Nanocrystals as phenotypic expression of genotypes—An example in coralline red algae

Coralline red algae (CRA) are important ecosystem engineers in oceans. They play key roles as a primary food source and carbonate producers in marine habitats. CRA are also vital for modern reef systems, where they act as a substrate for coral growth and stabilizers of reef frameworks. Calcification in CRA occurs as the precipitation of high-magnesium calcite along the polysaccharide microfibrils within the organic walls of individual cells. Through this process, total CRA biomass consists of 80-90% high-magnesian calcite.

However, morphotaxonomic identification of these important marine organisms is hampered because morphological concepts used for their classification do not correspond to molecular data. We present the first analysis of nanoscale features in calcified cell walls of CRA in a globally distributed sample set. Using a simple fracture-based preparation method, nanoscale ultrastructures were gathered using a field-emission scanning electron microscope (SEM). We used the gathered morphological traits based on these cell wall ultrastructures to construct an independent morphological phyletic tree with good congruency with existing CRA molecular phylogenies.

The results of our SEM analyses highlight cellular ultrastructures as a tool to define the phenotypic expression of genotypic information. We illustrate the potential of ultrastructure-based studies to unify morphology with molecular phylogeny. Furthermore, we show a strong biological control of calcification along the fixed organic templates in CRA cell walls, confirming that it is biomineralization in a strict sense. The morphological difference between the primary (PW) and secondary (SW) cell wall crystallites highlights the radically different organization of the organic matrix present in the PW and SW of CRA. Further evidence that PW and SW calcification are controlled by distinct metabolic processes/pathways is offered by the fact that the magnesium-to-calcium ratio of PW and SW calcite is also radically different.

The described skeletal ultrastructures in the secondary cell wall of CRA subfamilies provide an independent morphotaxonomic concept that appears widely consistent with molecular phylogenic clades/subfamilies. This level of distinction was previously only accomplished by the application rarely present soft tissue features in CRA reproductive organs. Secondary wall ultrastructures are in accordance with molecular phylogenies and provide evidence that crystal shapes formed by the secondary calcification step of CRA cells reflect larger phylogenetic CRA groups.

On a higher (sub)- familial taxonomic level, our independent morphological analysis of nanoscale PW ultrastructures corresponds with the phylogenetic clades/subfamilies. This study ultimately highlights the need and potential for detailed and integrative analyses of skeletal ultrastructure-based approaches to complement molecular phylogeny. Only integrating both recent and fossil morphological with molecular data will provide accurate information on the evolutionary relationships of taxa, not only in CRA but also in many other organism groups.

Citation: Auer, G., & Piller, W. E. (2020). Nanocrystals as phenotypic expression of genotypes—An example in coralline red algae. Science Advances, 6, eaay2126. https://doi.org/10.1126/sciadv.aay2126