Molecular mechanisms of biomineralization in marine invertebrates

Abstract

Much recent marine research has been directed towards understanding the effects of anthropogenic-induced environmental change on marine biodiversity, particularly for those animals with heavily calcified exoskeletons, such as corals, molluscs and urchins. This is because life in our oceans is becoming more challenging for these animals with changes in temperature, pH and salinity. In the future, it will be more energetically expensive to make marine skeletons and the increasingly corrosive conditions in seawater are expected to result in the dissolution of these external skeletons. However, initial predictions of wide-scale sensitivity are changing as we understand more about the mechanisms underpinning skeletal production (biomineralization). These studies demonstrate the complexity of calcification pathways and the cellular responses of animals to these altered conditions. Factors including parental conditioning, phenotypic plasticity and epigenetics can significantly impact the production of skeletons and thus future population success. This understanding is paralleled by an increase in our knowledge of the genes and proteins involved in biomineralization, particularly in some phyla, such as urchins, molluscs and corals. This Review will provide a broad overview of our current understanding of the factors affecting skeletal production in marine invertebrates. It will focus on the molecular mechanisms underpinning biomineralization and how knowledge of these processes affects experimental design and our ability to predict responses to climate change. Understanding marine biomineralization has many tangible benefits in our changing world, including improvements in conservation and aquaculture and exploitation of natural calcified structure design using biomimicry approaches that are aimed at producing novel biocomposites.

Ocean Acidification Induces Subtle Shifts in Gene Expression and DNA Methylation in Mantle Tissue of the Eastern Oyster (Crassostrea virginica)

“…Recent studies have begun to clarify the role of particular genes, pathways, and associated molecular mechanisms in the biomineralization process, and their responsiveness to OA across a diverse group of marine calcifiers (see review by Clark, 2020). In bivalves, a principal component of the biomineralization process is the transport of ions between the mantle epithelium and the EPF, in particular Ca 2+ and HCO − 3 , needed for the formation of calcium carbonate.…”

“…While under OA conditions, some bivalves will actually increase their pH EPF above that of pH seawater (e.g., Liu et al, 2020), potentially enabling them to continue calcifying even under highly acidic scenarios. Only recently have investigators studied the molecular mechanisms that regulate calcification within the mantle tissue (see reviews by Clark, 2020;Rajan and Vengatesen, 2020).…”

The pond snail Lymnaea stagnalis

“…More recently, relevant asymmetrically expressed molluscan shell matrix proteins (SMPs) were found using proteomic and transcriptomic datasets in the left and right sides of mantle tissue [30,31]. Recent exciting methodological developments available to the molecular biologist open a new channel for communication between biologists and mineralogists with common interests in a variety of aspects of biomineralization, ranging from structural biology to evo-devo, to material properties and beyond [32,33].…”

Deciphering mollusc shell production: the roles of genetic mechanisms through to ecology, aquaculture and biomimetics

“…It is difficult, if not impossible, to incorporate the wide range of environmental heterogeneity, natural fluctuations and dispersal opportunities over different spatial scales into laboratory experiments (Sanford & Kelly, 2011; Urban et al ., 2016). Thus, it is perhaps not surprising that as experimental protocols become more complicated, using, for example, long experimental timescales and multiple generations, significant resilience is being found within populations to altered environmental conditions, much more than was predicted 10 years ago (Clark, 2020). Whilst such experimental approaches have limitations for predicting future biodiversity patterns at assemblage and ecosystem levels, they have two major advantages.…”

“…It should be also emphasized that whilst ecological studies evaluating molluscs’ resilience to climate change have taken centre stage over recent years, there are many other areas of research where a greater understanding of biomineralization is important. These include evolution of species and particular proteins, global carbon cycling and more applied areas including optimization of aquaculture practices, development of novel bio‐inspired materials (biomimicry) and re‐use of shells for societal sustainability (Clark, 2020). Irrespective of the research field, what the recent ecological and molecular‐related studies highlight is that a full mechanistic understanding of shell production, even in a single species is an enormous task.…”