disulphide bridges (S‐S) or linearly after oxidising two individual DOPA side chains. Deviations from a repeat motif in preCOL‐D can lead to kinks in the characteristically rod‐like collagen morphology.
Source: From Hagenau et al. (2009). Reproduced with permission from John Wiley & Sons.
Figure 2.11 Localisation of adhesive proteins in the byssal thread and plaque of Mytilus.
Source: From Silverman & Roberto (2011). Reproduced with permission from Springer Nature.
Attachment
To prepare a surface for attachment, the mussel uses the distal tip of the foot to scrub it, removing weakly attached micro fouling and dirt particles (Wiegemann 2005). The foot is then placed firmly on the surface, forming an airtight and watertight seal. Adhesive proteins are secreted and/or released into the ventral pedal groove, and within 3–10 min (Waite 1992) the foot is lifted to reveal a single thread that connects the mussel and its shell to the plaque attached to the surface (Silvermann & Roberto 2011). Using the same process, additional threads are added to the byssus, thus tethering the mussel to the substrate.
Adhesion is a surface physico‐chemical process. It is achieved through a combination of adsorption, mechanical interlocking and molecular diffusion across an interface. The primer proteins fp‐3 and fp‐5, which connect the plaque to the surface, have unusually high DOPA contents (>20%). Both primers are highly hydroxylated and therefore have the potential to form numerous hydrogen bonds (Wiegemann 2005). The primers are also very low‐molecular‐weight proteins, which likely causes them to have greater mobility to dissolve into the interstitial areas of a surface and bond by mechanical interlocking. DOPA not only mediates adhesion to the surface but is also able to form strong hydrogen bonds with hydrophilic polymers, as well as strong complexes with metal ions, metal oxide and silicon oxide present in mineral surfaces (Wiegemann 2005). Also, histidine‐rich domains in preCOLs form crosslinks with metal ions such as Zn2+ and Cu2+ (Harrington & Waite 2007; Figure 2.10B). These bonds are pH sensitive, which in the face of ocean acidification in a climate change scenario could have implications for mussel attachment in suspension culture and for intertidal communities anchored by mussels (O’Donnell et al. 2013; Carrington et al. 2015; see also Chapter 3). Hydrogen bonds and complex formation contribute to the cohesive strength of the adhesive plaque. George et al. (2018) examined the effect of seawater temperature, salinity and dissolved oxygen concentration in M. trossulus, using tensile testing, atomic force miscroscopy (AFM) and amino acid compositional analysis. High temperature (30°C) and hyposalinity (1 psu) had no effect on adhesion strength, while incubation in hypoxia (0.9 mg l−1) caused plaques to have a mottled colouration and to prematurely peel from substrates, leading to a 51% decrease in adhesion strength. AFM imaging of the plaque cuticle found that plaques cured in hypoxia had regions of lower stiffness throughout, indicative of reductions in DOPA crosslinking between adhesive proteins. A better understanding of the dynamics of plaque curing could aid in the design of better synthetic adhesives, particularly in medicine, where adhesion must take place within wet body cavities (see later).
Various abiotic and biotic factors also influence byssal thread formation and strength of attachment. Carrington et al. (2008) examined the effect of water flow on byssal production in four species, M. trossulus, M. galloprovincialis, M. californianus and Modiolus modiolus, and found that for all four, thread formation decreased with flow rates above ~25 cm/s, with the critical flow threshold estimated at 50 cm/s. But how can mussels persist on shores with rates of flow considerably higher than this? Apparently, living as they do in dense beds modulates flow, thereby creating microhabitats that are conducive to thread production. Temperature is another factor that affects thread production. Mytella charruana is native to Central/South America, but has been introduced along the southeastern Atlantic coast of the United States. When water temperature was manipulated to near lethal temperatures 6–9°C for this species – thread production ceased at 10 °C (Brodsky 2011). However, Geukensia demissa collected from the same area produced some threads at 10 °C and showed no difference in mean thread production between 13 and 23 °C, while M. charruana had significantly fewer threads at 13 than at 23 °C. These data suggest that M. charruana may experience difficulty surviving in the wild at 10 °C for extended periods of time, which could have implications for its survival and future spread as an alien species. Garner & Litvaitis (2013a) have shown that M. edulis can increase the strength (see later), number and attachment sites of byssal threads in response to waterborne cues from an array of predators and injured conspecifics. Also, the same authors found that more threads with greater attachment strength were produced when mussels were fouled with epibionts (Garner & Litvaitis 2013b). Epibionts increase the chance of dislodgement due to an increase in hydrodynamic forces exerted on mussels: specifically, a higher drag‐induced loading.
Wave action is probably the factor that has been most often cited as influencing mussel attachment (references in Garner & Litvaitis 2013b). Babarro & Carrington (2011) compared byssus tenacity (attachment) and associated features in mussels at an exposed and a sheltered site in the Ría de Vigo (NW Spain). They found that mussels inhabiting the rougher outer Ría secreted stronger and stiffer threads and had a higher potential to form crosslinks or metal chelation in the byssal collagen in order to gain structural integrity when needed (Figure 2.10B). Their results from reciprocal transplants indicated that mussels have the potential to change byssus diameter and mechanical properties in order to increase strength in stressful abiotic conditions, and can reallocate energy for vital activities such as gonadal and soft tissue growth in more benign environments (see also Babarro & Carrington 2013). However, Moeser & Carrington (2006) and Moeser et al. (2006) suggest that seasonal variations in material properties of the byssus play an even more significant role than wave action in determining mussel attachment strength. They found that thread strength and extensibility increase after autumn and winter, leading to the strongest attachment occurring during the spring, at which point energetic resources switch their focus toward gamete production (see also Zardi et al. 2007). This shift in energetic allocation, combined with increased thread decay, decreases attachment strength throughout the summer, leading to the weakest attachment strength occurring in the autumn. Hawkins & Bayne (1985) estimate that byssus production can consume up to 8% of a mussel’s monthly energy expenditure.
The mechanical properties of byssal threads vary depending on the species. An examination of the material and structural properties of the threads of M. californianus, M. galloprovincialis and M. trossulus indicated that while the material properties of the threads were similar among species, the distal portion of the threads of M. californianus extended further before breaking, leading to a stronger attachment strength (8–17% increase) relative to the other two species. This may be a factor in the domination of M. californianus on wave‐exposed shores on the Pacific coast of North America (Bell & Gosline 1996). The preCOLs in this species are more divergent from those of the other two than the preCOLs of M. galloprovincialis and M. trossulus are from each other. The single most influential factor in the tensile superiority of M. californianus is the greater abundance of silk‐like alanine‐rich sequences in the flanking domains of preCOLs (Harrington & Waite 2007). See Bell & Gosline (1997), Lucas et al. (2002), Brazee & Carrington (2006), Pearce & LaBarbera (2009), Bouhlel et al. (2017), George et al. (2018) and Newcomb et al. (2019) and references therein for additional comparative studies on mytilid thread properties.
As
