Crystal growth kinetics as an architectural constraint on the evolution of molluscan shells

Crystal growth kinetics as an architectural constraint on the evolution of molluscan shells
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DOI:
10.1073/pnas.1907229116
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发表时间:
2019-09
影响因子:
11.1
通讯作者:
Vanessa Schoeppler;R. Lemanis;E. Reich;T. Pusztai;L. Gránásy;I. Zlotnikov
Vanessa Schoeppler;R. Lemanis;E. Reich;T. Pusztai;L. Gránásy;I. Zlotnikov
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Vanessa Schoeppler;R. Lemanis;E. Reich;T. Pusztai;L. Gránásy;I. Zlotnikov

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意义使用经典材料科学的概念,我们扩大我们的理解可能的软体动物外壳形状的宏观形态空间的可能的超微结构,包括他们的水平。这为我们提供了一个独特的机会,探索这种形态空间使用发达的分析,理论和数值工具,并测试壳生物矿化的离散数量的参数的影响。这里提出的物理模型揭示了一个新的光的进化方面的软体动物壳超微结构的制造,并表明,重复的“发现”的一些矿物形态部分反映了一系列的建筑约束所提供的生物矿物生长动力学。软体动物贝壳是研究生物材料形成-结构-功能关系和生物矿化组织形态发生过程的经典模型系统。通常情况下,每个壳由许多高度矿化的超微结构组成,每个超微结构的特征是特定的3D矿物有机结构。令人惊讶的是,在某些情况下,尽管缺乏一个共同的生物化学工具包的生物矿化或同源性的证据,壳从不同的独立进化的物种包含相似的超微结构图案。在本研究中,使用最近开发的物理框架,这是基于一个类比的定向凝固过程和相场模型模拟,我们比较的过程中的超微结构形态的外壳从3个主要的软体动物类:一个双壳类Unio pictorum,头足类鹦鹉螺pompilius,和腹足类Haliotis asinina。我们证明,这些组织的制造是由生物体通过调节控制矿物相的生长动力学的化学和物理边界条件来指导的。这个生物矿化的概念被假定为作为一个建筑约束的软体动物壳的进化,通过定义一个形态空间的可能的壳超微结构,晶体生长的热力学和动力学的界限。
Significance Using notions from classic materials science, we expand our understanding of the macroscopic morphospace of possible molluscan shell shapes to the level of possible ultrastructures that comprise them. This provides us with a unique opportunity to explore this morphospace using well-developed analytical, theoretical, and numerical tools and to test the effects of a discrete number of parameters on shell biomineralization. The physical model presented here sheds a new light on the evolutionary aspect of molluscan shell ultrastructural fabrication and suggests that the repeated “discovery” of some mineral morphologies partially reflects a series of architectural constraints provided by biomineral growth kinetics. Molluscan shells are a classic model system to study formation–structure–function relationships in biological materials and the process of biomineralized tissue morphogenesis. Typically, each shell consists of a number of highly mineralized ultrastructures, each characterized by a specific 3D mineral–organic architecture. Surprisingly, in some cases, despite the lack of a mutual biochemical toolkit for biomineralization or evidence of homology, shells from different independently evolved species contain similar ultrastructural motifs. In the present study, using a recently developed physical framework, which is based on an analogy to the process of directional solidification and simulated by phase-field modeling, we compare the process of ultrastructural morphogenesis of shells from 3 major molluscan classes: A bivalve Unio pictorum, a cephalopod Nautilus pompilius, and a gastropod Haliotis asinina. We demonstrate that the fabrication of these tissues is guided by the organisms by regulating the chemical and physical boundary conditions that control the growth kinetics of the mineral phase. This biomineralization concept is postulated to act as an architectural constraint on the evolution of molluscan shells by defining a morphospace of possible shell ultrastructures that is bounded by the thermodynamics and kinetics of crystal growth.