Molluscan Biology Research Articles

MolluscDB 2.0: a comprehensive functional and evolutionary genomics database for over 1400 molluscan species.

Mollusca represents the second-largest animal phylum but remains less explored genomically. The increase in high-quality genomes and diverse functional genomic data holds great promise for advancing our understanding of molluscan biology and evolution. To address the opportunities and challenges facing the molluscan research community in managing vast multi-omics resources, we developed MolluscDB 2.0 (http://mgbase.qnlm.ac), which integrates extensive functional genomic data and offers user-friendly tools for multilevel integrative and comparative analyses. MolluscDB 2.0 covers 1450 species across all eight molluscan classes and compiles ∼4200 datasets, making it the most comprehensive multi-omics resource for molluscs to date. MolluscDB 2.0 expands the layers of multi-omics data, including genomes, bulk transcriptomes, single-cell transcriptomes, proteomes, epigenomes and metagenomes. MolluscDB 2.0 also more than doubles the number of functional modules and analytical tools, updating 14 original modules and introducing 20 new, specialized modules. Overall, MolluscDB 2.0 provides highly valuable, open-access multi-omics platform for the molluscan research community, expediting scientific discoveries and deepening our understanding of molluscan biology and evolution.

Genome of the lepidopleurid chiton Hanleya hanleyi (Mollusca, Polyplacophora).

Mollusca is the second most species-rich phylum and includes animals as disparate as octopuses, clams, and chitons. Dozens of molluscan genomes are available, but only one representative of the subphylum Aculifera, the sister taxon to all other molluscs, has been sequenced to date, hindering comparative and evolutionary studies. To facilitate evolutionary studies across Mollusca, we sequenced the genome of a second aculiferan mollusc, the lepidopleurid chiton Hanleya hanleyi (Bean 1844), using a hybrid approach combining Oxford Nanopore and Illumina reads. After purging redundant haplotigs and removing contamination from this 1.3% heterozygous genome, we produced a 2.5 Gbp haploid assembly (>4X the size of the other chiton genome sequenced to date) with an N50 of 65.0 Kbp. Despite a fragmented assembly, the genome is rather complete (92.0% of BUSCOs detected; 79.4% complete plus 12.6% fragmented). Remarkably, the genome has the highest repeat content of any molluscan genome reported to date (>66%). Our gene annotation pipeline predicted 69,284 gene models (92.9% of BUSCOs detected; 81.8% complete plus 11.1% fragmented) of which 35,362 were supported by transcriptome and/or protein evidence. Phylogenomic analysis recovered Polyplacophora sister to all other sampled molluscs with maximal support. The Hanleya genome will be a valuable resource for studies of molluscan biology with diverse potential applications ranging from evolutionary and comparative genomics to molecular ecology.

Slipper snail tales: How Crepidula fornicata and Crepidula atrasolea became model molluscs.

Despite the great abundance and diversity of molluscs, only a few have attained "model research organism" status. One of those species is the slipper snail Crepidula fornicata. Its embryos were first used for classical lineage tracing studies in the late 19th century, and over a 100 years later they were "re-discovered" by our labs and used for modern fate mapping, gene perturbation, in vivo imaging, transcriptomics, and the first application of CRISPR/Cas9-mediated genome editing among the Spiralia/Lophotrochozoa. Simultaneously, other labs made extensive examinations of taxonomy, phylogeny, ecology, life-history, mode of development, larval feeding behavior, and responses to the environment in members of the family Calyptraeidae, which includes the genus Crepidula. Recently, we developed tools, resources, and husbandry protocols for another, direct-developing species, Crepidula atrasolea. This species is an ideal "lab rat" among molluscs. Together these species will be valuable for probing the cellular and molecular mechanisms underlying molluscan biology and evolution.

The hard clam genome reveals massive expansion and diversification of inhibitors of apoptosis in Bivalvia

BackgroundInhibitors of apoptosis (IAPs) are critical regulators of programmed cell death that are essential for development, oncogenesis, and immune and stress responses. However, available knowledge regarding IAP is largely biased toward humans and model species, while the distribution, function, and evolutionary novelties of this gene family remain poorly understood in many taxa, including Mollusca, the second most speciose phylum of Metazoa.ResultsHere, we present a chromosome-level genome assembly of an economically significant bivalve, the hard clam Mercenaria mercenaria, which reveals an unexpected and dramatic expansion of the IAP gene family to 159 members, the largest IAP gene repertoire observed in any metazoan. Comparative genome analysis reveals that this massive expansion is characteristic of bivalves more generally. Reconstruction of the evolutionary history of molluscan IAP genes indicates that most originated in early metazoans and greatly expanded in Bivalvia through both lineage-specific tandem duplication and retroposition, with 37.1% of hard clam IAPs located on a single chromosome. The expanded IAPs have been subjected to frequent domain shuffling, which has in turn shaped their architectural diversity. Further, we observed that extant IAPs exhibit dynamic and orchestrated expression patterns among tissues and in response to different environmental stressors.ConclusionsOur results suggest that sophisticated regulation of apoptosis enabled by the massive expansion and diversification of IAPs has been crucial for the evolutionary success of hard clam and other molluscan lineages, allowing them to cope with local environmental stresses. This study broadens our understanding of IAP proteins and expression diversity and provides novel resources for studying molluscan biology and IAP function and evolution.

MolluscDB: an integrated functional and evolutionary genomics database for the hyper-diverse animal phylum Mollusca.

Mollusca represents the second largest animal phylum but remains poorly explored from a genomic perspective. While the recent increase in genomic resources holds great promise for a deep understanding of molluscan biology and evolution, access and utilization of these resources still pose a challenge. Here, we present the first comprehensive molluscan genomics database, MolluscDB (http://mgbase.qnlm.ac), which compiles and integrates current molluscan genomic/transcriptomic resources and provides convenient tools for multi-level integrative and comparative genomic analyses. MolluscDB enables a systematic view of genomic information from various aspects, such as genome assembly statistics, genome phylogenies, fossil records, gene information, expression profiles, gene families, transcription factors, transposable elements and mitogenome organization information. Moreover, MolluscDB offers valuable customized datasets or resources, such as gene coexpression networks across various developmental stages and adult tissues/organs, core gene repertoires inferred for major molluscan lineages, and macrosynteny analysis for chromosomal evolution. MolluscDB presents an integrative and comprehensive genomics platform that will allow the molluscan community to cope with ever-growing genomic resources and will expedite new scientific discoveries for understanding molluscan biology and evolution.

MolluscDB: an integrated functional and evolutionary genomics database for the hyper-diverse animal phylum Mollusca.

Mollusca represents the second largest animal phylum but remains poorly explored from a genomic perspective. While the recent increase in genomic resources holds great promise for a deep understanding of molluscan biology and evolution, access and utilization of these resources still pose a challenge. Here, we present the first comprehensive molluscan genomics database, MolluscDB (http://mgbase.qnlm.ac), which compiles and integrates current molluscan genomic/transcriptomic resources and provides convenient tools for multi-level integrative and comparative genomic analyses. MolluscDB enables a systematic view of genomic information from various aspects, such as genome assembly statistics, genome phylogenies, fossil records, gene information, expression profiles, gene families, transcription factors, transposable elements and mitogenome organization information. Moreover, MolluscDB offers valuable customized datasets or resources, such as gene coexpression networks across various developmental stages and adult tissues/organs, core gene repertoires inferred for major molluscan lineages, and macrosynteny analysis for chromosomal evolution. MolluscDB presents an integrative and comprehensive genomics platform that will allow the molluscan community to cope with ever-growing genomic resources and will expedite new scientific discoveries for understanding molluscan biology and evolution.

The evo-devo of molluscs: Insights from a genomic perspective.

Molluscs represent one of ancient and evolutionarily most successful groups of marine invertebrates, with a tremendous diversity of morphology, behavior, and lifestyle. Molluscs are excellent subjects for evo-devo studies; however, understanding of the evo-devo of molluscs has been largely hampered by incomplete fossil records and limited molecular data. Recent advancement of genomics and other technologies has greatly fueled the molluscan "evo-devo" field, and decoding of several molluscan genomes provides unprecedented insights into molluscan biology and evolution. Here, we review the recent progress of molluscan genome sequencing as well as novel insights gained from their genomes, by emphasizing how molluscan genomics enhances our understanding of the evo-devo of molluscs.

The genome of the oyster Saccostrea offers insight into the environmental resilience of bivalves.

Oysters are keystone species in estuarine ecosystems and are of substantial economic value to fisheries and aquaculture worldwide. Contending with disease and environmental stress are considerable challenges to oyster culture. Here we report a draft genome of the Sydney Rock Oyster, Saccostrea glomerata, an iconic and commercially important species of edible oyster in Australia known for its enhanced resilience to harsh environmental conditions. This is the second reference genome to be reported from the family Ostreidae enabling a genus-level study of lophotrochozoan genome evolution. Our analysis of the 784-megabase S. glomerata genome shows extensive expansions of gene families associated with immunological non-self-recognition. Transcriptomic analysis revealed highly tissue-specific patterns of expression among these genes, suggesting a complex assortment of immune receptors provide this oyster with a unique capacity to recognize invading microbes. Several gene families involved in stress response are notably expanded in Saccostrea compared with other oysters, and likely key to this species’ adaptations for improved survival higher in the intertidal zone. The Sydney Rock Oyster genome provides a valuable resource for future research in molluscan biology, evolution and environmental resilience. Its close relatedness to Crassostrea will further comparative studies, advancing the means for improved oyster agriculture and conservation.

Molluscan Genomics: Implications for Biology and Aquaculture

As a result of advances in DNA sequencing technology, molluscan genome research, which initially lagged behind that of many other animal groups, has recently seen a rapid succession of decoded genomes. Since molluscs are highly divergent, the subjects of genome projects have been highly variable, including evolution, neuroscience, and ecology. In this review, recent findings of molluscan genome projects are summarized, and their applications to aquaculture are discussed. Recently, 14 molluscan genomes have been published. All bivalve genomes show high heterozygosity rates, making genome assembly difficult. Unique gene expansions were evident in each species, corresponding to their specialized features, including shell formation, adaptation to the environment, and complex neural systems. To construct genetic maps and to explore quantitative trait loci (QTL) and genes of economic importance, genome-wide genotyping using massively parallel, targeted sequencing of cultured molluscs was employed. Molluscan genomics provides information fundamental to both biology and industry. Modern genomic studies facilitate molluscan biology, genetics, and aquaculture.

Integration of sediment contamination with multi-biomarker responses in a novel potential bioindicator (Sepia officinalis) for risk assessment in impacted estuaries

For the purpose of biomonitoring, species that combine ecological and commercial importance may provide a link between ecological and human health risk. The common cuttlefish, Sepia officinalis, holds both characteristics in south-western Europe, albeit remaining unsurveyed in ecotoxicological studies. Cuttlefish collected from an impacted estuary in SW Portugal and a reference location off the coast were analysed for a battery of biomarker responses in the digestive gland and gills. The contrast to reference animals revealed that biomarker responses, especially those related to oxidative stress, were consistent with sediment contamination by PAHs, even in a situation that combines complex toxicant mixtures, moderate levels of contamination and high ecotoxicological diversity. However, environmental parameters related to the differences between shore and estuarine habitats should not be overruled. Also, digestive gland metallothionein retained significant specificity to metals even though previous studies in the area with clams and fish failed to trigger a conclusive response. The highest net differences in biomarker responses were detected in the gills, likely indicating higher sensitivity to environmental stressors. Still, the digestive gland responses were overall the most consistent with sediment contamination and effectively differentiated between estuarine industrial- and rural-impacted sites. The results indicate that S. officinalis may be a candidate to meet the European Union's requirements for efficient biomonitoring programmes, with the additional importance of being cosmopolitan, abundant, commercially valuable and combining the molluscan biology that has been granting bivalves their high value for biomonitoring with foraging behaviour, thus better able to reflect anthropogenic stressors impacting a wider area than sedentary organisms. Nevertheless, further investigations in unpolluted sites are needed to better evaluate the background levels of biomarker responses in the species.

Annotation of the Pearl Oyster Genome

The initial, manual annotation analysis of the pearl oyster genome is reported in the present issue of Zoological Science. Contributors represent a wide array of research fields, including bioinformatics, molecular and cellular biology, fisheries science, biochemistry, biomineralogy, molluscan biology, evolutionary and developmental biology, and paleobiology, reflecting the pearl oyster's broad biological and economic importance. The annotated pearl oyster genome paves the way for future studies in diverse areas including pearl aquaculture, biomineralization, and lophotrochozoan biology.

Freezing in the Antarctic limpet, Nacella concinna

The process of organismal freezing in the Antarctic limpet, Nacella concinna, is complicated by molluscan biology. Internal ice formation is, in particular, mediated by two factors: (a) the provision of an inoculative target for ice formation in the exposed mucus-secreting foot; and (b) osmoconformity to the marine environment. With regard to the first, direct observations of the independent freezing of pedal mucus support the hypothesis that internal ice formation is delayed by the mucal film. As to the second, ice nucleation parametrics of organismal tissue (head, midgut, gonad, foot) and mucus in both inter- and subtidal populations were characterized by high melting points (range = −4.61 to −6.29 °C), with only c.50% of a given sample osmotically active. At this stage it would be premature to ascribe a cryo-adaptive function to the mucus as the protective effects are more readily attributed to the physical properties of the secretion (i.e. viscosity) and their corresponding effects on the rate of heat transfer. As it is difficult to thermally distinguish between the freezing of mucus and the rest of the animal, the question as to whether it is tolerant of internal as well as external ice formation remains problematic, although it may be well suited to the osmotic stresses of organismal freezing.

Introducción: un vistazo a la historia natural de los moluscos

The natural history of molluscs is reviewed with emphasis on recent developments and the proper use of Spanish words in malacological translation. Mesoamerican examples are used to illustrate the general trends of molluscan biology.

Status of molluscan aquaculture on the Pacific coast of Mexico

The Mexican Pacific coastline is 7,165 km long and has 932,365 ha (2.3 million acres) of coastal logoons and estuaries which support many populations of commercially important molluscs. Only 29 of the 67 identified species are intensively exploited along their whole distribution range. Most bivalves are quite expensive in local Mexican markets; prices range from 5 to 20 pesos (5 to 20 U.S. cents) each or 200 to 400 pesos (2 to 4 U.S. dollars) per kilo of scallop adductor muscle and pen shell or snail flesh. Although mollusc production has been steadily rising in the last 10 years, stocks are constantly being depleted and previously overlooked species are being exploited. This inefficient exploitation is a result of inadequate knowledge of molluscan biology and inapproriate regulation which together make it difficult to advise fishermen on wise stock management. Very little is known about the biology and ecology of indigenous species, and this lack of information has been a major limitation on efforts to develop commercial cultures of these species. Although a few commercial enterprises have successfully introduced the Japanese oyster, seed hatcheries are being established. There is also a government mangrove oyster seed hatchery in operation; this hatchery supports the only native species culture.

Bursting neurons command consummatory feeding behavior and coordinated visceral receptivity in the predatory mollusk Pleurobranchaea

The identification of central neuronal loci that command complex and coordinated behavioral expression offers the opportunity to study basic neural mechanisms that determine whether and under what conditions a specific behavior is expressed. It was previously shown in the isolated nervous system of Pleurobranchaea that the bilaterally paired ventral white cells (VWCs) of the buccal ganglion drive cyclic motor output in the neural network recorded in cut nerve roots to the buccal mass during prolonged endogenous burst episodes (Gillette, R., M. U. Gillette, and W. J. Davis (1978) Sot. Neurosci. Abstr. 4: 1210, (1980) J. Neurophysiol. 43: 669-685). Such burst episodes are also inducible by CAMP and its agonists (Gillette, M. U., R. Gillette, and W. J. Davis (1978) Sot. Neurosci. Abstr. 4: 1209; Gillette, R., M. U. Gillette, and W. J. Davis (1982) J. Comp. Physiol. 146: 461-470). The behavioral significance of the activity driven by the VWCs and the nature of their normal extrinsic activators has been a subject for speculation (Gillette, R., M. U. Gillette, and W. J. Davis (1978) Sot. Neurosci. Abstr. 4: 1210, (1980) J. Neurophysiol. 43: 669-685; McClellan, A. D. (1980) Ph.D. thesis, Case Western Reserve University; Croll, R. P., and W. J. Davis (1982) J. Comp. Physiol. 147: 143-153) but has remained to be established by exact specification of cell activity during behavior. In an anterior hemi-animal preparation, which responds to appetitive and emetic stimuli with appropriate behavior, appetitive (food) stimuli, but not emetic substances, activate the previously quiescent VWCs. This activation is characterized by slow depolarization of the membrane potential accompanied by short rhythmic bursts (5 to 8 spikes); it culminates in a prolonged burst episode (sustained depolarization and spiking at 3 to 5 Hz for 0.7 to 5.0 min). Activation of a VWC by squid homogenate resembles in detail the activation of the cell by CAMP and its agonists (M. Gillette, submitted for publication). Appetitive substances can activate the VWCs via stimulation of the oral veil, but they are most effective in the buccal cavity. During the prolonged burst episode activated by squid homogenate, at the time the spike has broadened appreciably, the VWCs begin to drive the extreme retraction/protraction cycles of the radula that are characteristic of feeding behavior. This is consistent with earlier work which demonstrated that spike broadening during the burst is obligatory for driving motor output in the isolated nervous system (Gillette, R., M. U. Gillette, and W. J. Davis (1980) J. Neurophysiol. 43: 669-685). Simultaneously, in concerted action via their peripheral axons, the VWCs stimulate opening of a sphincter-like buccal-esophageal constriction, as well as marked longitudinal contraction and circular dilation of the esophagus, which is a food storage organ. During prolonged VWC burst episodes, solid food material is progressively moved from the buccal cavity into this shortened esophagus by the extreme retraction/protraction movements of the radula, confirming the ingestive nature of this motor pattern. Emetic substances applied to the oral veil or buccal cavity were never observed to produce extensive or prolonged spike activity, nor did they result in bursting of the VWCs. Emetic stimuli produce cyclic buccal mass movements distinctly different from feeding which we interpret as 1 This work was supported by a research grant from the American University of Washington for facilities used in some studies; and Philosophical Society to M. U. G. and National Science Foundation especially Dr. Vera Fretter for her early guidance in molluscan biology. Grant BNS-79-18329 to R. G. We thank Dr. C. L. Prosser, J. London, * To whom correspondence should be addressed, at Department of D. Green, Dr. M. P. Morse, and Dr. F. Delcomyn for helpful discussion Physiology and Biophysics, 524 Burrill Hall, University of Illinois, and critical reading of the manscript; Friday Harbor Laboratories, Urbana, IL 61801.

Biological Notes

BORING POWER OF MAGILUS.—We have received from Mr. Charlesworth a preliminary note giving briefly a result of his study of the genus Magilus, the remarkable testaceous gasteropod that is found immersed in the large hemispherical corals of the genus Meandrina. The current belief, as set forth by Sowerby, Owen, Woodward, and other authorities in molluscan biology who have treated of this coral-inhabiting mollusc, is that Magilus in its young state effects a lodgment in a crevice of a Meandrina, and that as the coral enlarges, the Magilus extends the margins of the mouth of its shell in the form of a cylindrical corrugated tube, the growth of this tube and of the coral proceeding together paripassu, and consequently that there is no penetration of the coral by the Magilus at all. Mr. Charlesworth, however, finds that Magilus not only drives through solid masses of coral in any direction with apparently the same facility that the bivalve Teredo tunnels masses of wood, but he finds that it even surpasses Teredo in its power of suddenly reflecting its shell and returning to the point from which it commenced its advance; and this bending back of the shell upon itself is not accomplished in such natural cavities as frequently prevail in large corals of the Meandrina genus, but in the solid mass of the coral.