Byssus Research Articles

Facultative Parasitism by the Bivalve Kurtiella pedroana in the Mole Crab Emerita analoga.

Evolutionary transitions to parasitism are rare. In this study, we documented a potential step toward parasitism in the commensal clam Kurtiella pedroana (Bivalvia: Galeommatoidea). Galeommatoideans are known commensals of various invertebrates, including crustaceans. Emerita analoga (Decapoda: Hippidae) is an abundant intertidal mole crab inhabiting Pacific coast beaches in North and South America. Mole crabs collected from Monterey Bay, California, were measured and examined externally and internally for associated molluscs. Out of the 520 mole crabs, 37 large female individuals harbored 49 clams (prevalence of 7.11% and mean intensity of 1.3). Forty-one ectocommensal clams were attached by their byssal threads to the inside of the gill chambers or to the lateroventral surfaces. However, our key finding was 8 clams that lacked byssal threads and were living in the hemocoel of 6 crabs. These internal clams were smaller than the ectocommensals. Because these internal clams lacked access to their normal food, we hypothesize they might have fed on hemolymph as would a parasite. Clam larvae have no obvious exit from the hemocoel, implying that endoparasitism is a dead-end for K. pedroana. Regardless, facultative parasitism in a free-living or an ectocommensal is uncommon and suggests a pathway to parasitism.

Biomimetic Hybridization of Kevlar into Silk Fibroin: Nanofibrous Strategy for Improved Mechanic Properties of Flexible Composites and Filtration Membranes.

Silk, one of the strongest natural biopolymers, was hybridized with Kevlar, one of the strongest synthetic polymers, through a biomimetic nanofibrous strategy. Regenerated silk materials have outstanding properties in transparency, biocompatibility, biodegradability and sustainability, and promising applications as diverse as in pharmaceutics, electronics, photonic devices and membranes. To compete with super mechanic properties of their natural counterpart, regenerated silk materials have been hybridized with inorganic fillers such as graphene and carbon nanotubes, but frequently lose essential mechanic flexibility. Inspired by the nanofibrous strategy of natural biomaterials (e.g., silk fibers, hemp and byssal threads of mussels) for fantastic mechanic properties, Kevlar was integrated in regenerated silk materials by combining nanometric fibrillation with proper hydrothermal treatments. The resultant hybrid films showed an ultimate stress and Young's modulus two times as high as those of pure regenerated SF films. This is not only because of the reinforcing effect of Kevlar nanofibrils, but also because of the increasing content of silk β-sheets. When introducing Kevlar nanofibrils into the membranes of silk nanofibrils assembled by regenerated silk fibroin, the improved mechanic properties further enabled potential applications as pressure-driven nanofiltration membranes and flexible substrates of electronic devices.

Influencing Mechanism of Ocean Acidification on Byssus Performance in the Pearl Oyster Pinctada fucata.

The byssus is an important adhesive structure by which bivalves robustly adhere to underwater substrates. It is susceptible to carbon dioxide-driven ocean acidification (OA). Previous investigations have documented significant adverse effects of OA on the performance of byssal threads, but the mechanisms remain largely unknown. In this study, multiple approaches were employed to reveal the underlying mechanisms for the effects of OA on byssus production and mechanical properties in the pearl oyster Pinctada fucata. The results showed that OA altered the abundance and secondary structure of byssal proteins and affected the contents of metal ions in distal threads, which together reduced the byssus diameter and amplified byssus nanocavity, causing reductions in mechanical properties (strength and extensibility). Expression analysis of key foot protein genes further confirmed changes in byssal protein abundance. Moreover, comparative transcriptome analysis revealed enrichment of ion transportation- and apoptosis-related categories, up-regulation of apoptosis-related pathways, and down-regulation of the "extracellular matrix-receptor interaction" pathway, which may influence foot locomotion physiology, leading to a decrease in byssus production. This study provides mechanistic insight into the effects of OA on pearl oyster byssus, which should broaden our overall understanding of the impacts of OA on marine ecosystem.

Does peripheral dislodgement contribute to heterozygote deficiencies in blue mussels?

AbstractDifferential loss of heterozygous individuals that move to the periphery of mussel aggregations, where they are at greater risk for dislodgement, has been proposed as an explanation for observed heterozygote deficiencies in blue mussels. To test the dislodgement hypothesis, correlations between heterozygosity and mussel motility, as well as characteristics of byssogenesis and byssal thread attachment strengths, were determined in a wild and a farmed population of blue mussels (Mytilus edulis) from New Hampshire, USA. Although both populations exhibited a heterozygote deficit as measured by three microsatellite loci, no relationship was found between heterozygosity and increased motility in either population. Similarly, no relationship was found between heterozygosity and byssogenesis or attachment strength. Hence, differential dislodgement is highly unlikely as a possible contributor to the loss of heterozygous individuals.

Single-Molecule Mechanics of Catechol-Iron Coordination Bonds.

Metal coordination bonds are widely found in natural adhesives and load-bearing and protective materials, in which they are thought to be responsible for the high mechanical strength and toughness. However, it remains unknown how metal-ligand complexes could give rise to such superb mechanical properties. Here, we developed a single-chain nanoparticle based force spectroscopy to directly quantify the mechanical properties of individual catechol-Fe3+ complexes, the key elements accounting for the high toughness and extensibility of byssal threads of marine mussels. We found that catechol-Fe3+ complexes possess a unique combination of mechanical features, including high mechanical stability, fast reformation kinetics, and stoichiometry-dependent mechanics. Therefore, they can serve as sacrificial bonds to efficiently dissipate energy in the materials, quickly recover the mechanical properties when load is released, and respond to pH and Fe3+ concentrations. Especially, we revealed that the bis-catechol-Fe3+ complex is mechanically ∼90% stronger than the tris-catechol-Fe3+ complex. Quantum calculation study suggested that the distinction between mechanical strength and thermodynamic stability of catechol-Fe3+ complexes is due to their different mechanical rupture pathways. Our study provides the nanoscale mechanistic understanding of the coordination bond-mediated mechanical properties of biogenetic materials, and could guide future rational design and regulation of the mechanical properties of synthetic materials.

Effects of Size-Dependent Allocation of Energy to Maintenance, Growth, and Reproduction on Rehabilitation Success in Overexploited Intertidal Mussels Perna perna (L.)

Mussels play an important supplementary role in the diet of coastal communities in many parts of the world. Over the last three decades, exploitation pressure on the intertidal brown mussel Perna perna on the southeast coast of South Africa has become unsustainable, eliminating mussels from substantial areas of suitable habitat and creating the need to rehabilitate denuded shores. The effect of mussel size on the effectiveness of the rehabilitation technique was tested, hypothesizing that mussel size may influence the effectiveness of rehabilitation due to size-dependent energy allocation (e.g., growth versus reproduction). Immature, small (1–2 cm), and sexually mature larger mussels (3–4 cm) were deployed at four sites, separated by distances of about 100 m, and sampled after 2, 4, and 6 mo. It was found that there were no significant differences between the two size classes in survival rates, which were always high (∽60–80%). There were frequent size effects on the other variables measured, but these tended to depend on the criteria used. Small mussels showed significantly greater growth in terms of shell length, increase in weight, and percentage increase in dry weight. Similarly, small mussels had weaker byssal attachment strength than large mussels, but higher tenacity when attachment strength was normalized to shell area. Small mussels also generally had higher condition indices than large mussels. This was probably related to spawning by adults and the difference was not always significant. For large mussels, maintenance, including byssal thread production to resist dislodgement, seemed to have higher priority than shell growth and condition. The absence of significant differences in tenacity between size classes would explain their similar survival rates. No difference was found between size classes in the numbers of new recruits appearing in experimental patches. Deciding which size class is better for rehabilitation depends on the criterion used. Overall, it was found that ontogenetic reallocation of energy reserves affected neither biomass increase nor survival, probably the most meaningful definitions of success. Given their greater availability and efficiency at increasing biomass, it is suggested that on balance small mussels are likely to be more effective in restoring mussel populations.

Defense Responses to Short-term Hypoxia and Seawater Acidification in the Thick Shell Mussel Mytilus coruscus.

The rising anthropogenic atmospheric CO2 results in the reduction of seawater pH, namely ocean acidification (OA). In East China Sea, the largest coastal hypoxic zone was observed in the world. This region is also strongly impacted by ocean acidification as receiving much nutrient from Changjiang and Qiantangjiang, and organisms can experience great short-term natural variability of DO and pH in this area. In order to evaluate the defense responses of marine mussels under this scenario, the thick shell mussel Mytilus coruscus were exposed to three pH/pCO2 levels (7.3/2800 μatm, 7.7/1020 μatm, 8.1/376 μatm) at two dissolved oxygen concentrations (DO, 2.0, 6.0 mg L−1) for 72 h. Results showed that byssus thread parameters, such as the number, diameter, attachment strength and plaque area were reduced by low DO, and shell-closing strength was significantly weaker under both hypoxia and low pH conditions. Expression patterns of genes related to mussel byssus protein (MBP) were affected by hypoxia. Generally, hypoxia reduced MBP1 and MBP7 expressions, but increased MBP13 expression. In conclusion, both hypoxia and low pH induced negative effects on mussel defense responses, with hypoxia being the main driver of change. In addition, significant interactive effects between pH and DO were observed on shell-closing strength. Therefore, the adverse effects induced by hypoxia on the defense of mussels may be aggravated by low pH in the natural environments.

The recently introduced bivalve Xenostrobus securis has higher thermal and salinity tolerance than the native Brachidontes variabilis and established Mytilopsis sallei

The recently introduced bivalve Xenostrobus securis and the previously introduced Mytilopsis sallei (~30years) are dominant over the native Brachidontes variabilis in estuarine fouling communities in Hong Kong. This study tested whether these introduced species have higher thermal and salinity tolerance than the native species under local subtropical seawater conditions. Survival, attachment, clearance rate and byssal thread production of these three species were examined through 96-h acute temperature and salinity tests. The results indicated that X. securis responded normally over a wide range of temperature and salinity conditions. Though M. sallei exhibited a wide salinity tolerance, its sub-lethal responses decreased in cold-seawater conditions. Brachidontes variabilis had the narrowest tolerance to temperature and salinity. These findings may explain the dominance of the non-native bivalves over B. variabilis. The high tolerance of X. securis enables them to become highly invasive in subtropical regions across Southeast Asia, impacting natural communities and shellfish farming.

Ocean acidification decreases mussel byssal attachment strength and induces molecular byssal responses

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 565:67-77 (2017) - DOI: https://doi.org/10.3354/meps11992 Ocean acidification decreases mussel byssal attachment strength and induces molecular byssal responses Xinguo Zhao1, Cheng Guo1, Yu Han1, Zhumei Che2, Yichen Wang1, Xiying Wang1, Xueliang Chai3, Hongxi Wu3, Guangxu Liu1,* 1College of Animal Sciences, Zhejiang University, Hangzhou 310058, PR China 2Marine Monitoring and Forecasting Center of Zhejiang, Hangzhou 310007, PR China 3Zhejiang Mariculture Research Institute, Wenzhou 325000, PR China *Corresponding author: guangxu_liu@zju.edu.cn ABSTRACT: Ocean acidification (OA) is a term describing the uptake of CO2 from the atmosphere, decreasing seawater pH and altering carbonate chemistry. Mussels are an ecologically and economically important taxon that attach to solid surfaces via the byssus. To date, little is known about the effects of OA on mussel byssal attachment and the underlying molecular byssal responses. This study demonstrated that after 1 wk of exposure to acidified seawater, both mechanical properties (such as strength and extensibility) and the numbers of byssal threads produced by Mytilus coruscus were significantly reduced, leading to a 60 to 65% decrease in mussel byssal attachment strength. Real-time PCR results suggested that OA also altered the expression of genes encoding the proximal thread matrix protein (PTMP), precursor collagen proteins (preCOL-P, -NG and -D) and mussel foot proteins (mfp-1, -2, -3, -4, -5 and -6). The down-regulation of some specific byssal proteins may be one of the reasons for the weakened mechanical properties of individual byssal threads under OA conditions. In contrast, the up-regulation of some other specific byssal proteins may be adaptive responses to minimize the adverse effect of OA on byssal attachment. OA may weaken mussel byssal attachment by reducing the production and mechanical properties of byssal threads and by inducing byssal molecular responses. The weakened byssal attachment induced by OA therefore could pose a substantial threat to both mussel aquaculture and mussel-bed ecosystems. KEY WORDS: Elevated pCO2 · Mytilus coruscus · Byssal thread · Gene expression · Mechanical properties Full text in pdf format Supplementary material PreviousNextCite this article as: Zhao X, Guo C, Han Y, Che Z and others (2017) Ocean acidification decreases mussel byssal attachment strength and induces molecular byssal responses. Mar Ecol Prog Ser 565:67-77. https://doi.org/10.3354/meps11992 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 565. Online publication date: February 17, 2017 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2017 Inter-Research.

Why mussels stick together: spatial self-organization affects the evolution of cooperation

Cooperation with neighbours may be crucial for the persistence of populations in stressful environments. Yet, cooperation is often not evolutionarily stable, since non-cooperative individuals can reap the benefits of cooperation without having to pay the costs associated with cooperation. Here we show that active aggregation leading to self-organized spatial pattern formation can promote the evolution of cooperativeness. To this end, we study the effect of movement strategies on the evolution of cooperation in mussel beds. Mussels cooperate by attaching themselves to neighbours via byssal threads, thereby providing mutual protection. Using an individual-based model for mussel bed formation, we first demonstrate that the spatial pattern and the corresponding number of neighbours strongly depends on the movement strategies of the mussels. With an evolutionary model, we then show that this has important implications for the evolution of cooperation, since the evolved level of cooperativeness (the number of byssus threads produced) strongly depends on the number of neighbours and on the harshness and variability of the environment. Our results suggest that spatial aggregation, abundantly found in self-organized ecosystems, may promote the evolution of cooperation.

Superior Fatigue Resistant Bioinspired Graphene‐Based Nanocomposite via Synergistic Interfacial Interactions

Excellent fatigue resistance is a prerequisite for flexible energy devices to achieve high and stable performance under repeated deformation state. Inspired by the sophisticated interfacial architecture of nacre, herein a super fatigue‐resistant graphene‐based nanocomposite with integrated high tensile strength and toughness through poly(dopamine)‐nickel ion (Ni2+) chelate architecture that mimics byssal threads is demonstrated. These kind of synergistic interfacial interactions of covalent and ionic bonding effectively suppress the crack propagation in the process of fatigue testing, resulting in superhigh fatigue life of this bioinspired graphene‐based nanocomposite (BGBN). In addition, the electrical conductivity is well kept after fatigue testing. The proposed synergistic interfacial interactions could serve as a guideline for fabricating high‐performance multifunctional BGBNs with promising applications in flexible energy devices, such as flexible electrodes for supercapacitors and lithium batteries, etc.

Histidine–Zinc Interactions Investigated by Isothermal Titration Calorimetry (ITC) and their Application in Self‐Healing Polymers

Histidine–zinc interactions are believed to play a key role in the self‐healing behavior of mussel byssal threads due to their reversible character. Taking this as inspiration, the authors synthesize here histidine‐rich copolymers, as well as model histidine compounds and characterize them using isothermal titration calorimetry (ITC). With this approach, the influence of two different zinc(II) salts and the role in the complex formation of the amine function of the imidazole ring are investigated in detail. The extracted metal–ligand ratios are utilized to design novel self‐healing metallopolymers. For this purpose, n‐lauryl methacrylate is copolymerized with the histidine monomer via reversible addition‐fragmentation chain transfer polymerization. The copolymers are crosslinked using different zinc salts, and the resulting coatings are characterized with Raman spectroscopy to investigate the metal coordination behavior and with scratch healing tests to investigate the self‐healing capacity. Finally, the self‐healing behavior of the different materials is correlated with the metal–ligand binding affinity measured by ITC. image

A Method for Evaluating the Efficacy of Antifouling Paints Using Mytilus galloprovincialis in the Laboratory in a Flow-Through System.

A laboratory test with a flow-through system was designed and its applicability for testing antifouling paints of varying efficacies was investigated. Six different formulations of antifouling paints were prepared to have increasing contents (0 to 40 wt.%) of Cu2O, which is the most commonly used antifouling substance, and each formulation of paint was coated on just one surface of every test plate. The test plates were aged for 45 days by rotating them at a speed of 10 knots inside a cylinder drum. A behavioral test was then conducted using five mussels (Mytilus galloprovincialis) that were pasted onto the coated surface of each aged test plate. The number of the byssus threads produced by each mussel generally decreased with increasing Cu2O content of the paint. The newly designed method was considered valid owing to the high consistency of its results with observations from the field experiment.

Physiological effects of biocide on marine bivalve blue mussels in context prevent macrofouling

Mussels are stubborn organisms attached to solid substrata by means of byssus threads. The abundance of marine mussel Mytilus edulis in marine facilities like power stations was reason to select among fouling animals. Mortality patterns as well as physiological behavior (oxygen consumption, foot activity, and byssus thread production) of two different size groups (14- and 25-mm shell length) of M. edulis were studied at different hydrogen peroxide concentrations (1–4 mg l−1). Studied mussels showed progressive reduction in physiological activities as the hydrogen peroxide concentration increased. Mussel mortality was tested in 30 days exposure, and 14 mm mussels reached the highest percentage of 90% while 25 mm mussels reached 81%. Produced data was echoed by Chick-Watson model extracted equation. This study points that, while it could affect the mussel mortality moderately in its low concentrations, hydrogen peroxide has a strong influence on mussels’ physiological activities related to colonization. Therefore, hydrogen peroxide can be an alternative for preventing mussel colonization on facilities of marine environment.

Antifouling Activity towards Mussel by Small-Molecule Compounds from a Strain of Vibrio alginolyticus Bacterium Associated with Sea Anemone Haliplanella sp.

Mussels are major fouling organisms causing serious technical and economic problems. In this study, antifouling activity towards mussel was found in three compounds isolated from a marine bacterium associated with the sea anemone Haliplanella sp. This bacterial strain, called PE2, was identified as Vibrio alginolyticus using morphology, biochemical tests, and phylogenetic analysis based on sequences of 16S rRNA and four housekeeping genes (rpoD, gyrB, rctB, and toxR). Three small-molecule compounds (indole, 3-formylindole, and cyclo (Pro-Leu)) were purified from the ethyl acetate extract of V. alginolyticus PE2 using column chromatography techniques. They all significantly inhibited byssal thread production of the green mussel Perna viridis, with EC50 values of 24.45 μg/ml for indole, 50.07 μg/ml for 3-formylindole, and 49.24 μg/ml for cyclo (Pro-Leu). Previous research on the antifouling activity of metabolites from marine bacteria towards mussels is scarce. Indole, 3-formylindole and cyclo (Pro-Leu) also exhibited antifouling activity against settlement of the barnacle Balanus albicostatus (EC50 values of 8.84, 0.43, and 11.35 μg/ml, respectively) and the marine bacterium Pseudomonas sp. (EC50 values of 42.68, 69.68, and 39.05 μg/ml, respectively). These results suggested that the three compounds are potentially useful for environmentally friendly mussel control and/or the development of new antifouling additives that are effective against several biofoulers.

Sole and Combined Usage of Ultra-sonication and Hydrogen Peroxide as Mitigation Techniques of Bio-fouling

Mussels are stubborn organism attached to solid substrate by byssus threads and caused operational problems in utility of power generating stations. Sole and combined usage of ultrasonic (28 kHz- and 42 kHz- frequencies) and hydrogen peroxide (H2O2) has studied for control of blue mussel larvae and adult stage in seawater condition. A theoretical wo rking model using disinfection (Chick and Watson type) approaches is presented based on helpful results of experiments. This study also demonstrate that the combined treatment (ultra-sonication with H2O2) is overall highly efficient than individual treatment would, but on the basis of exposure time, the ultra-sonication was the most efficient among them. Therefore the development of sole and combined technique might be effective practical mitigation strategy against mussel attachment for water handling facilities.

Borniopsis mortoni sp. n. (Heterodonta, Galeommatoidea, Galeommatidaesensu lato), a new bivalve commensal with a synaptid sea cucumber from Japan.

The Galeommatoidea is a bivalve superfamily that exhibits high species diversity in shallow waters. Many members of this superfamily are associated commensally with burrowing marine invertebrates in benthic sediments. The genus Borniopsis is known only from eastern Asia and exhibits high host diversity (e.g., mantis shrimps, crabs, holothurians, sipunculans and echiurans). A new species, Borniopsis mortoni sp. n., is described from mud flats at the mouth of the Souzu River, southwestern Shikoku Island, Japan. This species has elongate-ovate shells covered by a tan to dark brown periostracum, and lives attached by both its foot and byssal threads to the body surface of the synaptid sea cucumber Patinapta ooplax. Several individuals of Borniopsis mortoni are often found on the same host, but sometimes more than 10 individuals can occur together. Borniopsis mortoni is one of the smallest species in this genus. Probably, its small body size is an adaptation to the mode of life in a narrow host burrow. Until now, only two other Borniopsis species were known to have commensal associations with synaptids. Thus, this is the third example of a synaptid-associated species from this genus. In addition, we briefly review the galeommatoideans commensal with apodid sea cucumbers.

Rolling Cockles: Shell Abrasion and Repair in a Living Bivalve Cerastoderma edule L.

ABSTRACTLive cockles were eroded from a tidal flat by a storm event and naturally transported to a nearby dike and beach. Their fate was observed regularly for two months. Some died from desiccation high on the shore, and some were consumed by oystercatchers. Others were caught by the byssus threads of mussels inhabiting the intertidal area, while a few tried to reburrow high on the shore. These cockles were supposedly rolled while being transported to the beach and were later observed being rolled by the waves just below the high water line. Hence, it was concluded that the shells were subjected to abrasion and that this was the cause of the holes that some individuals developed near the umbo of one or both of their (still articulated) valves. A few had repaired such holes, supporting the hypothesis that these holes were made during rolling transportation. Similar shell assemblages of articulated cockleshells partly with subumbonal; holes were later found elsewhere on the Wadden Sea coast of Texel. This “natural” experiment and the repair indicated that this abrasion occurred while the cockles were still alive, and not after their death. It may also help to better discriminate between biologically and physically produced traces on shells.

PH‐Responsive Self‐Organization of Metal‐Binding Protein Motifs from Biomolecular Junctions in Mussel Byssus

Mussels rapidly fabricate tough and self‐healing biopolymeric fibers called byssal threads that provide an excellent role model for bio‐inspired design. The remarkable tensile properties arise from a collagenous protein family known as preCols, which self‐assemble into a semicrystalline array in the distal thread core. Histidine‐rich domains (HRDs) at the preCol ends are critical both for the self‐healing capacity and for the thread assembly process due to their propensity for coordinating transition metal ions; however, very little is understood about the molecular relationship between HRD sequence, structure, and function. Here, a comprehensive spectroscopic investigation of two model peptides based on conserved repetitive motifs in the HRDs is performed to elucidate molecular level details of their role in thread assembly and function. It is observed that environmental factors relevant to the natural assembly process (e.g., concentration, pH, and metal content) trigger dramatic changes in HRD nanostructure and higher order assembly, leading to the formation of highly defined backbone conformation and metal binding geometry.

Cooperative behavior of a sacrificial bond network and elastic framework in providing self-healing capacity in mussel byssal threads.

The dissipative and self-healing properties of mussel byssal threads are critical for their function as anchoring fibers in wave-battered habitats and central to their emergence as an exciting model system for bio-inspired polymers. Much is now understood about the structure-function relationships defining this remarkable proteinaceous bio-fiber; however, the molecular mechanisms underlying the distinctive tough, viscoelastic and self-healing behavior are still unclear. Here, we investigate elastic and dissipative contributions from the primary load-bearing proteins in the distal region of byssal threads (the preCols) using X-ray diffraction (XRD) combined with in situ tensile testing. Specifically, we identified cross β-sheet structure in the preCol flanking domains that functions as an elastic framework, providing hidden length. Dissipative behavior was associated with a strain-rate dependent phase transition of a sacrificial network stabilized by strong, reversible cross-links. Based on these findings, we posit a new model for byssal thread deformation and self-healing.