Selective Adsorption of Amino Acids in Crystals of Monohydrocalcite Induced by the Facultative Anaerobic Enterobacter ludwigii SYB1

The morphology, crystal structure, and elemental composition of biominerals are commonly different from chemically synthesized minerals, but the reasons for these are not fully understood. A facultative anaerobic bacterium, Enterobacter ludwigii SYB1, is used in experiments to document the hydrochem...

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Main Authors: Yanyang Zhao, Zuozhen Han, Huaxiao Yan, Hui Zhao, Maurice E. Tucker, Xiao Gao, Na Guo, Ruirui Meng, Daniel Cosmos Owusu
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.696557/full
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author Yanyang Zhao
Yanyang Zhao
Zuozhen Han
Zuozhen Han
Huaxiao Yan
Hui Zhao
Maurice E. Tucker
Maurice E. Tucker
Xiao Gao
Na Guo
Ruirui Meng
Daniel Cosmos Owusu
author_facet Yanyang Zhao
Yanyang Zhao
Zuozhen Han
Zuozhen Han
Huaxiao Yan
Hui Zhao
Maurice E. Tucker
Maurice E. Tucker
Xiao Gao
Na Guo
Ruirui Meng
Daniel Cosmos Owusu
author_sort Yanyang Zhao
collection DOAJ
description The morphology, crystal structure, and elemental composition of biominerals are commonly different from chemically synthesized minerals, but the reasons for these are not fully understood. A facultative anaerobic bacterium, Enterobacter ludwigii SYB1, is used in experiments to document the hydrochemistry, mineral crystallization, and cell surface characteristics of biomineralization. It was found that carbonate anhydrase and ammonia production were major factors influencing the alkalinity and saturation of the closed biosystem. X-ray diffraction (XRD) spectra showed that calcite, monohydrocalcite (MHC), and dypingite formed in samples with bacterial cells. It was also found that the (222) plane of MHC was the preferred orientation compared to standard data. Scanning transmission electron microscopy (STEM) analysis of cell slices provides direct evidence of concentrated calcium and magnesium ions on the surface of extracellular polymeric substances (EPS). In addition, high-resolution transmission electron microscopy (HRTEM) showed that crystallized nanoparticles were formed within the EPS. Thus, the mechanism of the biomineralization induced by E. ludwigii SYB1 can be divided into three stages: (i) the production of carbonate anhydrase and ammonia increases the alkalinity and saturation state of the milieu, (ii) free calcium and magnesium ions are adsorbed and chelated onto EPS, and (iii) nanominerals crystallize and grow within the EPS. Seventeen kinds of amino acids were identified within both biotic MHC and the EPS of SYB1, while the percentages of glutamic and aspartic acid in MHC increased significantly (p < 0.05). Furthermore, the adsorption energy was calculated for various amino acids on seven diffracted crystal faces, with preferential adsorption demonstrated on (111) and (222) faces. At the same time, the lowest adsorption energy was always that of glutamic and aspartic acid for the same crystal plane. These results suggest that aspartic and glutamic acid always mix preferentially in the crystal lattice of MHC and that differential adsorption of amino acids on crystal planes can lead to their preferred orientation. Moreover, the mixing of amino acids in the mineral structure may also have a certain influence on the mineral lattice dislocations, thus enhancing the thermodynamic characteristics.
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spelling doaj.art-563cd9acba084923a11105272b86607e2022-12-21T22:27:17ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-07-011210.3389/fmicb.2021.696557696557Selective Adsorption of Amino Acids in Crystals of Monohydrocalcite Induced by the Facultative Anaerobic Enterobacter ludwigii SYB1Yanyang Zhao0Yanyang Zhao1Zuozhen Han2Zuozhen Han3Huaxiao Yan4Hui Zhao5Maurice E. Tucker6Maurice E. Tucker7Xiao Gao8Na Guo9Ruirui Meng10Daniel Cosmos Owusu11Shandong Provincial Key Laboratory of Depositional Mineralization and Sedimentary Minerals, College of Earth Science and Engineering, Shandong University of Science and Technology, Qingdao, ChinaLaboratory for Marine Mineral Resources, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaShandong Provincial Key Laboratory of Depositional Mineralization and Sedimentary Minerals, College of Earth Science and Engineering, Shandong University of Science and Technology, Qingdao, ChinaLaboratory for Marine Mineral Resources, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaDepartment of Bioengineering, College of Chemical and Biological Engineering, Shandong University of Science and Technology, Qingdao, ChinaDepartment of Bioengineering, College of Chemical and Biological Engineering, Shandong University of Science and Technology, Qingdao, ChinaSchool of Earth Sciences, University of Bristol, Bristol, United KingdomCabot Institute, University of Bristol, Bristol, United KingdomShandong Provincial Key Laboratory of Depositional Mineralization and Sedimentary Minerals, College of Earth Science and Engineering, Shandong University of Science and Technology, Qingdao, ChinaShandong Provincial Key Laboratory of Depositional Mineralization and Sedimentary Minerals, College of Earth Science and Engineering, Shandong University of Science and Technology, Qingdao, ChinaShandong Provincial Key Laboratory of Depositional Mineralization and Sedimentary Minerals, College of Earth Science and Engineering, Shandong University of Science and Technology, Qingdao, ChinaDepartment of Bioengineering, College of Chemical and Biological Engineering, Shandong University of Science and Technology, Qingdao, ChinaThe morphology, crystal structure, and elemental composition of biominerals are commonly different from chemically synthesized minerals, but the reasons for these are not fully understood. A facultative anaerobic bacterium, Enterobacter ludwigii SYB1, is used in experiments to document the hydrochemistry, mineral crystallization, and cell surface characteristics of biomineralization. It was found that carbonate anhydrase and ammonia production were major factors influencing the alkalinity and saturation of the closed biosystem. X-ray diffraction (XRD) spectra showed that calcite, monohydrocalcite (MHC), and dypingite formed in samples with bacterial cells. It was also found that the (222) plane of MHC was the preferred orientation compared to standard data. Scanning transmission electron microscopy (STEM) analysis of cell slices provides direct evidence of concentrated calcium and magnesium ions on the surface of extracellular polymeric substances (EPS). In addition, high-resolution transmission electron microscopy (HRTEM) showed that crystallized nanoparticles were formed within the EPS. Thus, the mechanism of the biomineralization induced by E. ludwigii SYB1 can be divided into three stages: (i) the production of carbonate anhydrase and ammonia increases the alkalinity and saturation state of the milieu, (ii) free calcium and magnesium ions are adsorbed and chelated onto EPS, and (iii) nanominerals crystallize and grow within the EPS. Seventeen kinds of amino acids were identified within both biotic MHC and the EPS of SYB1, while the percentages of glutamic and aspartic acid in MHC increased significantly (p < 0.05). Furthermore, the adsorption energy was calculated for various amino acids on seven diffracted crystal faces, with preferential adsorption demonstrated on (111) and (222) faces. At the same time, the lowest adsorption energy was always that of glutamic and aspartic acid for the same crystal plane. These results suggest that aspartic and glutamic acid always mix preferentially in the crystal lattice of MHC and that differential adsorption of amino acids on crystal planes can lead to their preferred orientation. Moreover, the mixing of amino acids in the mineral structure may also have a certain influence on the mineral lattice dislocations, thus enhancing the thermodynamic characteristics.https://www.frontiersin.org/articles/10.3389/fmicb.2021.696557/fullbiomineralizationamino acidsextracellular polymeric substancesmonohydrocalcitefacultative anaerobic bacteria
spellingShingle Yanyang Zhao
Yanyang Zhao
Zuozhen Han
Zuozhen Han
Huaxiao Yan
Hui Zhao
Maurice E. Tucker
Maurice E. Tucker
Xiao Gao
Na Guo
Ruirui Meng
Daniel Cosmos Owusu
Selective Adsorption of Amino Acids in Crystals of Monohydrocalcite Induced by the Facultative Anaerobic Enterobacter ludwigii SYB1
Frontiers in Microbiology
biomineralization
amino acids
extracellular polymeric substances
monohydrocalcite
facultative anaerobic bacteria
title Selective Adsorption of Amino Acids in Crystals of Monohydrocalcite Induced by the Facultative Anaerobic Enterobacter ludwigii SYB1
title_full Selective Adsorption of Amino Acids in Crystals of Monohydrocalcite Induced by the Facultative Anaerobic Enterobacter ludwigii SYB1
title_fullStr Selective Adsorption of Amino Acids in Crystals of Monohydrocalcite Induced by the Facultative Anaerobic Enterobacter ludwigii SYB1
title_full_unstemmed Selective Adsorption of Amino Acids in Crystals of Monohydrocalcite Induced by the Facultative Anaerobic Enterobacter ludwigii SYB1
title_short Selective Adsorption of Amino Acids in Crystals of Monohydrocalcite Induced by the Facultative Anaerobic Enterobacter ludwigii SYB1
title_sort selective adsorption of amino acids in crystals of monohydrocalcite induced by the facultative anaerobic enterobacter ludwigii syb1
topic biomineralization
amino acids
extracellular polymeric substances
monohydrocalcite
facultative anaerobic bacteria
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.696557/full
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