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Adaptive Strategies in a Poly-Extreme Environment: Differentiation of Vegetative Cells in Serratia ureilytica and Resistance to Extreme Conditions

Poly-extreme terrestrial habitats are often used as analogs to extra-terrestrial environments. Understanding the adaptive strategies allowing bacteria to thrive and survive under these conditions could help in our quest for extra-terrestrial planets suitable for life and understanding how life evolv...

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Autores principales: Filippidou, Sevasti, Junier, Thomas, Wunderlin, Tina, Kooli, Wafa M., Palmieri, Ilona, Al-Dourobi, Andrej, Molina, Veronica, Lienhard, Reto, Spangenberg, Jorge E., Johnson, Shannon L., Chain, Patrick S. G., Dorador, Cristina, Junier, Pilar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6370625/
https://www.ncbi.nlm.nih.gov/pubmed/30804904
http://dx.doi.org/10.3389/fmicb.2019.00102
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author Filippidou, Sevasti
Junier, Thomas
Wunderlin, Tina
Kooli, Wafa M.
Palmieri, Ilona
Al-Dourobi, Andrej
Molina, Veronica
Lienhard, Reto
Spangenberg, Jorge E.
Johnson, Shannon L.
Chain, Patrick S. G.
Dorador, Cristina
Junier, Pilar
author_facet Filippidou, Sevasti
Junier, Thomas
Wunderlin, Tina
Kooli, Wafa M.
Palmieri, Ilona
Al-Dourobi, Andrej
Molina, Veronica
Lienhard, Reto
Spangenberg, Jorge E.
Johnson, Shannon L.
Chain, Patrick S. G.
Dorador, Cristina
Junier, Pilar
author_sort Filippidou, Sevasti
collection PubMed
description Poly-extreme terrestrial habitats are often used as analogs to extra-terrestrial environments. Understanding the adaptive strategies allowing bacteria to thrive and survive under these conditions could help in our quest for extra-terrestrial planets suitable for life and understanding how life evolved in the harsh early earth conditions. A prime example of such a survival strategy is the modification of vegetative cells into resistant resting structures. These differentiated cells are often observed in response to harsh environmental conditions. The environmental strain (strain Lr5/4) belonging to Serratia ureilytica was isolated from a geothermal spring in Lirima, Atacama Desert, Chile. The Atacama Desert is the driest habitat on Earth and furthermore, due to its high altitude, it is exposed to an increased amount of UV radiation. The geothermal spring from which the strain was isolated is oligotrophic and the temperature of 54°C exceeds mesophilic conditions (15 to 45°C). Although the vegetative cells were tolerant to various environmental insults (desiccation, extreme pH, glycerol), a modified cell type was formed in response to nutrient deprivation, UV radiation and thermal shock. Scanning (SEM) and Transmission Electron Microscopy (TEM) analyses of vegetative cells and the modified cell structures were performed. In SEM, a change toward a circular shape with reduced size was observed. These circular cells possessed what appears as extra coating layers under TEM. The resistance of the modified cells was also investigated, they were resistant to wet heat, UV radiation and desiccation, while vegetative cells did not withstand any of those conditions. A phylogenomic analysis was undertaken to investigate the presence of known genes involved in dormancy in other bacterial clades. Genes related to spore-formation in Myxococcus and Firmicutes were found in S. ureilytica Lr5/4 genome; however, these genes were not enough for a full sporulation pathway that resembles either group. Although, the molecular pathway of cell differentiation in S. ureilytica Lr5/4 is not fully defined, the identified genes may contribute to the modified phenotype in the Serratia genus. Here, we show that a modified cell structure can occur as a response to extremity in a species that was previously not known to deploy this strategy. This strategy may be widely spread in bacteria, but only expressed under poly-extreme environmental conditions.
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spelling pubmed-63706252019-02-25 Adaptive Strategies in a Poly-Extreme Environment: Differentiation of Vegetative Cells in Serratia ureilytica and Resistance to Extreme Conditions Filippidou, Sevasti Junier, Thomas Wunderlin, Tina Kooli, Wafa M. Palmieri, Ilona Al-Dourobi, Andrej Molina, Veronica Lienhard, Reto Spangenberg, Jorge E. Johnson, Shannon L. Chain, Patrick S. G. Dorador, Cristina Junier, Pilar Front Microbiol Microbiology Poly-extreme terrestrial habitats are often used as analogs to extra-terrestrial environments. Understanding the adaptive strategies allowing bacteria to thrive and survive under these conditions could help in our quest for extra-terrestrial planets suitable for life and understanding how life evolved in the harsh early earth conditions. A prime example of such a survival strategy is the modification of vegetative cells into resistant resting structures. These differentiated cells are often observed in response to harsh environmental conditions. The environmental strain (strain Lr5/4) belonging to Serratia ureilytica was isolated from a geothermal spring in Lirima, Atacama Desert, Chile. The Atacama Desert is the driest habitat on Earth and furthermore, due to its high altitude, it is exposed to an increased amount of UV radiation. The geothermal spring from which the strain was isolated is oligotrophic and the temperature of 54°C exceeds mesophilic conditions (15 to 45°C). Although the vegetative cells were tolerant to various environmental insults (desiccation, extreme pH, glycerol), a modified cell type was formed in response to nutrient deprivation, UV radiation and thermal shock. Scanning (SEM) and Transmission Electron Microscopy (TEM) analyses of vegetative cells and the modified cell structures were performed. In SEM, a change toward a circular shape with reduced size was observed. These circular cells possessed what appears as extra coating layers under TEM. The resistance of the modified cells was also investigated, they were resistant to wet heat, UV radiation and desiccation, while vegetative cells did not withstand any of those conditions. A phylogenomic analysis was undertaken to investigate the presence of known genes involved in dormancy in other bacterial clades. Genes related to spore-formation in Myxococcus and Firmicutes were found in S. ureilytica Lr5/4 genome; however, these genes were not enough for a full sporulation pathway that resembles either group. Although, the molecular pathway of cell differentiation in S. ureilytica Lr5/4 is not fully defined, the identified genes may contribute to the modified phenotype in the Serratia genus. Here, we show that a modified cell structure can occur as a response to extremity in a species that was previously not known to deploy this strategy. This strategy may be widely spread in bacteria, but only expressed under poly-extreme environmental conditions. Frontiers Media S.A. 2019-02-05 /pmc/articles/PMC6370625/ /pubmed/30804904 http://dx.doi.org/10.3389/fmicb.2019.00102 Text en Copyright © 2019 Filippidou, Junier, Wunderlin, Kooli, Palmieri, Al-Dourobi, Molina, Lienhard, Spangenberg, Johnson, Chain, Dorador and Junier. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Filippidou, Sevasti
Junier, Thomas
Wunderlin, Tina
Kooli, Wafa M.
Palmieri, Ilona
Al-Dourobi, Andrej
Molina, Veronica
Lienhard, Reto
Spangenberg, Jorge E.
Johnson, Shannon L.
Chain, Patrick S. G.
Dorador, Cristina
Junier, Pilar
Adaptive Strategies in a Poly-Extreme Environment: Differentiation of Vegetative Cells in Serratia ureilytica and Resistance to Extreme Conditions
title Adaptive Strategies in a Poly-Extreme Environment: Differentiation of Vegetative Cells in Serratia ureilytica and Resistance to Extreme Conditions
title_full Adaptive Strategies in a Poly-Extreme Environment: Differentiation of Vegetative Cells in Serratia ureilytica and Resistance to Extreme Conditions
title_fullStr Adaptive Strategies in a Poly-Extreme Environment: Differentiation of Vegetative Cells in Serratia ureilytica and Resistance to Extreme Conditions
title_full_unstemmed Adaptive Strategies in a Poly-Extreme Environment: Differentiation of Vegetative Cells in Serratia ureilytica and Resistance to Extreme Conditions
title_short Adaptive Strategies in a Poly-Extreme Environment: Differentiation of Vegetative Cells in Serratia ureilytica and Resistance to Extreme Conditions
title_sort adaptive strategies in a poly-extreme environment: differentiation of vegetative cells in serratia ureilytica and resistance to extreme conditions
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6370625/
https://www.ncbi.nlm.nih.gov/pubmed/30804904
http://dx.doi.org/10.3389/fmicb.2019.00102
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