Shapeshifting in the Venus flytrap (Dionaea muscipula): Morphological and biomechanical adaptations and the potential costs of a failed hunting cycle.

The evolutionary roots of carnivory in the Venus flytrap (Dionaea muscipula) stem from a defense response to plant injury caused by, e.g., herbivores. Dionaea muscipula aka. Darwin's most wonderful plant underwent extensive modification of leaves into snap-traps specialized for prey capture. Even the tiny seedlings of the Venus flytrap already produce fully functional, millimeter-sized traps. The trap size increases as the plant matures, enabling capture of larger prey. The movement of snap-traps is very fast (~100-300 ms) and is actuated by a combination of changes in the hydrostatic pressure of the leaf tissue with the release of prestress (embedded energy), triggering a snap-through of the trap lobes. This instability phenomenon is facilitated by the double curvature of the trap lobes. In contrast, trap reopening is a slower process dependent on trap size and morphology, heavily reliant on turgor and/or cell growth. Once a prey item is caught, the trap reconfigures its shape, seals itself off and forms a digestive cavity allowing the plant to release an enzymatic cocktail to draw nutrition from its captive. Interestingly, a failed attempt to capture prey can come at a heavy cost: the trap can break during reopening, thus losing its functionality. In this mini-review, we provide a detailed account of morphological adaptations and biomechanical processes involved in the trap movement during D. muscipula hunting cycle, and discuss possible reasons for and consequences of trap breakage. We also provide a brief introduction to the biological aspects underlying plant motion and their evolutionary background.

Smooth or with a Snap! Biomechanics of Trap Reopening in the Venus Flytrap (Dionaea muscipula).

Fast snapping in the carnivorous Venus flytrap (Dionaea muscipula) involves trap lobe bending and abrupt curvature inversion (snap-buckling), but how do these traps reopen? Here, the trap reopening mechanics in two different D. muscipula clones, producing normal-sized (N traps, max. ≈3 cm in length) and large traps (L traps, max. ≈4.5 cm in length) are investigated. Time-lapse experiments reveal that both N and L traps can reopen by smooth and continuous outward lobe bending, but only L traps can undergo smooth bending followed by a much faster snap-through of the lobes. Additionally, L traps can reopen asynchronously, with one of the lobes moving before the other. This study challenges the current consensus on trap reopening, which describes it as a slow, smooth process driven by hydraulics and cell growth and/or expansion. Based on the results gained via three-dimensional digital image correlation (3D-DIC), morphological and mechanical investigations, the differences in trap reopening are proposed to stem from a combination of size and slenderness of individual traps. This study elucidates trap reopening processes in the (in)famous Dionaea snap traps - unique shape-shifting structures of great interest for plant biomechanics, functional morphology, and applications in biomimetics, i.e., soft robotics.

Pseudo-Biomineralization: Complex Mineral Structures Shaped by Microbes.

Biomineralization is an active, biologically governed process of mineral formation, established early on in the history of life. The appearance of biomineralizing organisms heavily influenced the course of evolution, leading to the development of the large diversity of the extant taxa. Yet, we are still only beginning to grasp the intricate, genetically regulated mechanisms involved. Since prokaryotic organisms were the first to emerge from the primordial environments, we investigated bacteria-mineral interactions using titration and gas diffusion systems adapted to emulate conditions, which may have facilitated the development of biomineralization initially. By screening the minerals and bacteria from titration experiments with scanning electron microscopy, we discovered a broad spectrum of behavioral strategies employed by bacteria confronted with calcification, which fell into three main categories: (1) evasion of mineralization by the formation of the biofilm, (2) random embedding into the mineral, and (3) control over the mineral shape during its formation. The latter phenomenon we termed pseudo-biomineralization. Our experiments indicate that pseudo-biomineralization is an active process obligatorily reliant on the external calcifying conditions and allowing considerable degree of control over mineral shape, thus producing structures reminiscent of true biominerals. Here, we describe this notion for the first time, thus providing vital insight into the genesis of a transitional stage to calcium carbonate-based biomineralization systems.

The requirement for calcification differs between ecologically important coccolithophore species.

Coccolithophores are globally distributed unicellular marine algae that are characterized by their covering of calcite coccoliths. Calcification by coccolithophores contributes significantly to global biogeochemical cycles. However, the physiological requirement for calcification remains poorly understood as non-calcifying strains of some commonly used model species, such as Emiliania huxleyi, grow normally in laboratory culture. To determine whether the requirement for calcification differs between coccolithophore species, we utilized multiple independent methodologies to disrupt calcification in two important species of coccolithophore: E. huxleyi and Coccolithus braarudii. We investigated their physiological response and used time-lapse imaging to visualize the processes of calcification and cell division in individual cells. Disruption of calcification resulted in major growth defects in C. braarudii, but not in E. huxleyi. We found no evidence that calcification supports photosynthesis in C. braarudii, but showed that an inability to maintain an intact coccosphere results in cell cycle arrest. We found that C. braarudii is very different from E. huxleyi as it exhibits an obligate requirement for calcification. The identification of a growth defect in C. braarudii resulting from disruption of the coccosphere may be important in considering their response to future changes in ocean carbonate chemistry.

The role of the cytoskeleton in biomineralisation in haptophyte algae.

The production of calcium carbonate by coccolithophores (haptophytes) contributes significantly to global biogeochemical cycling. The recent identification of a silicifying haptophyte, Prymnesium neolepis, has provided new insight into the evolution of biomineralisation in this lineage. However, the cellular mechanisms of biomineralisation in both calcifying and silicifying haptophytes remain poorly understood. To look for commonalities between these two biomineralisation systems in haptophytes, we have determined the role of actin and tubulin in the formation of intracellular biomineralised scales in the coccolithophore, Coccolithus braarudii and in P. neolepis. We find that disruption of the actin network interferes with secretion of the biomineralised elements in both C. braarudii and P. neolepis. In contrast, disruption of the microtubule network does not prevent secretion of the silica scales in P. neolepis but results in production of abnormally small silica scales and also results in the increased formation of malformed coccoliths in C. braarudii. We conclude that the cytoskeleton plays a crucial role in biomineralisation in both silicifying and calcifying haptophytes. There are some important similarities in the contribution of the cytoskeleton to these different forms of biomineralisation, suggesting that common cellular mechanisms may have been recruited to perform similar roles in both lineages.

A role for diatom-like silicon transporters in calcifying coccolithophores.

Biomineralization by marine phytoplankton, such as the silicifying diatoms and calcifying coccolithophores, plays an important role in carbon and nutrient cycling in the oceans. Silicification and calcification are distinct cellular processes with no known common mechanisms. It is thought that coccolithophores are able to outcompete diatoms in Si-depleted waters, which can contribute to the formation of coccolithophore blooms. Here we show that an expanded family of diatom-like silicon transporters (SITs) are present in both silicifying and calcifying haptophyte phytoplankton, including some globally important coccolithophores. Si is required for calcification in these coccolithophores, indicating that Si uptake contributes to the very different forms of biomineralization in diatoms and coccolithophores. Significantly, SITs and the requirement for Si are absent from highly abundant bloom-forming coccolithophores, such as Emiliania huxleyi. These very different requirements for Si in coccolithophores are likely to have major influence on their competitive interactions with diatoms and other siliceous phytoplankton.