Organization and crystallography of the microstructures of bryozoans (Phylum Bryozoa) and serpulids (Phylum Annelida)
- Autores: Cristian Grenier Romero
- Directores de la Tesis: Antonio Gerardo Checa González (dir. tes.)
- Lectura: En la Universidad de Granada ( España ) en 2024
- Idioma: inglés
- ISBN: 9788411954525
- Número de páginas: 244
- Tribunal Calificador de la Tesis: Ismael Coronado (presid.), Julio Aguirre Rodríguez (secret.), Elizabeth Harper (voc.)
- Programa de doctorado: Programa de Doctorado en Ciencias de la Tierra por la Universidad de Granada
- Materias:
- Enlaces
- Tesis en acceso abierto en: DIGIBUG
- Resumen
Introduction and motivation:
Marine calcifying organisms have a great significance in the biodiversity and stability of the ecosystems they inhabit. They play a key role as global carbon dioxide reservoirs and are of major economic relevance, both in food production and biotechnology applications.
The investigation of their microstructures, mineralogy, and crystallography holds paramount importance for a comprehensive understanding of their biomechanical properties, their biomineralization processes, and their susceptibility to the intrinsic factors associated with climate change (e.g., variations in ocean acidity and temperature). However, while major marine calcifying taxa (such as corals, mollusks, echinoderms, and foraminifera) have garnered considerable attention and research in recent decades, other groups, albeit less recognized but equally important, have been comparatively understudied.
This is the case of the two principal classes of bryozoans (stenolaemates and gymnolaemates) and of the serpulid polychaetes. Both are marine calcifying animals that belong to different phyla. They build calcium carbonate skeletons and are pivotal in marine ecosystems worldwide. They produce sophisticated microstructures for which little to nothing is known regarding their crystallography or their biomineralization processes.
The present Ph.D. work aims at elucidating the mineralogy and crystallography of the main microstructures found in bryozoans and serpulids. Further, we unravel the biomineralization processes inherent to each group considering the morphology of the microstructures, their growth dynamics, and the theoretical position of the secretory epithelium.
Methods:
For this purpose, we have applied high-resolution techniques such as scanning electron microscopy (SEM) and associated techniques: energy dispersive spectroscopy (EDX), focused ion beam (FIB), and electron backscatter diffraction (EBSD). We have completed the micro and nano-structural analysis with micro-computed tomography (micro-CT) and atomic force microscopy (AFM), respectively. Likewise, we have studied the mineralogy and characterized the organic fraction using X-ray diffraction (XRD), RAMAN and Fourier transform infrared spectroscopy (FTIR), and thermogravimetric analysis (TGA).
Objectives:
Within the framework of a major research project on diverse marine calcifying organisms (I+D Spanish National Project CGL 2017-85118-P) the present Ph.D. thesis (FPI fellowship PRE-2018-085419) focuses on applying high-resolution techniques to perform an in-depth study to elucidate the microstructures and crystallography of the bryozoans and serpulid polychaetes skeletons.
Therefore, the main objective of the present Ph.D. work is to determine the degree of organization and the physical and biological factors operating on the microstructures of bryozoans and serpulids polychaetes.
To achieve this objective, the following goals were established: 1. Characterize the organization and crystallography of bryozoan microstructures: - Study the calcitic microstructures of stenolaemate bryozoans.
- Identify the calcitic and aragonitic microstructures of gymnolaemate bryozoans.
- Analyze the membranes and organic matrices involved in the biomineralization process.
- Establish the relationship between the position of the calcifying epithelium, the morphology of the microstructures, and the growth mechanisms.
2. Determine the organization and crystallography of microstructures of serpulid polychaetes: - Identify the calcitic and aragonitic microstructures of the different genera selected.
- Study the membranes and organic matrices involved in the biomineralization process.
- Investigate the relationship of the calcifying epithelium at the growing edge of the tube.
- Elucidate the biomineralization processes that occur in serpulids.
Results:
To achieve the aforementioned objectives, this Ph.D. study is divided into three main lines of research: - Bryozoan class Stenolaemata. We have studied the microstructures, mineralogy, and crystallography of three extant species (Fasciculipora ramosa, Hornera robusta, and Cinctipora elegans). We differentiate two sophisticated microstructures: foliated calcite and tabular calcite. For each one, we have established consistent models of their crystallography. Foliated calcite is present in Fasciculipora ramosa and Cinctipora elegans and consists of co-oriented laths arranged with their c-axes aligned to their elongation axis and parallel to their main surfaces. One of the a*-axis is perpendicular to the main surfaces. The foliated calcite displays a well-defined sheet texture. In contrast, the tabular calcite is only present in Hornera robusta and consists of polygonal tablets with the c-axis as the fiber axis, perpendicular to the tablet surface. Thus, tabular calcite displays a characteristic axial texture.
- Bryozoans class Gymnolaemata. We have studied the microstructures, mineralogy, and crystallography of eight extant cheilostome species (Calpensia nobilis, Schizobrachiella sanguinea, Rhynchozoon neapolitanum, Schizoretepora serratimargo, Pentapora fascialis, Adeonella pallasii, Schizomavella cornuta, and Smittina cervicornis). We have distinguished five basic microstructures, three calcitic (tabular, irregularly platy and granular) and two aragonitic (granular-platy and fibrous). The calcitic microstructures consist of crystal aggregates that transition from tabular or irregularly platy to granular assemblies toward the interior of the zooid chambers. Fibrous aragonite consists of fibers arranged into spherulites. In all cases, the crystallographic textures are axial, and stronger in aragonite than in calcite, with the c-axis as the fiber axis. We reconstruct the biomineralization sequence in the different species by taking into account the distribution and morphology of the growth fronts of crystals and the location of the secretory epithelium.
- Serpulid polychaetes. We have reviewed the microstructures of seven different serpulid species (Cruzigera websteri, Spirobranchus triqueter, Serpula vermicularis, Spirobranchus giganteus, Serpula crenata, Crucigera zygphora, and Floriprotis sabiuraensis), and studied their mineralogy and crystallography. We have identified three main microstructures: granular-prismatic and lamello-fibrillar calcite, and fibrous aragonite. The granular-prismatic may present two different appearances: finely unoriented and coarsely oriented prisms. Serpulids generally have a high amount of organic matter within the tube structure, consisting of chitin + proteins. Calcite is always present as medium to high magnesium calcite. Except for the finely granular-prismatic, which displays a scattered texture for all their crystallographic axes, the rest of the microstructures display axial textures, with the c-axis aligned with the crystal elongation axis.
Conclusions:
We conclude that stenolaemate bryozoans, despite being an older group and currently having less evolutionary success, present more sophisticated microstructures than gymnolaemates. This is due to the secretory epithelium being close to the forming shell in the former. The foliated calcite of stenolaematans is homeomorph to that of bivalves but has significantly different crystallography. As for the tabular calcite, it lacks the spiral morphology of the tablet-shaped calcite of craniiform brachiopods, differing also in their crystallography. Conversely, except for the tabular calcite, the biomineralization in gymnolaematans is remote and occurs within a relatively wide extrapallial space, which is consistent with the inorganic-like appearance of the microstructures, whose surfaces show signs of free growth.
In serpulids, recrystallization processes are widespread. Only the external coarse prismatic layer and the lamello-fibrillar are primary (i.e. directly secreted by the animal) microstructures. Secondary (i.e. substitution) microstructures grow within the primary calcitic microstructures and retain remnants of the original structures, such as vestigial crystals or major growth increments. We conclude that the absence of a proper extrapallial space in serpulids and their characteristic growth by episodic increments is directly related to the biomineralization by high-magnesium calcite, which eventually favors the recrystallization processes. The high-ordered arrangement of the lamello-fibrillar microstructure may be explained by a previous cholesteric liquid crystal phase of the organic precursors, which would serve as a template for the fiber's crystallization by oriented nucleation.
Bibliography:
Grenier C, Griesshaber E, Schmahl WW, Checa AG (2023) Microstructure and crystallographic characteristics of stenolaemate bryozoans (Phylum Bryozoa and Class Stenolaemata). Cryst Growth Des 23:965-979.
Grenier C, Griesshaber E, Schmahl WW, Berning B, Checa AG (2024) Skeletal microstructures of cheilostome bryozoans (phylum Bryozoa, class Gymnolaemata): crystallography and secretion patterns. Mar Life Sci Technol.
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