Mechanism for microbial population collapse in a fluctuating resource environment
Abstract Managing trade‐offs through gene regulation is believed to confer resilience to a microbial community in a fluctuating resource environment. To investigate this hypothesis, we imposed a fluctuating environment that required the sulfate‐reducer Desulfovibrio vulgaris to undergo repeated ecol...
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| Format: | Article |
| Language: | English |
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Springer Nature
2017-03-01
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| Series: | Molecular Systems Biology |
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| Online Access: | https://doi.org/10.15252/msb.20167058 |
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| author | Serdar Turkarslan Arjun V Raman Anne W Thompson Christina E Arens Mark A Gillespie Frederick von Netzer Kristina L Hillesland Sergey Stolyar Adrian López García de Lomana David J Reiss Drew Gorman‐Lewis Grant M Zane Jeffrey A Ranish Judy D Wall David A Stahl Nitin S Baliga |
| author_facet | Serdar Turkarslan Arjun V Raman Anne W Thompson Christina E Arens Mark A Gillespie Frederick von Netzer Kristina L Hillesland Sergey Stolyar Adrian López García de Lomana David J Reiss Drew Gorman‐Lewis Grant M Zane Jeffrey A Ranish Judy D Wall David A Stahl Nitin S Baliga |
| author_sort | Serdar Turkarslan |
| collection | DOAJ |
| description | Abstract Managing trade‐offs through gene regulation is believed to confer resilience to a microbial community in a fluctuating resource environment. To investigate this hypothesis, we imposed a fluctuating environment that required the sulfate‐reducer Desulfovibrio vulgaris to undergo repeated ecologically relevant shifts between retaining metabolic independence (active capacity for sulfate respiration) and becoming metabolically specialized to a mutualistic association with the hydrogen‐consuming Methanococcus maripaludis. Strikingly, the microbial community became progressively less proficient at restoring the environmentally relevant physiological state after each perturbation and most cultures collapsed within 3–7 shifts. Counterintuitively, the collapse phenomenon was prevented by a single regulatory mutation. We have characterized the mechanism for collapse by conducting RNA‐seq analysis, proteomics, microcalorimetry, and single‐cell transcriptome analysis. We demonstrate that the collapse was caused by conditional gene regulation, which drove precipitous decline in intracellular abundance of essential transcripts and proteins, imposing greater energetic burden of regulation to restore function in a fluctuating environment. |
| format | Article |
| id | doaj-art-a655ac4e70d1467cac12e10d18846903 |
| institution | Kabale University |
| issn | 1744-4292 |
| language | English |
| publishDate | 2017-03-01 |
| publisher | Springer Nature |
| record_format | Article |
| series | Molecular Systems Biology |
| spelling | doaj-art-a655ac4e70d1467cac12e10d188469032025-01-12T12:45:34ZengSpringer NatureMolecular Systems Biology1744-42922017-03-0113311610.15252/msb.20167058Mechanism for microbial population collapse in a fluctuating resource environmentSerdar Turkarslan0Arjun V Raman1Anne W Thompson2Christina E Arens3Mark A Gillespie4Frederick von Netzer5Kristina L Hillesland6Sergey Stolyar7Adrian López García de Lomana8David J Reiss9Drew Gorman‐Lewis10Grant M Zane11Jeffrey A Ranish12Judy D Wall13David A Stahl14Nitin S Baliga15Institute for Systems BiologyInstitute for Systems BiologyInstitute for Systems BiologyInstitute for Systems BiologyInstitute for Systems BiologyCivil and Environmental Engineering, University of WashingtonBiological Sciences, University of Washington BothellInstitute for Systems BiologyInstitute for Systems BiologyInstitute for Systems BiologyEarth and Space Sciences, University of WashingtonDepartment of Biochemistry, University of MissouriInstitute for Systems BiologyDepartment of Biochemistry, University of MissouriCivil and Environmental Engineering, University of WashingtonInstitute for Systems BiologyAbstract Managing trade‐offs through gene regulation is believed to confer resilience to a microbial community in a fluctuating resource environment. To investigate this hypothesis, we imposed a fluctuating environment that required the sulfate‐reducer Desulfovibrio vulgaris to undergo repeated ecologically relevant shifts between retaining metabolic independence (active capacity for sulfate respiration) and becoming metabolically specialized to a mutualistic association with the hydrogen‐consuming Methanococcus maripaludis. Strikingly, the microbial community became progressively less proficient at restoring the environmentally relevant physiological state after each perturbation and most cultures collapsed within 3–7 shifts. Counterintuitively, the collapse phenomenon was prevented by a single regulatory mutation. We have characterized the mechanism for collapse by conducting RNA‐seq analysis, proteomics, microcalorimetry, and single‐cell transcriptome analysis. We demonstrate that the collapse was caused by conditional gene regulation, which drove precipitous decline in intracellular abundance of essential transcripts and proteins, imposing greater energetic burden of regulation to restore function in a fluctuating environment.https://doi.org/10.15252/msb.20167058fluctuating resource environmentmicrobial population collapseregulationresiliencesyntrophy |
| spellingShingle | Serdar Turkarslan Arjun V Raman Anne W Thompson Christina E Arens Mark A Gillespie Frederick von Netzer Kristina L Hillesland Sergey Stolyar Adrian López García de Lomana David J Reiss Drew Gorman‐Lewis Grant M Zane Jeffrey A Ranish Judy D Wall David A Stahl Nitin S Baliga Mechanism for microbial population collapse in a fluctuating resource environment Molecular Systems Biology fluctuating resource environment microbial population collapse regulation resilience syntrophy |
| title | Mechanism for microbial population collapse in a fluctuating resource environment |
| title_full | Mechanism for microbial population collapse in a fluctuating resource environment |
| title_fullStr | Mechanism for microbial population collapse in a fluctuating resource environment |
| title_full_unstemmed | Mechanism for microbial population collapse in a fluctuating resource environment |
| title_short | Mechanism for microbial population collapse in a fluctuating resource environment |
| title_sort | mechanism for microbial population collapse in a fluctuating resource environment |
| topic | fluctuating resource environment microbial population collapse regulation resilience syntrophy |
| url | https://doi.org/10.15252/msb.20167058 |
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