Cargando…

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

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 tr...

Descripción completa

Detalles Bibliográficos
Autores principales: Chaiyasitdhi, Atitheb, Miphonpanyatawichok, Wirat, Riehle, Mathis Oliver, Phatthanakun, Rungrueang, Surareungchai, Werasak, Kundhikanjana, Worasom, Kuntanawat, Panwong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5945045/
https://www.ncbi.nlm.nih.gov/pubmed/29746494
http://dx.doi.org/10.1371/journal.pone.0196383
_version_ 1783321933579812864
author Chaiyasitdhi, Atitheb
Miphonpanyatawichok, Wirat
Riehle, Mathis Oliver
Phatthanakun, Rungrueang
Surareungchai, Werasak
Kundhikanjana, Worasom
Kuntanawat, Panwong
author_facet Chaiyasitdhi, Atitheb
Miphonpanyatawichok, Wirat
Riehle, Mathis Oliver
Phatthanakun, Rungrueang
Surareungchai, Werasak
Kundhikanjana, Worasom
Kuntanawat, Panwong
author_sort Chaiyasitdhi, Atitheb
collection PubMed
description 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 (L(p)), indicating a higher resistance to bending or a large value of flexural rigidity (k(f)), 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 k(f) variation. According to our estimation, increasing the helical radii alone can increase k(f) by 2 orders of magnitude. We also observe that straight trichomes have improved gliding ability, due to its structure and lower k(f). Our study shows that dimorphism provides mechanical adjustability to the organism and may allow it to thrive in different environmental conditions. The higher k(f) provides helical trichomes a better nutrient uptake through advection in aquatic environments. On the other hand, the lower k(f) 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.
format Online
Article
Text
id pubmed-5945045
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-59450452018-05-25 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 Miphonpanyatawichok, Wirat Riehle, Mathis Oliver Phatthanakun, Rungrueang Surareungchai, Werasak Kundhikanjana, Worasom Kuntanawat, Panwong PLoS One Research Article 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 (L(p)), indicating a higher resistance to bending or a large value of flexural rigidity (k(f)), 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 k(f) variation. According to our estimation, increasing the helical radii alone can increase k(f) by 2 orders of magnitude. We also observe that straight trichomes have improved gliding ability, due to its structure and lower k(f). Our study shows that dimorphism provides mechanical adjustability to the organism and may allow it to thrive in different environmental conditions. The higher k(f) provides helical trichomes a better nutrient uptake through advection in aquatic environments. On the other hand, the lower k(f) 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. Public Library of Science 2018-05-10 /pmc/articles/PMC5945045/ /pubmed/29746494 http://dx.doi.org/10.1371/journal.pone.0196383 Text en © 2018 Chaiyasitdhi et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Chaiyasitdhi, Atitheb
Miphonpanyatawichok, Wirat
Riehle, Mathis Oliver
Phatthanakun, Rungrueang
Surareungchai, Werasak
Kundhikanjana, Worasom
Kuntanawat, Panwong
The biomechanical role of overall-shape transformation in a primitive multicellular organism: A case study of dimorphism in the filamentous cyanobacterium Arthrospira platensis
title The biomechanical role of overall-shape transformation in a primitive multicellular organism: A case study of dimorphism in the filamentous cyanobacterium Arthrospira platensis
title_full The biomechanical role of overall-shape transformation in a primitive multicellular organism: A case study of dimorphism in the filamentous cyanobacterium Arthrospira platensis
title_fullStr The biomechanical role of overall-shape transformation in a primitive multicellular organism: A case study of dimorphism in the filamentous cyanobacterium Arthrospira platensis
title_full_unstemmed The biomechanical role of overall-shape transformation in a primitive multicellular organism: A case study of dimorphism in the filamentous cyanobacterium Arthrospira platensis
title_short The biomechanical role of overall-shape transformation in a primitive multicellular organism: A case study of dimorphism in the filamentous cyanobacterium Arthrospira platensis
title_sort biomechanical role of overall-shape transformation in a primitive multicellular organism: a case study of dimorphism in the filamentous cyanobacterium arthrospira platensis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5945045/
https://www.ncbi.nlm.nih.gov/pubmed/29746494
http://dx.doi.org/10.1371/journal.pone.0196383
work_keys_str_mv AT chaiyasitdhiatitheb thebiomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT miphonpanyatawichokwirat thebiomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT riehlemathisoliver thebiomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT phatthanakunrungrueang thebiomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT surareungchaiwerasak thebiomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT kundhikanjanaworasom thebiomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT kuntanawatpanwong thebiomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT chaiyasitdhiatitheb biomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT miphonpanyatawichokwirat biomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT riehlemathisoliver biomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT phatthanakunrungrueang biomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT surareungchaiwerasak biomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT kundhikanjanaworasom biomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis
AT kuntanawatpanwong biomechanicalroleofoverallshapetransformationinaprimitivemulticellularorganismacasestudyofdimorphisminthefilamentouscyanobacteriumarthrospiraplatensis