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Showing papers in "The Biological Bulletin in 2012"


Journal ArticleDOI
TL;DR: The history of “omics” studies of cnidarian-algal symbiosis and the current availability of sequence resources for corals and anemones are reviewed, identifying genes putatively involved in symbiosis across 10 anthozoan species.
Abstract: The symbiotic associations between cnidarians and dinoflagellate algae (Symbiodinium) support productive and diverse ecosystems in coral reefs. Many aspects of this association, including the mechanistic basis of host-symbiont recognition and metabolic interaction, remain poorly understood. The first completed genome sequence for a symbiotic anthozoan is now available (the coral Acropora digitifera), and extensive expressed sequence tag resources are available for a variety of other symbiotic corals and anemones. These resources make it possible to profile gene expression, protein abundance, and protein localization associated with the symbiotic state. Here we review the history of "omics" studies of cnidarian-algal symbiosis and the current availability of sequence resources for corals and anemones, identifying genes putatively involved in symbiosis across 10 anthozoan species. The public availability of candidate symbiosis-associated genes leaves the field of cnidarian-algal symbiosis poised for in-depth comparative studies of sequence diversity and gene expression and for targeted functional studies of genes associated with symbiosis. Reviewing the progress to date suggests directions for future investigations of cnidarian-algal symbiosis that include (i) sequencing of Symbiodinium, (ii) proteomic analysis of the symbiosome membrane complex, (iii) glycomic analysis of Symbiodinium cell surfaces, and (iv) expression profiling of the gastrodermal cells hosting Symbiodinium.

88 citations


Journal ArticleDOI
TL;DR: Nematodes are ubiquitous organisms that have a significant global impact on ecosystems, economies, ag-riculture, and human health as mentioned in this paper and are particularly well suited for the investigation of host associ- ations with bacteria because all organisms have interacted with bacteria during their evolutionary history and engage in a variety of association types.
Abstract: Nematodes are ubiquitous organisms that have a significant global impact on ecosystems, economies, ag- riculture, and human health. The applied importance of nematodes and the experimental tractability of many species have promoted their use as models in various research areas, including developmental biology, evolutionary biology, ecology, and animal-bacterium interactions. Nematodes are particularly well suited for the investigation of host associ- ations with bacteria because all nematodes have interacted with bacteria during their evolutionary history and engage in a variety of association types. Interactions between nem- atodes and bacteria can be positive (mutualistic) or negative (pathogenic/parasitic) and may be transient or stably main- tained (symbiotic). Furthermore, since many mechanistic aspects of nematode-bacterium interactions are conserved, their study can provide broader insights into other types of associations, including those relevant to human diseases. Recently, genome-scale studies have been applied to di- verse nematode-bacterial interactions and have helped re- veal mechanisms of communication and exchange between the associated partners. In addition to providing specific information about the system under investigation, these studies also have helped inform our understanding of ge- nome evolution, mutualism, and innate immunity. In this review we discuss the importance and diversity of nema- todes, "omics"' studies in nematode-bacterial systems, and the wider implications of the findings.

62 citations


Journal ArticleDOI
TL;DR: The use of light sheet microscopy is reported to provide high-resolution imaging of bacterial colonization of the intestine of Danio rerio, the zebrafish and allows us to characterize bacterial population dynamics across the entire organ and the behaviors of individual bacterial and host cells throughout the colonization process.
Abstract: Microbial colonization of the digestive tract is a crucial event in vertebrate development, required for mat- uration of host immunity and establishment of normal di- gestive physiology. Advances in genomic, proteomic, and metabolomic technologies are providing a more detailed picture of the constituents of the intestinal habitat, but these approaches lack the spatial and temporal resolution needed to characterize the assembly and dynamics of microbial communities in this complex environment. We report the use of light sheet microscopy to provide high-resolution imaging of bacterial colonization of the intestine of Danio rerio, the zebrafish. The method allows us to characterize bacterial population dynamics across the entire organ and the behaviors of individual bacterial and host cells through- out the colonization process. The large four-dimensional data sets generated by these imaging approaches require new strategies for image analysis. When integrated with other "omics" data sets, information about the spatial and temporal dynamics of microbial cells within the vertebrate intestine will provide new mechanistic insights into how microbial communities assemble and function within hosts.

54 citations


Journal ArticleDOI
TL;DR: New discoveries regarding the onset of coral-bacterial associations; the functional roles that bacteria play in healthy corals; and how bacteria influence coral reef response to environmental change are reviewed, leading to a model describing how reef microbiota direct ecosystem-level response to a changing global climate are reviewed.
Abstract: Recent research has explored the possibility that increased sea-surface temperatures and decreasing pH (ocean acidification) contribute to the ongoing decline of coral reef ecosystems. Within corals, a diverse microbiome exerts significant influence on biogeochemical and ecolog- ical processes, including food webs, organismal life cycles, and chemical and nutrient cycling. Microbes on coral reefs play a critical role in regulating larval recruitment, bacterial colonization, and pathogen abundance under ambient con- ditions, ultimately governing the overall resilience of coral reef systems. As a result, microbial processes may be in- volved in reef ecosystem-level responses to climate change. Developments of new molecular technologies, in addition to multidisciplinary collaborative research on coral reefs, have led to the rapid advancement in our understanding of bac- terially mediated reef responses to environmental change. Here we review new discoveries regarding (1) the onset of coral-bacterial associations; (2) the functional roles that bacteria play in healthy corals; and (3) how bacteria influ- ence coral reef response to environmental change, leading to a model describing how reef microbiota direct ecosystem- level response to a changing global climate.

53 citations


Journal ArticleDOI
TL;DR: The phylogenetic analyses of the bathymodiolin symbionts show that both the sulfur and the methane oxidizers fall into multiple clades interspersed with free-living bacteria, many of which were discovered recently in metagenomes from marine oxygen minimum zones.
Abstract: Bathymodiolin mussels dominate hydrothermal vent and cold seep communities worldwide. Symbiotic associations with chemosynthetic sulfur- and methane-oxidizing bacteria that provide for their nutrition are the key to their ecological and evolutionary success. The current paradigm is that these symbioses evolved from two free-living ancestors, one methane-oxidizing and one sulfur-oxidizing bacterium. In contrast to previous studies, our phylogenetic analyses of the bathymodiolin symbionts show that both the sulfur and the methane oxidizers fall into multiple clades interspersed with free-living bacteria, many of which were discovered recently in metagenomes from marine oxygen minimum zones. We therefore hypothesize that symbioses between bathymodiolin mussels and free-living sulfur- and methane-oxidizing bacteria evolved multiple times in convergent evolution. Furthermore, by 16S rRNA sequencing and fluorescence in situ hybridization, we show that close relatives of the bathymodiolin symbionts occur on host...

51 citations


Journal ArticleDOI
TL;DR: The data support the idea that acclimatory responses to temperature stress can drive trade-offs among traits, as predicted by theory, and suggest individuals with limited access to resources are at greater risk because they are less able to mitigate potential costs of thermal stress through physiological mechanisms.
Abstract: In response to thermal stress, many rocky shore organisms exhibit characteristic physiological changes associated with increased tolerance to subsequent high temperatures. Although presumably adaptive, activation of the heat-shock response requires a significant energetic investment and therefore may impose a trade-off between survival and other life-history traits. We investigated the effects of chronic heat stress and variation in food availability on the relative allocation of resources to competing demographic parameters in the California mussel, Mytilus californianus. Our data support the idea that acclimatory responses to temperature stress can drive trade-offs among traits, as predicted by theory. Chronic heat stress invoked a cost to individuals, expressed as a reduction in shell growth or size-specific tissue mass in the field and laboratory, respectively. At the same time, prior thermal conditioning resulted in higher proportional survival after acute exposure to more extreme temperatures. Overa...

49 citations


Journal ArticleDOI
TL;DR: While blaming the reporter is easy, it is first and foremost the scientist’s job to share his or her research with the broader community, and it is the scientists who are ultimately to blame when their research isn’t communicated well.
Abstract: Now, more than ever, science is fundamentally intertwined with national and international political issues, yet less than one-third of Americans can pass a science literacy test with questions like “Does the Earth revolve around the sun?” and “Did human beings live alongside dinosaurs?” When only a small percentage of our populace—including our policy-makers—has a firm grasp on the science behind the debates, we are doomed to make grievous errors in our decisions on a wide variety of issues, from climate change and genetically modified foods to stem cell research and public health and vaccinations. The question isn’t whether America has a problem—it’s how to solve it. It’s easy to place blame. More than half of scientists will say the main problem is with the education system. More than a third will point a finger at the media. Very few will look critically at their own actions and instead suggest that it is our fault—that we, as scientists, are failing at communicating science to the public (The Wellcome Trust. 2001. “The Role of Scientists in Public Debate”). The fact of the matter is, we are. Science communication has become a public relations nightmare. Scientists and science are under constant attack from political and religious interests. It is a culture where former U.S. Senate majority leader Trent Lott can call his four years of science and math in high school “a waste of my time and a waste of my teacher’s time” and receive roaring applause. We aren’t powerless against this bad public image. The onus is on us, though, to be more engaged. Right now, we fade into the background. In 2009, Research!America polled the average American and asked them a very simple question: name a living scientist (ResearchAmerica. 2009. “Your Congress—Your Health”: Poll). About 18% got it wrong, but what is more sobering is that 65% of people didn’t even try to name anyone. The average American doesn’t know who we are. If we view science communication through the lens of public relations, the advice given by Rick Borchelt and his colleagues in an essay for the American Association for the Advancement of Science becomes even more poignant: “The scientific community needs to understand what ethical practitioners of public relations have long known: trust is not about information; it’s about dialogue and transparency” (Borchelt et al. 2010. Science and The Media, D. Kennedy and G. Overholser, eds. AAAS). Right now, science is almost entirely a monologue given to a very specific audience. As scientists, we pride ourselves on doing meaningful, cutting-edge research and publishing it in the top-tier journals of our field. The problem is, these publications only communicate science to other scientists. Articles are locked behind paywalls, and even those that are published in open access journals still lie behind jargon walls—the barriers that keep the people we want to become more scientifically literate from understanding what we do because they do not know the terminology. Putting out a press release isn’t a conversation either. Sure, major media outlets have a much broader audience than scientific journals, and thus handing our research over to a journalist to translate and publicize will ensure that more people learn about it. But this kind of passing the buck is fraught with its own difficulties. Most science journalists have never set foot in a lab or taken a college level course in science. We complain about sensationalist or poor reporting, but the fact of the matter is that journalists often haven’t had the training to understand the science they are assigned to explain. While blaming the reporter is easy, it is first and foremost the scientist’s job to share his or her research with the broader community. That means it is the scientists who are ultimately to blame when their research isn’t communicated well. Perhaps even more importantly, journalists engage in one-way communication, too, rarely taking feedback from or engaging in a conversation with their audience. Although their reach may be broader, the message is the same: here is the information; end of story. This single-sided approach is struggling to keep up with a fast-paced younger generation that holds the attitude that if something is important enough, it will find them. As Gaston Small said in a column for Nature, “The days of scientists communicating only with each other, in the languages of our individual disciplines, and relying on science journalists to translate for the public, are rapidly coming to an end” (Nature 2011. 479: 141). How do we achieve dialogue instead? First and foremost, we have to make a concentrated effort to get involved in the public discussion about science. We have to be approachable and available to talk about our research. More than Reference: Biol. Bull. 222: 85–87. (April 2012) © 2012 Marine Biological Laboratory

44 citations


Journal ArticleDOI
TL;DR: The results of this study suggest that this species may either prioritize endogenous energy toward development and physiological function at the expense of growth, or that reduced larval length may be strictly due to higher costs of growth under OA conditions.
Abstract: Ocean acidification (OA) is expected to have a major impact on marine species, particularly during early life-history stages. These effects appear to be species-specific and may include reduced survival, altered morphology, and depressed metabolism. However, less information is available regarding the bioenergetics of development under elevated CO(2) conditions. We examined the biochemical and morphological responses of Strongylocentrotus purpuratus during early development under ecologically relevant levels of pCO(2) (365, 1030, and 1450 μatm) that may occur during intense upwelling events. The principal findings of this study were (1) lipid utilization rates and protein content in S. purpuratus did not vary with pCO(2); (2) larval growth was reduced at elevated pCO(2) despite similar rates of energy utilization; and (3) relationships between egg phospholipid content and larval length were found under control but not high pCO(2) conditions. These results suggest that this species may either prioritize endogenous energy toward development and physiological function at the expense of growth, or that reduced larval length may be strictly due to higher costs of growth under OA conditions. This study highlights the need to further expand our knowledge of the physiological mechanisms involved in OA response in order to better understand how present populations may respond to global environmental change.

42 citations


Journal ArticleDOI
Yoko Nozawa1
TL;DR: This study was conducted at a high-latitude location, where annual seawater temperatures show large fluctuations due to the meandering of the Kuroshio Current, providing a unique opportunity to examine the influence of temperature on coral reproduction.
Abstract: This study was conducted at a high-latitude location (32°N; Kochi, Japan), where annual seawater temperatures show large fluctuations due to the meandering of the Kuroshio Current, providing a unique opportunity to examine the influence of temperature on coral reproduction. Annual spawning of individual colonies of four reef coral species—two Acropora species (Acropora hyacinthus and A. japonica) and two faviid species (Favites pentagona and Platygyra contorta)—was monitored in situ for 4 years in 2006–2009. The spawning of the four species always occurred around the last quarter moon in the local summer, July or August, irrespective of high annual variations in seawater temperatures (from 23.7 to 29.5 °C) and weather during the spawning period. However, the exact timing of spawning during the spawning period varied among the years and was correlated with the cumulative seawater temperature during the late period of gametogenesis (0–3 months before spawning). When seawater temperatures were higher, spawni...

42 citations


Journal ArticleDOI
TL;DR: Despite the very similar visual systems, it is found that T. cystophora is active exclusively during the day, whereas C. sivickisi is actively swimming at night, when it forages and mates.
Abstract: Cubozoan medusae have a stereotypic set of 24 eyes, some of which are structurally similar to vertebrate and cephalopod eyes. Across the approximately 25 described species, this set of eyes varies surprisingly little, suggesting that they are involved in an equally stereotypic set of visual tasks. During the day Tripedalia cystophora is found at the edge of mangrove lagoons where it accumulates close to the surface in sun-lit patches between the prop roots. Copula sivickisi (formerly named Carybdea sivickisi) is associated with coral reefs and has been observed to be active at night. At least superficially, the eyes of the two species are close to identical. We studied the diurnal activity pattern of these two species both in the wild and under controlled conditions in laboratory experiments. Despite the very similar visual systems, we found that they display opposite patterns of diurnal activity. T. cystophora is active exclusively during the day, whereas C. sivickisi is actively swimming at night, when it forages and mates. At night T. cystophora is found on the muddy bottom of the mangrove lagoon. C. sivickisi spends the day attached to structures such as the underside of stones and coral skeletons. This species difference seems to have evolved to optimize foraging, since the patterns of activity follow those of the available prey items in their respective habitats.

41 citations


Journal ArticleDOI
TL;DR: How symbiotic algae and stably associated bacteria interact with the Hydra host and where in the tissue they are located is reviewed and the role of Toll-like receptor (TLR) signaling in maintaining Hydra’s species-specific microbiota is discussed.
Abstract: The Hydra holobiont involves at least three types of organisms that all share a long coevolutionary history and appear to depend on each other. Here I review how symbiotic algae and stably associated bacteria interact with the Hydra host and where in the tissue they are located. In particular I discuss the role of Toll-like receptor (TLR) signaling in maintaining Hydra's species-specific microbiota. I also discuss studies in Hydra viridis and its symbiotic Chlorella algae which indicate that the symbiotic algae are critically involved in the control of sexual differentiation in green Hydra. Finally, I review the state of "omics" in this tripartite association and the fact that the functioning of this holobiont is also a tale of several genomes.

Journal ArticleDOI
TL;DR: The shelter of the tube-dwelling polychaete Sabellaria alveolata is composed of mineral particles assembled with spots of a proteinaceous cement, which contains two positively charged proteins and two variants of a serine-rich protein, which suggests that Sa-3 is very acidic and negatively charged.
Abstract: The shelter of the tube-dwelling polychaete Sabellaria alveolata is composed of mineral particles assembled with spots of a proteinaceous cement. The adhesive proteins constituting the cement were identified on the basis of their sequence similarity with proteins of a phylogenetically related species, Phragmatopoma californica. Two positively charged proteins, Sa-1 and Sa-2, share common features: they both have a mass of 22 kDa; are rich in glycine, tyrosine and basic residues; and show repeated peptide motifs. The consensus repeat of Sa-1 is KGAYGAKGLGYGNKAGYGAYG (occurring 6–8 times), while Sa-2 displays the consensus heptapeptide VHKAAWG (5 times) and undecapeptide VHKAAGYGGYG (8 times). Two variants of a serine-rich protein, Sa-3A (22 kDa) and Sa-3B (21 kDa), were also identified. Their serine residues account for 75 mol% and are probably phosphorylated, meaning that Sa-3 is very acidic and negatively charged. Moreover, tyrosine residues of all adhesive proteins are presumably modified into DOPA. Alt...

Journal ArticleDOI
TL;DR: Examination of temperature-mediated plasticity in offspring size, brooding duration, and fecundity in the adelphophagic marine gastropod Crepidula cf.
Abstract: Adelphophagic development, where embryos consume sibling embryos or nurse eggs, is particularly common in marine caenogastropods and some families of polychaetes. When exogenous nutrition is provided before hatching, egg size and hatching size can be uncoupled, but advantages and constraints of adelphophagic development compared to development from large eggs are unknown. Here we examine temperature-mediated plasticity in off- spring size, brooding duration, and fecundity in the adel- phophagic marine gastropod Crepidula cf. onyx .W e use these data combined with previously published data on two planktotrophic Crepidula and two Crepidula species that develop from large eggs to test hypotheses about the con- sequences of adelphophagic development and patterns of variation in offspring size. In Crepidula cf. onyx, egg size shows no significant effect of temperature. Hatching size is significantly larger at 28 °C than at 23 °C but proceeds from fewer eggs per capsule at 28 °C. Hatching size is therefore decoupled from both egg size and the number of eggs per capsule. Although development is faster at the higher tem- perature, broods are produced roughly every 26-27 days at both temperatures. Increased rate of development has been cited as a potential advantage of adelphophagic develop- ment in muricids, but the adelphophagic C. cf. onyx did not develop more quickly than C. atrasolea or C. ustulatulina, species that produce similarly sized hatchlings from large eggs. Comparisons across calyptraeid species support the role of adelphophagy in increasing variance in offspring size. This increased variability is primarily expressed within broods or among broods from the same female, not among females.

Journal ArticleDOI
TL;DR: Findings pertaining to quorum sensing, luminescence, responses to reactive oxygen and nitrogen species, recognition of microbe-associated molecular patterns by the innate immune system of the host, and a diel rhythm that helps regulate the symbiont population are highlighted.
Abstract: The association between Euprymna scolopes, the Hawaiian bobtail squid, and Vibrio fischeri, a bioluminescent bacterium, has served as a model for beneficial symbioses for over 25 years. The experimental tractability of this association has helped researchers characterize many of the colonization events necessary for symbiosis. Recent technological advances, such as the sequenced genome of V. fischeri, DNA microarrays, and high-throughput transcriptomics and proteomics, have allowed for the identification of host and symbiont factors that are important in establishing and maintaining specificity in the association. We highlight some of these findings pertaining to quorum sensing, luminescence, responses to reactive oxygen and nitrogen species, recognition of microbe-associated molecular patterns by the innate immune system of the host, and a diel rhythm that helps regulate the symbiont population. We also discuss how comparative genomics has allowed the identification of symbiont factors important for specificity and why sequencing the host's genome should be a priority for the research community.

Journal ArticleDOI
TL;DR: These findings provide a launching point for a new era of genomic explorations of bacterial-animal symbioses, to reveal symbiotic strategies across a broad ecological and phylogenetic range, to clarify key transitions along a spectrum of interaction types, and to fuel the mechanistic basis of intimate host-symbiont associations.
Abstract: Insects, the most diverse group of macroorganisms with 900,000 known species, have been a rich playground for the evolution of symbiotic associations. Symbionts of this enormous animal group include a range of microbial partners. Insects are prone to establishing relationships with intracellular bacteria, which include the most intimate, highly integrated mutualisms known in the biological world. In recent years, an explosion of genomic studies has offered new insights into the molecular, functional, and evolutionary consequences of these insect-bacterial partnerships. In this review, I highlight some insights from genome sequences of bacterial endosymbionts and select insect hosts. Notably, comparisons between facultative and obligate bacterial mutualists have revealed distinct genome features representing different stages along a shared trajectory of genome reduction. Bacteria associated with the cedar aphid offer a snapshot of a transition from facultative to obligate mutualism, illustrating the genomi...

Journal ArticleDOI
TL;DR: Two approaches, phylogenomics and transcriptional clustering, are discussed that can divide the primary output of omics studies—long lists of factors—into manageable subsets, and how they have been applied to analyze large datasets and generate testable hypotheses are described.
Abstract: Omics, including genomics, proteomics, and metabolomics, enable us to explain symbioses in terms of the underlying molecules and their interactions. The central task is to transform molecular catalogs of genes, metabolites, etc., into a dynamic understanding of symbiosis function. We review four exemplars of omics studies that achieve this goal, through defined biological questions relating to metabolic integration and regulation of animal-microbial symbioses, the genetic autonomy of bacterial symbionts, and symbiotic protection of animal hosts from pathogens. As omic datasets become increasingly complex, computationally sophisticated downstream analyses are essential to reveal interactions not evident from visual inspection of the data. We discuss two approaches, phylogenomics and transcriptional clustering, that can divide the primary output of omics studies—long lists of factors—into manageable subsets, and we describe how they have been applied to analyze large datasets and generate testable hypotheses.

Journal ArticleDOI
TL;DR: This study attempts to dispel the story of the flatfish by exploring more recent developments in deep-sea exploration and biological research, including the mismatch of depths compared with fish of similar body form, an improbable window of opportunity to have made observations, and the absence of fish from other cameras deployed in the trenches.
Abstract: In 1960, the first-ever manned dive to the deepest place on earth (11,000 m) took place. The pilots reported that on contact with the seafloor they observed a ”flatfish.” This story captured the public imagination yet bears no scientific credibility. In the myriad of publicity surrounding James Cameron’s latest dive, some 52 years later, the story of the flatfish is once again being perpetuated in the popular media, misinforming the public about deep-sea biology. This study attempts to dispel the story of the flatfish by exploring more recent developments in deep-sea exploration and biological research: (1) the mismatch of depths compared with fish of similar body form, (2) an improbable window of opportunity to have made the observations, (3) the absence of fish from other cameras deployed in the trenches, (4) the absence of fish from subsequent exploration of the area, and (5) new hypotheses that predict that fish are, at a cellular level, physiologically incapable of surviving at depths greater than 8500 m. On the basis of all these aspects, it is clear that the Trieste flatfish story is either a misidentification or entirely erroneous. On the 23rd of January 1960, the Bathyscaphe Trieste descended to the deepest place on Earth—Challenger Deep (10,916 m) in the Mariana Trench, Central Pacific Ocean. This exercise represented the first human presence in the deepest part of the oceans. Such an achievement was understandably embroiled in a myriad of publicity at the time, and the story of Jacques Piccard and Don Walsh’s exploit has been told in the contexts of ocean exploration and human endeavor ever since. The legendary status of the Trieste dive is founded not only upon being the first to achieve such feats but also to have remained the only humans to have done so for more than 50 years. The story of the Trieste is once again at the forefront of popular science news and media, partly due to the 50th anniversary of the dive in 2010 and more recently as a result of the X Prize Foundation competition to construct a manned submersible capable of transporting humans to and from the deepest place on Earth. This “race” to Challenger Deep involved several competitors including high-profile personalities such as Virgin Group Chairman Sir Richard Branson, Google founder Eric Schmidt, and the Hollywood film producer James Cameron, who recently won the race. While this renewed and high-profile interest in sending humans to Challenger Deep represents a ground-breaking endeavor in terms of new deep-submergence technology, promotion of the deep-sea environment, and inspiration for future generations of scientists and technologists, it has also resurrected details from the Trieste story that are misleading and most likely erroneous. Recent media coverage has brought the story of the “Trieste flatfish” back into the public arena. The story relates to a flatfish observed through the viewport of the Trieste by Jacques Piccard at nearly 11,000 m deep. Very little was known about the geographic and bathymetric distribution of deep-sea fauna at the time of the dive, and the story of the flatfish sighting was heralded as proof that life exists at full ocean depth and provided the kind of detail that made the dive such a success and so popular. However, 50 years on from the Trieste dive, considerable progress has been made in understanding the bathymetric distribution of fish and exploring the trenches, and despite the ever-increasing wealth of information to suggest that the flatfish sighting is dubious, the story still persists. For example, Philippe Cousteau Jr., an environmental advocate, even related this story live on CNN to an Received 12 April 2012; accepted 6 May 2012. * To whom correspondence should be addressed. E-mail: a.jamieson@ abdn.ac.uk Reference: Biol. Bull. 222: 171–175. (June 2012) © 2012 Marine Biological Laboratory

Journal ArticleDOI
TL;DR: The phyllosoma, a larva of spiny and slipper lobsters, has an exceptionally flat body and long appendages and is likely that they have evolved to utilize venomous jellyfish as a food in the open sea, where food may be scarce.
Abstract: The phyllosoma, a larva of spiny and slipper lobsters, has an exceptionally flat body and long appendages. It is known to associate with several species of cnidarian jellyfish, a behavior that is n...

Journal ArticleDOI
TL;DR: Bacteria capable of polysaccharide digestion and photosynthesis, as well as putative nitrogen fixation, vitamin B12 production, and natural product biosynthesis were associated with the sea slug and algal samples.
Abstract: The molluscan sea slug Elysia chlorotica is best known for its obligate endosymbiosis with chloroplasts (= kleptoplasty) from its algal prey Vaucheria litorea and its ability to sustain itself photoautotrophically for several months. This unusual photosynthetic sea slug also harbors an array of undescribed bacteria, which may contribute to the long-term success of the symbiosis. Here, we utilized 16S rDNA-based metagenomic analyses to characterize the microbial diversity associated with two populations of E. chlorotica from Halifax, Nova Scotia, Canada, and from Martha’s Vineyard, Massachusetts, USA. Animals were examined immediately after collection from their native environments, after being starved of their algal prey for several months, and after being bred in the laboratory (second-generation sea slugs) to characterize the effect of varying environmental and culturing conditions on the associated bacteria. Additionally, the microbiome of the algal prey, laboratory-cultured V. litorea, was analyzed to...

Journal ArticleDOI
TL;DR: The power of single-cell genomics for symbiosis research is explored and recent insights into the symbiotic systems that were obtained by this approach are highlighted.
Abstract: Single-cell genomics has advanced the field of microbiology from the analysis of microbial metagenomes where information is "drowning in a sea of sequences," to recognizing each microbial cell as a separate and unique entity. Single-cell genomics employs Phi29 polymerase- mediated whole-genome amplification to yield microgram- range genomic DNA from single microbial cells. This method has now been applied to a handful of symbiotic systems, including bacterial symbionts of marine sponges, insects (grasshoppers, termites), and vertebrates (mouse, human). In each case, novel insights were obtained into the functional genomic repertoire of the bacterial partner, which, in turn, led to an improved understanding of the corresponding host. Single-cell genomics is particularly valuable when dealing with uncultivated microorganisms, as is still the case for many bacterial symbionts. In this review, we explore the power of single-cell genomics for symbiosis research and highlight recent insights into the symbiotic systems that were obtained by this approach. Background The fields of metagenomics, metatranscriptomics, and metaproteomics, among others collectively referred to as "omics," have made a tremendous impact on symbiosis research (see other articles in this special issue). For many decades, symbiosis research was possible solely by descrip- tive approaches because neither could the symbionts be cultured (largely unchanged to this day) nor was there experimental access to many symbiotic systems (also largely unchanged). The implementation of cultivation- independent approaches based on 16S rRNA gene se- quences thus initiated a major revolution by making it possible to place organisms that were frequently known only by electron microscopy into a phylogenetic context. 16S rRNA gene phylogenies further helped to delineate co-evolution and co-speciation events by comparing host and symbiont phylogenies. The implementation of omics methods spurred a second wave of information in symbiosis research as it became possible to predict the genomic underpinnings of symbio- ses. For example, the discovery that many insects had

Journal ArticleDOI
TL;DR: The distribution and high number of oral denticles appears to spatially compromise the capacity for oral (taste) papillae to populate the oropharyngeal cavity but provides increased friction and grip on prey items as they are manipulated within the mouth.
Abstract: The placoid scales, or denticles, of the external epidermis of elasmobranchs are well known as a hard protective coat over the skin to reduce abrasion or as elements to reduce hydrodynamic drag. However, the structure and function of denticles within the oral cavity is uncertain. Using stereological and scanning electron microscopy, this study examines the structure and distribution of oral denticles in a range of elasmobranchs. Of the batoids analyzed, only members of the Rhinobatidae possessed oral denticles, with no denticles found in the members sampled in the Gymnuridae or Dasyatidae. In contrast, oral denticles were located in all the selachians examined, except for members of the Orectolobidae. Within the selachians, the denticles of the Carcharhinidae have a grooved surface and a central spine, which is angled toward the posterior of the mouth. These denticular adaptations are beneficial to reduce hydrodynamic drag, an advantage for these free-swimming species with ram ventilation. Alternatively, members of the Hemiscyllidae have broad bulbous denticles that often overlap, providing a hard surface to protect the epithelium from abrasion during the consumption of hard-bodied prey. The distribution and high number of oral denticles appears to spatially compromise the capacity for oral (taste) papillae to populate the oropharyngeal cavity but provides increased friction and grip on prey items as they are manipulated within the mouth.

Journal ArticleDOI
TL;DR: This study of Cidaris blakei, aDeep-sea cidaroid urchin with planktotrophic larvae, provides a description of development from fertilization through early juvenile stages and is the first report of a deep-sea urchi reared through metamorphosis.
Abstract: Cidaroids, one of the two major sister clades of sea urchins, first appeared during the lower Permian (ca. 270 mya) and are considered to represent the primitive form of all living echinoids. This study of Cidaris blakei ,a deep-sea cidaroid urchin with planktotrophic larvae, pro- vides a description of development from fertilization through early juvenile stages and is the first report of a deep-sea urchin reared through metamorphosis. C. blakei resembles other cidaroids in its lack of a cohesive hyaline layer, the absence of an amniotic invagination for juvenile rudiment formation, and the presence of spines with a single morphotype at metamorphosis. C. blakei differed from other cidaroids in the presence of an apical tuft, the extent of fenestration of postoral skeletal rods, the shape of juvenile spines, and an extended (14-day) lecithotrophic stage prior to development of a complete gut. The development of C. blakei, 120 days from fertilization to metamorphosis, was protracted relative to that of shallow-water cidaroids. Pre- liminary work on temperature tolerances suggests that C. blakei larvae would be unable to survive the warmer tem- peratures higher in the water column and are therefore unable to vertically migrate.

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TL;DR: Using fluorescent in situ hybridization, it is demonstrated that bacterial symbionts, while present within the gills, are absent within acini that enclose female gametes and male gamets, which supports the hypothesis of environmental acquisition of symbiontts in chemosynthetic mytilids.
Abstract: We describe the first reproductive features of a chemosynthetic mussel collected at cold seeps from the eastern Mediterranean Sea. Idas modiolaeformis (Bivalvia, Mytilidae) is a hermaphroditic species in which production of male and female gametes likely alternates, a feature regarded as an adaptation to patchy and ephemeral habitats. By using fluorescent in situ hybridization, we demonstrate that bacterial symbionts, while present within the gills, are absent within acini that enclose female gametes and male gametes. This supports the hypothesis of environmental acquisition of symbionts in chemosynthetic mytilids. Pro- dissoconch I (PI) is relatively small compared to prodisso- conch II (PII), suggesting a planktotrophic larval stage. Diameters of the two larval shells are in the range of sizes reported for mytilids, with a PII size between that of the shallow Mytilus edulis and that of the cold-seep mussel "Bathymodiolus" childressi.

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TL;DR: A general theory and propose mechanisms that could lead to the evolution of keystone molecules, which provide critical information to phylogenetically diverse species, initiate major trophic cascades, and structure communities within terrestrial, freshwater, coastal-Ocean and open-ocean habitats.
Abstract: Molecules of keystone significance are vital in structuring ecological communities. Select bioactive compounds can cause disproportionately large effects by connecting such seemingly disparate processes as microbial loop dynamics and apex predation. Here, we develop a general theory and propose mechanisms that could lead to the evolution of keystone molecules. Introduced into a respective community by one, or only a few, autotrophic or microbial species, these compounds often originate as chemical defenses. When co-opted by resistant consumer species, however, they are used either in chemical defense against higher-order predators or as chemosensory cues that elicit courtship and mating, alarm, and predatory search. Requisite to these multifunctional properties, biosynthetic capacity evolves along with mechanisms for resistance and/or toxin storage in primary producers. Subsequently, consumers acquire resistances or tolerances, and the toxins are transferred through food webs via trophic interactions. In ...

Journal ArticleDOI
TL;DR: It is concluded that GPCRs and these pathways do not mediate settlement and metamorphosis in either coral species and two compounds that had an effect on both species, forskolin and phorbol-12-myristate-13-acetate (TPA), may be acting on other cellular processes not related to GPCR.
Abstract: Larvae of the scleractinian coral Pocillopora damicornis are induced to settle and metamorphose by the presence of marine bacterial biofilms, and the larvae of Montipora capitata respond to a combi...

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TL;DR: All species exhibited as much (or more) sensitivity to red stimuli as to blue/green stimuli, which is consistent with a role for long-wavelength visible light in the preference for substrata observed during settlement and in facilitating vertical positioning of larvae in the water column.
Abstract: Light influences the swimming behavior and settlement of the planktonic planula larvae of coral, but little is known regarding the photosensory biology of coral at this or any life-history stage. Here we used changes in the electrical activity of coral planula tissue upon light flashes to investigate the photosensitivity of the larvae. Recordings were made from five species: two whose larvae are brooded and contain algal symbionts (Porites astreoides and Agaricia agaricites), and three whose larvae are spawned and lack algal symbionts (Acropora cervicornis, Acropora palmata,and Montastrea faveolata). Photosensitivity originated from the coral larva rather than from, or in addition to, its algal symbionts as species with and without symbionts displayed similar tissue-level electrical responses to light. All species exhibited as much (or more) sensitivity to red stimuli as to blue/green stimuli, which is consistent with a role for long-wavelength visible light in the preference for substrata observed during settlement and in facilitating vertical positioning of larvae in the water column.

Journal ArticleDOI
TL;DR: This work is the first to demonstrate that trypsin phenotypic variation in crustacean protein digestion relies on the biochemical properties of the different isoforms, which are relevant for understandingtrypsin polymorphism and protein digestion in lobster.
Abstract: It is well known that crustaceans exhibit several isoforms of trypsin in their digestive system. Although the number of known crustacean trypsin isoforms continues increasing, especially those derived from cDNA sequences, the role of particular isoenzymes in digestion remains unknown. Among invertebrates, significant advances in the understanding of the role of multiple trypsins have been made only in insects. Since it has been demonstrated that trypsin isoenzyme patterns (phenotypes) in lobster differ in digestion efficiency, we used this crustacean as a model for assessing the biochemical basis of such differences. We demonstrated that the trypsin isoform known to be present in all individuals of Panulirus argus has a high catalytic efficiency (kcat/Km ) and is the most reactive toward native proteinaceous substrates, whereas one of the isoforms present in less efficient individuals has a lower kcat and a lower kcat/Km, and it is less competent at digesting native proteins. A fundamental question in bio...

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TL;DR: Since the shell was a crucial adaptation for the evolution of the argonauts’ holopelagic existence, persistence of A. nodosa may be compromised by shell dissolution in an ocean-change world.
Abstract: Shell calcification in argonauts is unique. Only females of these cephalopods construct the paper nautilus shell, which is used as a brood chamber for developing embryos in the pelagic realm. As one of the thinnest (225 m) known adult mollusc shells, and lacking an outer protective periostracum-like cover, this shell may be sus- ceptible to dissolution as the ocean warms and decreases in pH. Vulnerability of the A. nodosa shell was investigated through immersion of shell fragments in multifactorial ex- periments of control (19 °C/pH 8.1; pCO2 419; Ca 4.23) and near-future conditions (24 °C/pH 7.8-7.6; pCO2 932- 1525; Ca 2.72-1.55) for 14 days. More extreme pH treatments (pH 7.4-7.2; pCO2 2454-3882; Ca 1.20- 0.67) were used to assess tipping points in shell dissolution. X-ray diffractometry revealed no change in mineralogy between untreated and treated shells. Reduced shell weight due to dissolution was evident in shells incubated at pH 7.8 (projected for 2070) after 14 days at control temperature, with increased dissolution in warmer and lower pH treat- ments. The greatest dissolution was recorded at 24 °C (projected for local waters by 2100) compared to control temperature across all low-pH treatments. Scanning elec- tron microscopy revealed dissolution and etching of shell mineral in experimental treatments. In the absence of com- pensatory mineralization, the uncovered female brood chamber will be susceptible to dissolution as ocean pH decreases. Since the shell was a crucial adaptation for the evolution of the argonauts' holopelagic existence, persis- tence of A. nodosa may be compromised by shell dissolu- tion in an ocean-change world.

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TL;DR: The stalked barnacle Dosima fascicularis is of special interest as it produces a large amount of foam-like cement that can be used as a float and the morphology of the cement apparatus and of the polymerized cement of this species is almost unknown.
Abstract: Barnacles produce a proteinaceous adhesive called cement to attach permanently to rocks or to other hard substrata. The stalked barnacle Dosima fascicularis is of special interest as it produces a large amount of foam-like cement that can be used as a float. The morphology of the cement apparatus and of the polymerized cement of this species is almost unknown. The current study aims at filling these gaps in our knowledge using light and electron mi- croscopy as well as x-ray microtomography. The shape of the cement gland cells changes from round to ovoid during barnacle development. The cytoplasm of the gland cells, unlike that of some other barnacles, does not have distinct secretory and storage regions. The cement canals, which transport the cement from the gland cells to the base of the stalk, end at different positions in juvenile and mature animals. With increasing size of the cement float, the exit of the cement canals shift from the centrally positioned attach- ment disk of the vestigial antennules to more lateral posi- tions on the stalk. The bubbles enclosed in the foam-like float are most likely filled with CO2 that diffuses from the

Journal ArticleDOI
TL;DR: An association between blue and food was acquired in fewer trials than between yellow and food, perhaps because some prey of juvenile loggerheads in oceanic surface waters (jellyfishes, polyps, and pelagic gastropods) are blue or violet in color.
Abstract: Marine turtles are visual animals, yet we know remarkably little about how they use this sensory capacity. In this study, our purpose was to determine whether log- gerhead turtles could discriminate between objects on the basis of color. We used light-adapted hatchlings to deter- mine the minimum intensity of blue (450 nm), green (500 nm), and yellow (580 nm) visual stimuli that evoked a positive phototaxis (the phototaxis "threshold" (pt)). Juve- nile turtles were later trained to associate each color (pre- sented at 1 log unit above that color's pt) with food, then to discriminate between two colors (the original rewarded stimulus plus one of the other colors, not rewarded) when both were presented at 1 log unit above their pt. In the crucial test, turtles were trained to choose between the rewarded and unrewarded color when the colors varied in intensity. All turtles learned that task, demonstrating color discrimination. An association between blue and food was acquired in fewer trials than between yellow and food, perhaps because some prey of juvenile loggerheads in oce- anic surface waters (jellyfishes, polyps, and pelagic gastro- pods) are blue or violet in color.