stress test swab. Reproductive individuals responded to the stressor with a 2-fold increase in dermal cortisol concentrations at 15 and 90 min. Six of the eight senescent individuals did not produce a 2-fold increase in dermal cortisol concentrations. Reproductive individuals had significantly higher sex hormone concentrations compared to senescent individuals (progesterone and estradiol measured in females, and testosterone for both sexes). After the stressor, only reproductive males produced a 2-fold increase in dermal testosterone concentrations, while sex hormones in females showed no change. The stress hormone cortisol was significantly higher in senescent than in reproductive individuals, independent of sex. Dermal corticosterone concentrations were highest in senescent females followed by senescent males, and lowest in reproductive individuals regardless of sex. Dermal swabs provide an effective and noninvasive means for evaluating octopus hormones. Application of these indicators may be imperative as cephalopods are more commonly cultured in captivity for experimentation, display, and consumption.
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ArticleFunctional dissection and assembly of a small, newly evolved, W chromosome-specific genomic region of the African clawed frog Xenopus laevis(Public Library of Science, 2023-10-08)Genetic triggers for sex determination are frequently co-inherited with other linked genes that may also influence one or more sex-specific phenotypes. To better understand how sex-limited regions evolve and function, we studied a small W chromosome-specific region of the frog Xenopus laevis that contains only three genes (dm-w, scan-w, ccdc69-w) and that drives female differentiation. Using gene editing, we found that the sex-determining function of this region requires dm-w but that scan-w and ccdc69-w are not essential for viability, female development, or fertility. Analysis of mesonephros+gonad transcriptomes during sexual differentiation illustrates masculinization of the dm-w knockout transcriptome, and identifies mostly non-overlapping sets of differentially expressed genes in separate knockout lines for each of these three W-specific gene compared to wildtype sisters. Capture sequencing of almost all Xenopus species and PCR surveys indicate that the female-determining function of dm-w is present in only a subset of species that carry this gene. These findings map out a dynamic evolutionary history of a newly evolved W chromosome-specific genomic region, whose components have distinctive functions that frequently degraded during Xenopus diversification, and evidence the evolutionary consequences of recombination suppression.
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ArticleThe FMRF-NH2 gated sodium channel of Biomphalaria glabrata: Localization and expression following infection by Schistosoma mansoni(Public Library of Science, 2023-06-23)The neglected tropical disease schistosomiasis impacts over 700 million people globally. Schistosoma mansoni, the trematode parasite that causes the most common type of schistosomiasis, requires planorbid pond snails of the genus Biomphalaria to support its larval development and transformation to the cercarial form that can infect humans. A greater understanding of neural signaling systems that are specific to the Biomphalaria intermediate host could lead to novel strategies for parasite or snail control. This study examined a Biomphalaria glabrata neural channel that is gated by the neuropeptide FMRF-NH2. The Biomphalaria glabrata FMRF-NH2 gated sodium channel (Bgl-FaNaC) amino acid sequence was highly conserved with FaNaCs found in related gastropods, especially the planorbid Planorbella trivolvis (91% sequence identity). In common with the P. trivolvis FaNaC, the B. glabrata channel exhibited a low affinity (EC50: 3 x 10−4 M) and high specificity for the FMRF-NH2 agonist. Its expression in the central nervous system, detected with immunohistochemistry and in situ hybridization, was widespread, with the protein localized mainly to neuronal fibers and the mRNA confined to cell bodies. Colocalization of the Bgl-FaNaC message with its FMRF-NH2 agonist precursor occurred in some neurons associated with male mating behavior. At the mRNA level, Bgl-FaNaC expression was decreased at 20 and 35 days post infection (dpi) by S. mansoni. Increased expression of the transcript encoding the FMRF-NH2 agonist at 35 dpi was proposed to reflect a compensatory response to decreased receptor levels. Altered FMRF-NH2 signaling could be vital for parasite proliferation in its intermediate host and may therefore present innovative opportunities for snail control.
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ArticleComparison of blastema formation after injury in two cephalopod species(Caltech Library, 2023-09-19)Regeneration is the ability to functionally replace significant amounts of lost tissue or whole appendages like arms, limbs or tentacles. The amount of tissue that can be regenerated varies among species, but regeneration is found in both invertebrate and vertebrate animals. Cephalopods have been broadly reported in the literature to regenerate their arms. There are over 800 species of Cephalopod; however, regeneration has only been documented in the literature in a few species (1). Here we compare arm regeneration in two species of cephalopod, the Octopus bimaculoides and the hummingbird bobtail squid Euprymna berryi.
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ArticleStructure and optical anisotropy of spider scales and silk: the use of chromaticity and azimuth colors to optically characterize complex biological structures(MDPI, 2023-06-20)Herein, we give an overview of several less explored structural and optical characterization techniques useful for biomaterials. New insights into the structure of natural fibers such as spider silk can be gained with minimal sample preparation. Electromagnetic radiation (EMR) over a broad range of wavelengths (from X-ray to THz) provides information of the structure of the material at correspondingly different length scales (nm-to-mm). When the sample features, such as the alignment of certain fibers, cannot be characterized optically, polarization analysis of the optical images can provide further information on feature alignment. The 3D complexity of biological samples necessitates that there be feature measurements and characterization over a large range of length scales. We discuss the issue of characterizing complex shapes by analysis of the link between the color and structure of spider scales and silk. For example, it is shown that the green-blue color of a spider scale is dominated by the chitin slab’s Fabry–Pérot-type reflectivity rather than the surface nanostructure. The use of a chromaticity plot simplifies complex spectra and enables quantification of the apparent colors. All the experimental data presented herein are used to support the discussion on the structure–color link in the characterization of materials.