Novel Mechanism for Surface Layer Shedding and Regenerating in Bacteria Exposed to Metal-Contaminated Conditions
Surface layers (S-layers) are components of the cell walls throughout the Bacteria and the Archaea that provide protection for microorganisms against diverse environmental stresses, including metal stress. We have previously characterized the process by which S-layers serve as a nucleation site for...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2018.03210/full |
| _version_ | 1818287410631409664 |
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| author | Archjana Chandramohan Elodie Duprat Laurent Remusat Severine Zirah Carine Lombard Adrienne Kish |
| author_facet | Archjana Chandramohan Elodie Duprat Laurent Remusat Severine Zirah Carine Lombard Adrienne Kish |
| author_sort | Archjana Chandramohan |
| collection | DOAJ |
| description | Surface layers (S-layers) are components of the cell walls throughout the Bacteria and the Archaea that provide protection for microorganisms against diverse environmental stresses, including metal stress. We have previously characterized the process by which S-layers serve as a nucleation site for metal mineralization in an archaeon for which the S-layer represents the only cell wall component. Here, we test the hypothesis originally proposed in cyanobacteria that a “shedding” mechanism exists for replacing S-layers that have become mineral-encrusted, using Lysinibacillus sp. TchIII 20n38, metallotolerant gram-positive bacterium, as a model organism. We characterize for the first time a mechanism for resistance to metals through S-layer shedding and regeneration. S-layers nucleate the formation of Fe-mineral on the cell surface, depending on physiological state of the cells and metal exposure times, leading to the encrustation of the S-layer and changes in the cell morphology as observed by scanning electron microscopy. Using Nanoscale Secondary Ion Mass Spectrometry, we show that mineral-encrusted S-layers are shed by the bacterial cells after a period of latency (2 days under the conditions tested) in a heterogeneous fashion likely reflecting natural variations in metal stress resistance. The emerging cells regenerate new S-layers as part of their cell wall structure. Given the wide diversity of S-layer bearing prokaryotes, S-layer shedding may represent an important mechanism for microbial survival in metal-contaminated environments. |
| first_indexed | 2024-12-13T01:40:03Z |
| format | Article |
| id | doaj.art-837d6168df58484aa3b1a50e95ed1f28 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-13T01:40:03Z |
| publishDate | 2019-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-837d6168df58484aa3b1a50e95ed1f282022-12-22T00:03:46ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-01-01910.3389/fmicb.2018.03210424721Novel Mechanism for Surface Layer Shedding and Regenerating in Bacteria Exposed to Metal-Contaminated ConditionsArchjana Chandramohan0Elodie Duprat1Laurent Remusat2Severine Zirah3Carine Lombard4Adrienne Kish5Unité Molécules de Communication et Adaptation des Microorganismes (MCAM), Muséum National d’Histoire Naturelle, CNRS UMR 7245, Paris, FranceInstitut de Minéralogie, Physique des Matériaux et de Cosmochimie (IMPMC), Sorbonne Université, Muséum National d’Histoire Naturelle, CNRS UMR 7590, IRD UMR 206, Paris, FranceInstitut de Minéralogie, Physique des Matériaux et de Cosmochimie (IMPMC), Sorbonne Université, Muséum National d’Histoire Naturelle, CNRS UMR 7590, IRD UMR 206, Paris, FranceUnité Molécules de Communication et Adaptation des Microorganismes (MCAM), Muséum National d’Histoire Naturelle, CNRS UMR 7245, Paris, FranceUnité Molécules de Communication et Adaptation des Microorganismes (MCAM), Muséum National d’Histoire Naturelle, CNRS UMR 7245, Paris, FranceUnité Molécules de Communication et Adaptation des Microorganismes (MCAM), Muséum National d’Histoire Naturelle, CNRS UMR 7245, Paris, FranceSurface layers (S-layers) are components of the cell walls throughout the Bacteria and the Archaea that provide protection for microorganisms against diverse environmental stresses, including metal stress. We have previously characterized the process by which S-layers serve as a nucleation site for metal mineralization in an archaeon for which the S-layer represents the only cell wall component. Here, we test the hypothesis originally proposed in cyanobacteria that a “shedding” mechanism exists for replacing S-layers that have become mineral-encrusted, using Lysinibacillus sp. TchIII 20n38, metallotolerant gram-positive bacterium, as a model organism. We characterize for the first time a mechanism for resistance to metals through S-layer shedding and regeneration. S-layers nucleate the formation of Fe-mineral on the cell surface, depending on physiological state of the cells and metal exposure times, leading to the encrustation of the S-layer and changes in the cell morphology as observed by scanning electron microscopy. Using Nanoscale Secondary Ion Mass Spectrometry, we show that mineral-encrusted S-layers are shed by the bacterial cells after a period of latency (2 days under the conditions tested) in a heterogeneous fashion likely reflecting natural variations in metal stress resistance. The emerging cells regenerate new S-layers as part of their cell wall structure. Given the wide diversity of S-layer bearing prokaryotes, S-layer shedding may represent an important mechanism for microbial survival in metal-contaminated environments.https://www.frontiersin.org/article/10.3389/fmicb.2018.03210/fullS-layermetalbiomineralizationmetallotoleranceLysinibacillus |
| spellingShingle | Archjana Chandramohan Elodie Duprat Laurent Remusat Severine Zirah Carine Lombard Adrienne Kish Novel Mechanism for Surface Layer Shedding and Regenerating in Bacteria Exposed to Metal-Contaminated Conditions Frontiers in Microbiology S-layer metal biomineralization metallotolerance Lysinibacillus |
| title | Novel Mechanism for Surface Layer Shedding and Regenerating in Bacteria Exposed to Metal-Contaminated Conditions |
| title_full | Novel Mechanism for Surface Layer Shedding and Regenerating in Bacteria Exposed to Metal-Contaminated Conditions |
| title_fullStr | Novel Mechanism for Surface Layer Shedding and Regenerating in Bacteria Exposed to Metal-Contaminated Conditions |
| title_full_unstemmed | Novel Mechanism for Surface Layer Shedding and Regenerating in Bacteria Exposed to Metal-Contaminated Conditions |
| title_short | Novel Mechanism for Surface Layer Shedding and Regenerating in Bacteria Exposed to Metal-Contaminated Conditions |
| title_sort | novel mechanism for surface layer shedding and regenerating in bacteria exposed to metal contaminated conditions |
| topic | S-layer metal biomineralization metallotolerance Lysinibacillus |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2018.03210/full |
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