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The biomechanical role of overall-shape transformation in a primitive multicellular organism: A case study of dimorphism in the filamentous cyanobacterium Arthrospira platensis.

ABSTRACT: Morphological transformations in primitive organisms have long been observed; however, its biomechanical roles are largely unexplored. In this study, we investigate the structural advantages of dimorphism in Arthrospira platensis, a filamentous multicellular cyanobacterium. We report that helical trichomes, the default shape, have a higher persistence length (Lp), indicating a higher resistance to bending or a large value of flexural rigidity (kf), the product of the local cell stiffness (E) and the moment of inertia of the trichomes' cross-section (I). Through Atomic Force Microscopy (AFM), we determined that the E of straight and helical trichomes were the same. In contrast, our computational model shows that I is greatly dependent on helical radii, implying that trichome morphology is the major contributor to kf variation. According to our estimation, increasing the helical radii alone can increase kf by 2 orders of magnitude. We also observe that straight trichomes have improved gliding ability, due to its structure and lower kf. Our study shows that dimorphism provides mechanical adjustability to the organism and may allow it to thrive in different environmental conditions. The higher kf provides helical trichomes a better nutrient uptake through advection in aquatic environments. On the other hand, the lower kf improves the gliding ability of straight trichomes in aquatic environments, enabling it to chemotactically relocate to more favorable territories when it encounters certain environmental stresses. When more optimal conditions are encountered, straight trichomes can revert to their original helical form. Our study is one of the first to highlight the biomechanical role of an overall-shape transformation in cyanobacteria.

SUBMITTER: Chaiyasitdhi A

PROVIDER: S-EPMC5945045 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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The biomechanical role of overall-shape transformation in a primitive multicellular organism: A case study of dimorphism in the filamentous cyanobacterium Arthrospira platensis.

Chaiyasitdhi Atitheb A Miphonpanyatawichok Wirat W Riehle Mathis Oliver MO Phatthanakun Rungrueang R Surareungchai Werasak W Kundhikanjana Worasom W Kuntanawat Panwong P

PloS one 20180510 5

Morphological transformations in primitive organisms have long been observed; however, its biomechanical roles are largely unexplored. In this study, we investigate the structural advantages of dimorphism in Arthrospira platensis, a filamentous multicellular cyanobacterium. We report that helical trichomes, the default shape, have a higher persistence length (Lp), indicating a higher resistance to bending or a large value of flexural rigidity (kf), the product of the local cell stiffness (E) and ...[more]

PMID: 29746494

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Project description:Background:The extensive usage of zinc oxide nanoparticles (ZnO NPs) in industrial and consumer products raises the risk of releasing their residues into the aquatic environment. The presence of ZnO NPs in the aquatic environment could potentially cause cytotoxic effects on aquatic organisms. Thus, investigating the cytotoxic effects of ZnO NPs on microalgae, which form the base for the food web of aquatic biota, is essential to gain information regarding the ecotoxicological effects of metallic oxide nanoparticles in the aquatic ecosystem. Therefore, the present study has investigated in detail the assorted cytotoxic effects of ZnO NPs on S. platensis using various concentrations of ZnO NPs (10-200 mg/L) from 6 to 96 h to explore the dose- and time-dependent cytotoxic effects. Methods:The cytotoxic effects were all assessed through quantification of loss in cell viability, reduction in biomass and decrease in photosynthetic pigments such as chlorophyll-a, carotenoids and phycocyanin. The surface interactions of nanoparticles and the subsequent morphological alterations on algal cells were examined by optical and scanning electron microscopy (SEM). The intracellular alterations of algal cells were studied using transmission electron microscopy. Furthermore, Fourier transformed infrared (FTIR) spectrum was obtained to investigate the involvement of algal surface biomolecules in surface binding of ZnO NPs on algal cells. Results:The treatment of ZnO NPs on S. platensis exhibited a typical concentration- and time-dependent cytotoxicity. Results showed a significant (p < 0.05) cytotoxicity from 24 h onwards for all tested concentrations of ZnO NPs. The maximum cytotoxicity on algal cells was achieved at 96 h of exposure to ZnO NPs. In comparison with control, the algal cells that interacted with 200 mg/L of ZnO NPs for 96 h showed 87.3 ± 1% loss in cell viability, 76.1 ± 1.7% reduction in algal biomass, 92.5 ± 2.2%, 76.2 ± 2.2% and 74.1 ± 3.4% decrease in chlorophyll-a, carotenoids and phycocyanin contents respectively. Our study confirmed the cytotoxicity of ZnO NPs through the algal growth inhibition with 72 h EC10 and EC50 values of 1.29 and 31.56 mg/L, respectively. The microscopic examinations of the algal cells that interacted with ZnO NPs showed severe cell membrane and intracellular damage. The SEM EDX spectrum of ZnO NPs treated algal biomass evidenced the surface accumulation of zinc in the biomass. Finally, the FTIR spectrum confirmed the involvement of amino, hydroxyl and carboxylic groups of algal cell wall in the surface interaction of ZnO NPs on the algal cells. Discussion:The results showed that the treatment of ZnO NPs on S. platensis triggered substantial cytotoxicity and caused cell death. Hence, S. platensis could be potentially used as a bioindicator for testing toxicity of ZnO NPs in aquatic environment.

Dataset Information

The biomechanical role of overall-shape transformation in a primitive multicellular organism: A case study of dimorphism in the filamentous cyanobacterium Arthrospira platensis.

Publications

The biomechanical role of overall-shape transformation in a primitive multicellular organism: A case study of dimorphism in the filamentous cyanobacterium Arthrospira platensis.

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