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Euprymna scolopes produces one type of circulating macrophage‐like blood cell (hemocytes) that differentially bind bacteria. (a,d) Photographs of a juvenile and an adult E. scolopes respectively. (b,e) Cartoon depictions of the light organ in reference to the morphology of juvenile (b; hatchling) and adult E. scolopes (e). (c,f) Diagrams of the internal architecture of uncolonized hatchling and colonized adult light organs showing crypt spaces that house Vibrio fischeri. (g) Confocal micrographs of a hemocyte isolated from juvenile animals, adhered to a glass surface and fixed. A GFP expressing V. fischeri cell (arrows, green) was bound to the hemocyte cell membrane stained with Concanavalin A (Con A, red), and observed with differential interference contrast (DIC) microscopy, scale, 10 µm. n, nucleus; c, cytoplasm (h) Confocal micrographs of fixed hemocytes isolated from symbiotic wild‐caught adult animals bound to GFP‐expressing V. fischeri or V. harveyi. (i) The average number of V. fischeri or V. harveyi bound per hemocyte. Bars represent the average (±SE) of three biological replicates (10 hemocytes per replicate). †Levels of bacterial binding that are significantly different from each other (Students t test p < 0.001)
Source publication
The binary association between the squid, Euprymna scolopes, and its symbiont, Vibrio fischeri, serves as a model system to study interactions between beneficial bacteria and the innate immune system. Previous research demonstrated that binding of the squid's immune cells, hemocytes, to V. fischeri is altered if the symbiont is removed from the lig...
Citations
... Macrophage cells (hemocytes) can be easily obtained and observed for their interactions with symbiotic and non-symbiotic bacteria with microscopy (Nyholm et al. 2009;Rader, McAnulty and Nyholm 2019) and at the molecular level with proteomics and transcriptomics (Collins et al. 2012b;Schleicher et al. 2014). ...
Synopsis
Few animal groups can claim the level of wonder that cephalopods instill in the minds of researchers and the general public. Much of cephalopod biology, however, remains unexplored: the largest invertebrate brain, difficult husbandry conditions, and complex (meta-)genomes, among many other things, have hindered progress in addressing key questions. However, recent technological advancements in sequencing, imaging, and genetic manipulation have opened new avenues for exploring the biology of these extraordinary animals. The cephalopod molecular biology community is thus experiencing a large influx of researchers, emerging from different fields, accelerating the pace of research in this clade. In the first post-pandemic event at the Cephalopod International Advisory Council (CIAC) conference in April 2022, over 40 participants from all over the world met and discussed key challenges and perspectives for current cephalopod molecular biology and evolution. Our particular focus was on the fields of comparative and regulatory genomics, gene manipulation, single-cell transcriptomics, metagenomics, and microbial interactions. This article is a result of this joint effort, summarizing the latest insights from these emerging fields, their bottlenecks, and potential solutions. The article highlights the interdisciplinary nature of the cephalopod-omics community and provides an emphasis on continuous consolidation of efforts and collaboration in this rapidly evolving field.
... Essentially, the squid hemocytes "choose" to release Vibrio fischeri cells after the bacteria have been "captured" by the immune cells in preparation for phagocytic digestion. The Vibrio fischeri outer membrane protein OmpU may partially mediate this process [102]. ...
The Vibrionaceae encompasses a cosmopolitan group that is mostly aquatic and possesses tremendous metabolic and genetic diversity. Given the importance of this taxon, it deserves continued and deeper research in a multitude of areas. This review outlines emerging topics of interest within the Vibrionaceae. Moreover, previously understudied research areas are highlighted that merit further exploration, including affiliations with marine plants (seagrasses), microbial predators, intracellular niches, and resistance to heavy metal toxicity. Agarases, phototrophy, phage shock protein response, and microbial experimental evolution are also fields discussed. The squid–Vibrio symbiosis is a stellar model system, which can be a useful guiding light on deeper expeditions and voyages traversing these “seas of interest”. Where appropriate, the squid–Vibrio mutualism is mentioned in how it has or could facilitate the illumination of these various subjects. Additional research is warranted on the topics specified herein, since they have critical relevance for biomedical science, pharmaceuticals, and health care. There are also practical applications in agriculture, zymology, food science, and culinary use. The tractability of microbial experimental evolution is explained. Examples are given of how microbial selection studies can be used to examine the roles of chance, contingency, and determinism (natural selection) in shaping Earth’s natural history.
... The 1 H and 13 . The amino acid sequence could be determined by a thorough 2-D NMR analysis to be Trp 1 -Asn-Trp 2 -Thr-Lys-Arg-Phe. ...
... Even though the natural product was first identified from Photorhabdus strains, the corresponding BGC is more widespread among gammaproteobacteria. All of these (e.g., Pseudoalteromonas, Vibrio, and Yersinia) are reported to be associated with higher organisms (12)(13)(14). ...
Therapeutic options to combat Gram-negative bacterial pathogens are dwindling with increasing antibiotic resistance. This study presents a proof of concept for the heterologous-expression approach to expand on the novel antibiotic class of darobactins and to generate analogs with different activities and pharmacokinetic properties.
... The hemocytes of nonsymbiotic squid treat V. fischeri cells similarly to other bacteria; i.e., they bind and phagocytose numerous bacterial cells. However, after colonization of the light organ, the hemocytes lose their ability to recognize V. fischeri but retain the capacity to recognize other bacteria at the same rate as they do in the nonsymbiotic host (41). This bacterium-induced change in host hemocyte behavior is mediated, in part, by the symbiont membrane protein OmpU; it has not yet been determined how a mutation in the gene encoding OmpU results in a defect in the ability of V. fischeri cells to evade host hemocytes. ...
Symbiosis, by its basic nature, depends on partner interactions that are mediated by cues and signals. This kind of critical reciprocal communication shapes the trajectory of host-microbe associations from their onset through their maturation and is typically mediated by both biochemical and biomechanical influences. Symbiotic partnerships often involve communities composed of dozens to hundreds of microbial species, for which resolving the precise nature of these partner interactions is highly challenging. Naturally occurring binary associations, such as those between certain legumes, nematodes, fishes, and squids, and their specific bacterial partner species offer the opportunity to examine interactions with high resolution and at the scale at which the interactions occur. The goals of this review are to provide the conceptual framework for evolutionarily conserved drivers of host-symbiont communication in animal associations and to offer a window into some mechanisms of this phenomenon as discovered through the study of the squid-vibrio model. The discussion focuses upon the early events that lead to persistence of the symbiotic partnership. The biophysical and biochemical determinants of the initial hours of dialogue between partners and how the symbiosis is shaped by the environment that is created by their reciprocal interactions are key topics that have been difficult to approach in more complex systems. Through our research on the squid-vibrio system, we provide insight into the intricate temporal and spatial complexity that underlies the molecular and cellular events mediating successful microbial colonization of the host animal.
... Multifaceted links between immunity and symbiosis. Studies of symbiosis and immunity in cereal weevils [36][37][38][39], bees [40][41][42][43][44][45], bobtail squid [46][47][48][49][50] and zebrafish [51][52][53][54][55][56][57][58] have revealed many ways that immunity and symbiosis interact. Other systems central to the study of immunity and symbiosis include tsetse flies, aphids, hydra, mice and humans. ...
... Furthermore, females lacking Wigglesworthia produce larvae that have decreased expression of genes involved in haemocyte differentiation, suggesting that there are transgenerational effects of symbiont association [104]. These phenotypes have important fitness consequences: aposymbiotic flies infected with Escherichia coli, which is normally not pathogenic to flies, are overwhelmed by the bacterial infection [49]. Of applied importance, aposymbiotic flies are also less likely to clear trypanosome infections, which they vector to humans. ...
... These influences on immune system maturation might have evolved in part because they benefit the symbiont. In bobtail squid, for example, persistent association with their symbiont, V. fischeri, leads to reduced haemocyte responses in adults to their symbiont relative to non-symbiotic competitors [49]. ...
Immune system processes serve as the backbone of animal defences against pathogens and thus have evolved under strong selection and coevolutionary dynamics. Most microorganisms that animals encounter, however, are not harmful, and many are actually beneficial. Selection should act on hosts to maintain these associations while preventing exploitation of within-host resources. Here, we consider how several key aspects of beneficial symbiotic associations may shape host immune system evolution. When host immunity is used to regulate symbiont populations, there should be selection to evolve and maintain targeted immune responses that recognize symbionts and suppress but not eliminate symbiont populations. Associating with protective symbionts could relax selection on the maintenance of redundant host-derived immune responses. Alternatively, symbionts could facilitate the evolution of host immune responses if symbiont-conferred protection allows for persistence of host populations that can then adapt. The trajectory of immune system evolution will likely differ based on the type of immunity involved, the symbiont transmission mode and the costs and benefits of immune system function. Overall, the expected influence of beneficial symbiosis on immunity evolution depends on how the host immune system interacts with symbionts, with some interactions leading to constraints while others possibly relax selection on immune system maintenance.
This article is part of the theme issue ‘The role of the microbiome in host evolution’.
The Pacific oyster Crassostrea gigas lives in microbe-rich marine coastal systems subjected to rapid environmental changes. It harbours a diversified and fluctuating microbiota that cohabits with immune cells expressing a diversified immune gene repertoire. In the early stages of oyster development, just after fertilization, the microbiota plays a key role in educating the immune system. Exposure to a rich microbial environment at the larval stage leads to an increase in immune competence throughout the life of the oyster, conferring a better protection against pathogenic infections at later juvenile/adult stages. This beneficial effect, which is intergenerational, is associated with epigenetic remodelling. At juvenile stages, the educated immune system participates in the control of the homeostasis. In particular, the microbiota is fine-tuned by oyster antimicrobial peptides acting through specific and synergistic effects. However, this balance is fragile, as illustrated by the Pacific Oyster Mortality Syndrome, a disease causing mass mortalities in oysters worldwide. In this disease, the weakening of oyster immune defences by OsHV-1 µVar virus induces a dysbiosis leading to fatal sepsis. This review illustrates the continuous interaction between the highly diversified oyster immune system and its dynamic microbiota throughout its life, and the importance of this cross-talk for oyster health.
This article is part of the theme issue ‘Sculpting the microbiome: how host factors determine and respond to microbial colonization’.
Cephalopods are an interesting and diverse group of animals in nature, and their dexterity, speed, unique anatomical features, colorful beauty, visual acuity, and ability to learn various tasks make them popular with the communication media and public in general. Cephalopods are members of the phylum Mollusca and share basic body organizational features with the gastropods, bivalves, and other mollusks. The octopuses are represented by several families and have a worldwide distribution. The cephalopod immune system can be compromised easily with poor water quality, overcrowding, and/or increased bacterial load on the aquatic system. Disease management of captive cephalopods depends on careful and attentive husbandry with high-quality nutrition, frequent clinical assessment and observation of animals, and appropriate use of antibiotics. The best approach in the treatment of cephalopods is the careful monitoring and control of water quality. Since the high surface area skin has a microvillus border, drugs may be readily absorbed, and possibly at toxic levels.
Evolution is the single unifying principle of biology and core to everything in the life sciences. More than a century of work by scientists from across the biological spectrum has produced a detailed history of life across the phyla and explained the mechanisms by which new species form. This textbook covers both this history and the mechanisms of speciation; it also aims to provide students with the background needed to read the research literature on evolution. Students will therefore learn about cladistics, molecular phylogenies, the molecular-genetical basis of evolutionary change including the important role of protein networks, symbionts and holobionts, together with the core principles of developmental biology. The book also includes introductory appendices that provide background knowledge on, for example, the diversity of life today, fossils, the geology of Earth and the history of evolutionary thought. Key Features: Summarizes the origins of life and the evolution of the eukaryotic cell and of Urbilateria, the last common ancestor of invertebrates and vertebrates. Reviews the history of life across the phyla based on the fossil record and computational phylogenetics. Explains evo-devo and the generation of anatomical novelties. Illustrates the roles of small populations, genetic drift, mutation and selection in speciation. Documents human evolution using the fossil record and evidence of dispersal across the world leading to the emergence of modern humans.
For more than 30 years, the association between the Hawaiian bobtail squid, Euprymna scolopes, and the bioluminescent bacterium Vibrio fischeri has been studied as a model system for understanding the colonization of animal epithelia by symbiotic bacteria. The squid–vibrio light-organ system provides the exquisite resolution only possible with the study of a binary partnership. The impact of this relationship on the partners’ biology has been broadly characterized, including their ecology and evolutionary biology as well as the underlying molecular mechanisms of symbiotic dynamics. Much has been learned about the factors that foster initial light-organ colonization, and more recently about the maturation and long-term maintenance of the association. This Review synthesizes the results of recent research on the light-organ association and also describes the development of new horizons for E. scolopes as a model organism that promises to inform biology and biomedicine about the basic nature of host–microorganism interactions. In this Review Nyholm and McFall-Ngai describe recent advances in understanding the squid–vibrio symbiosis, specifically the strides that have been made in recent years in the study of bobtail squid symbiosis from the host viewpoint.
