Synergistic roles for lipids and proteins in the permanent adhesive of barnacle larvae

Gohad, Neeraj V.; Aldred, Nick; Hartshorn, Christopher M.; Lee, Young Jong; Cicerone, Marcus T.; Orihuela, Beatriz; Clare, Anthony S.; Rittschof, Dan; Mount, Andrew S.

doi:10.1038/ncomms5414

Cited by 101 publications

(104 citation statements)

References 52 publications

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“…Overall, spectral features are consistent with previous reports on the chemistry of barnacle and cyprid adhesive interfaces 14, 38, 39. The ν(CH 2 ):Amide III ratios confirms the presence of a lipid rich phase (IV) at the interface between ASW (V) and the gelatinous bulk phase of the surface‐cleaning fluid (III).…”

supporting

confidence: 91%

“…As previously mentioned, barnacle cement does not contain DOPA;10, 11, 12 however, Gohad et al and Dickinson et al demonstrated that cyprid cement and the barnacle cementing apparatus are phosphorylated, respectively 14, 30. Likewise, we observe that the cyprid adhesive plaque ( Figure 4 a), cuticular tissues, and some surface deposits positively stain for phosphorylation (Figure 4b).…”

supporting

confidence: 77%

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Acorn Barnacles Secrete Phase‐Separating Fluid to Clear Surfaces Ahead of Cement Deposition

et al. 2018

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Marine macrofoulers (e.g., barnacles, tubeworms, mussels) create underwater adhesives capable of attaching themselves to almost any material. The difficulty in removing these organisms frustrates maritime and oceanographic communities, and fascinates biomedical and industrial communities seeking synthetic adhesives that cure and hold steadfast in aqueous environments. Protein analysis can reveal the chemical composition of natural adhesives; however, developing synthetic analogs that mimic their performance remains a challenge due to an incomplete understanding of adhesion processes. Here, it is shown that acorn barnacles (Amphibalanus (=Balanus) amphitrite) secrete a phase‐separating fluid ahead of growth and cement deposition. This mixture consists of a phenolic laden gelatinous phase that presents a phase rich in lipids and reactive oxygen species at the seawater interface. Nearby biofilms rapidly oxidize and lift off the surface as the secretion advances. While phenolic chemistries are ubiquitous to arthropod adhesives and cuticles, the findings demonstrate that A. amphitrite uses these chemistries in a complex surface‐cleaning fluid, at a substantially higher relative abundance than in its adhesive. The discovery of this critical step in underwater adhesion represents a missing link between natural and synthetic adhesives, and provides new directions for the development of environmentally friendly biofouling solutions.

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supporting

confidence: 91%

supporting

confidence: 77%

Acorn Barnacles Secrete Phase‐Separating Fluid to Clear Surfaces Ahead of Cement Deposition

et al. 2018

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“…The SYPRO Ruby general protein stain protocol was adapted from the manufacturer' instructions; samples were incubated at room temperature in the dark for 5 h prior to PBS washes and imaging. Pro-Q Diamond stain for phosphoproteins was also developed for protein gels, but has been used for confocal scanning laser microscopy previously (Gohad et al, 2014); samples were incubated with the dye at room temperature in the dark for 1 h prior to PBS washes and imaging. Samples were stained with Pro-Q Diamond and imaged first and then washed and stained with SYPRO Ruby and imaged second, as instructed by the manufacturers.…”

Section: Stainingmentioning

confidence: 99%

“…Mechanisms of barnacle attachment via fluids that undergo curing have garnered scientific interest for applications to control biofouling in industrial (Callow and Callow, 2002;Holm, 2012) and medical contexts (Shivapooja et al, 2013) and bioinspired glues that cure in aqueous environments (Joseph et al, 2011;Kamino, 2013). First, the barnacle cyprid attaches to the substratum via a permanent adhesive, released from cement glands through the two walking appendages, a pair of antennules, embedding them completely, creating an adhesive plaque that anchors them in place (Knight-Jones and Crisp, 1953;Crisp, 1960;Walker, 1971Walker, , 1973Yule and Walker, 1985;Mullineaux and Butman, 1991;Matsumura et al, 1998;Phang et al, 2008;Gohad et al, 2012Gohad et al, , 2014Aldred et al, 2013). The subsequent phases of settlement and metamorphosis for acorn (balanomorph) barnacles involve major changes to the body plan and shape, resulting in a disk-shaped basis parallel to the substratum as a juvenile.…”

Section: Introductionmentioning

confidence: 99%

“…Initially, cyprids adhere using a heterogeneous mixture containing a proteinaceous bulk material (Hillman and Nace, 1970;Saroyan et al, 1970Saroyan et al, , 1996Gohad et al, 2014), including phosphoprotein (Gohad et al, 2014), with an outer barrier (Walker, 1971) that contains lipid (Gohad et al, 2014). Juvenile attachment mechanisms have been less well studied, but it was found that a proteinaceous juvenile cement appears to increase adhesion within 2 weeks of settlement and metamorphosis (Yule and Walker, 1984), earlier than the adult cement system is known to develop (40 days later) (Walker, 1973).…”

Section: Introductionmentioning

confidence: 99%

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Barnacle biology before, during and after settlement and metamorphosis: a study of the interface

Essock‐Burns

Gohad

Orihuela

et al. 2016

Journal of Experimental Biology

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Mobile barnacle cypris larvae settle and metamorphose, transitioning to sessile juveniles with morphology and growth similar to that of adults. Because biofilms exist on immersed surfaces on which they attach, barnacles must interact with bacteria during initial attachment and subsequent growth. The objective of this study was to characterize the developing interface of the barnacle and substratum during this key developmental transition to inform potential mechanisms that promote attachment. The interface was characterized using confocal microscopy and fluorescent dyes to identify morphological and chemical changes to the interface and the status of bacteria present as a function of barnacle developmental stage. Staining revealed patchy material containing proteins and nucleic acids, reactive oxygen species amidst developing cuticle, and changes in bacteria viability at the developing interface. We found that as barnacles metamorphose from the cyprid to juvenile stage, proteinaceous materials with the appearance of coagulated liquid were released into and remained at the interface. It stained positive for proteins, including phosphoprotein, as well as nucleic acids. Regions of the developing cuticle and the patchy material itself stained for reactive oxygen species. Bacteria were absent until the cyprid was firmly attached, but populations died as barnacle development progressed. The oxidative environment may contribute to the cytotoxicity observed for bacteria and has the potential for oxidative crosslinking of cuticle and proteinaceous materials at the interface.

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Bio‐Inspired Self‐Hydrophobized Sericin Adhesive with Tough Underwater Adhesion Enables Wound Healing and Fluid Leakage Sealing

Liu

Qin

Liu

et al. 2022

Adv Funct Materials

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Given that adhesion‐resistance of water severely weakens the bonding strength of tissue adhesives, instant adhesion to wet biological tissue surfaces remains challenging. Inspired by the robust underwater adhesion of natural creatures (such as mussels and barnacles whose underwater adhesion derives from the synergy of hydrophobic and adhesive matrix), a self‐hydrophobized adhesive is developed by co‐assembly of disulfide‐bond hydrolyzed hydrophobic natural sericin protein (a major component of silkworm silk fibers) and tannic acid. Once exposed to water, the self‐aggregation of hydrophobic chains within the adhesive repels water and enhances interfacial hydrogen bonding or electrostatic interactions, mechanistically leading to a robust (>0.5 MPa for solid plates and >0.1 MPa for tissues) and durable (still maintained at 0.4 Mpa even after five cycles) underwater adhesion. Owing to its robust underwater adhesion property, this adhesive possesses multiple advantages outperforming commercial adhesives, such as in vivo wound healing‐promoting effects, effective fluid leakage sealing, and rapid hemostasis activity. This study not only offers a novel strategy for designing and fabricating an underwater adhesive with natural protein but also provides a new adhesive for various potential applications, including promoting wound healing and hemostasis.

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Synergistic roles for lipids and proteins in the permanent adhesive of barnacle larvae

Cited by 101 publications

References 52 publications

Acorn Barnacles Secrete Phase‐Separating Fluid to Clear Surfaces Ahead of Cement Deposition

Acorn Barnacles Secrete Phase‐Separating Fluid to Clear Surfaces Ahead of Cement Deposition

Barnacle biology before, during and after settlement and metamorphosis: a study of the interface

Bio‐Inspired Self‐Hydrophobized Sericin Adhesive with Tough Underwater Adhesion Enables Wound Healing and Fluid Leakage Sealing

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