Salinity and hydraulic retention time induce membrane phospholipid acyl chain remodeling in Halanaerobium congolense WG10 and mixed cultures from hydraulically fractured shale wells
Bacteria remodel their plasma membrane lipidome to maintain key biophysical attributes in response to ecological disturbances. For Halanaerobium and other anaerobic halotolerant taxa that persist in hydraulically fractured deep subsurface shale reservoirs, salinity, and hydraulic retention time (HRT...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-11-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1023575/full |
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| author | Chika Jude Ugwuodo Chika Jude Ugwuodo Fabrizio Colosimo Jishnu Adhikari Yuxiang Shen Appala Raju Badireddy Paula J. Mouser |
| author_facet | Chika Jude Ugwuodo Chika Jude Ugwuodo Fabrizio Colosimo Jishnu Adhikari Yuxiang Shen Appala Raju Badireddy Paula J. Mouser |
| author_sort | Chika Jude Ugwuodo |
| collection | DOAJ |
| description | Bacteria remodel their plasma membrane lipidome to maintain key biophysical attributes in response to ecological disturbances. For Halanaerobium and other anaerobic halotolerant taxa that persist in hydraulically fractured deep subsurface shale reservoirs, salinity, and hydraulic retention time (HRT) are important perturbants of cell membrane structure, yet their effects remain poorly understood. Membrane-linked activities underlie in situ microbial growth kinetics and physiologies which drive biogeochemical reactions in engineered subsurface systems. Hence, we used gas chromatography–mass spectrometry (GC–MS) to investigate the effects of salinity and HRT on the phospholipid fatty acid composition of H. congolense WG10 and mixed enrichment cultures from hydraulically fractured shale wells. We also coupled acyl chain remodeling to membrane mechanics by measuring bilayer elasticity using atomic force microscopy (AFM). For these experiments, cultures were grown in a chemostat vessel operated in continuous flow mode under strict anoxia and constant stirring. Our findings show that salinity and HRT induce significant changes in membrane fatty acid chemistry of H. congolense WG10 in distinct and complementary ways. Notably, under nonoptimal salt concentrations (7% and 20% NaCl), H. congolense WG10 elevates the portion of polyunsaturated fatty acids (PUFAs) in its membrane, and this results in an apparent increase in fluidity (homeoviscous adaptation principle) and thickness. Double bond index (DBI) and mean chain length (MCL) were used as proxies for membrane fluidity and thickness, respectively. These results provide new insight into our understanding of how environmental and engineered factors might disrupt the physical and biogeochemical equilibria of fractured shale by inducing physiologically relevant changes in the membrane fatty acid chemistry of persistent microbial taxa.GRAPHICAL ABSTRACTSalinity significantly alters membrane bilayer fluidity and thickness in Halanaerobium congolense WG10. |
| first_indexed | 2024-04-11T17:33:05Z |
| format | Article |
| id | doaj.art-22a1f13a13e741e2a4cf1c2c5a7a3360 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-11T17:33:05Z |
| publishDate | 2022-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-22a1f13a13e741e2a4cf1c2c5a7a33602022-12-22T04:11:51ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-11-011310.3389/fmicb.2022.10235751023575Salinity and hydraulic retention time induce membrane phospholipid acyl chain remodeling in Halanaerobium congolense WG10 and mixed cultures from hydraulically fractured shale wellsChika Jude Ugwuodo0Chika Jude Ugwuodo1Fabrizio Colosimo2Jishnu Adhikari3Yuxiang Shen4Appala Raju Badireddy5Paula J. Mouser6Natural Resources and Earth Systems Science, University of New Hampshire, Durham, NH, United StatesDepartment of Civil and Environmental Engineering, University of New Hampshire, Durham, NH, United StatesNew England Biolabs, Ipswich, MA, United StatesSanborn, Head and Associates, Inc., Concord, NH, United StatesDepartment of Civil and Environmental Engineering, University of Vermont, Burlington, VT, United StatesDepartment of Civil and Environmental Engineering, University of Vermont, Burlington, VT, United StatesDepartment of Civil and Environmental Engineering, University of New Hampshire, Durham, NH, United StatesBacteria remodel their plasma membrane lipidome to maintain key biophysical attributes in response to ecological disturbances. For Halanaerobium and other anaerobic halotolerant taxa that persist in hydraulically fractured deep subsurface shale reservoirs, salinity, and hydraulic retention time (HRT) are important perturbants of cell membrane structure, yet their effects remain poorly understood. Membrane-linked activities underlie in situ microbial growth kinetics and physiologies which drive biogeochemical reactions in engineered subsurface systems. Hence, we used gas chromatography–mass spectrometry (GC–MS) to investigate the effects of salinity and HRT on the phospholipid fatty acid composition of H. congolense WG10 and mixed enrichment cultures from hydraulically fractured shale wells. We also coupled acyl chain remodeling to membrane mechanics by measuring bilayer elasticity using atomic force microscopy (AFM). For these experiments, cultures were grown in a chemostat vessel operated in continuous flow mode under strict anoxia and constant stirring. Our findings show that salinity and HRT induce significant changes in membrane fatty acid chemistry of H. congolense WG10 in distinct and complementary ways. Notably, under nonoptimal salt concentrations (7% and 20% NaCl), H. congolense WG10 elevates the portion of polyunsaturated fatty acids (PUFAs) in its membrane, and this results in an apparent increase in fluidity (homeoviscous adaptation principle) and thickness. Double bond index (DBI) and mean chain length (MCL) were used as proxies for membrane fluidity and thickness, respectively. These results provide new insight into our understanding of how environmental and engineered factors might disrupt the physical and biogeochemical equilibria of fractured shale by inducing physiologically relevant changes in the membrane fatty acid chemistry of persistent microbial taxa.GRAPHICAL ABSTRACTSalinity significantly alters membrane bilayer fluidity and thickness in Halanaerobium congolense WG10.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1023575/fullmembrane adaptationHalanaerobiumfractured shalelipidssalinityhydraulic retention time |
| spellingShingle | Chika Jude Ugwuodo Chika Jude Ugwuodo Fabrizio Colosimo Jishnu Adhikari Yuxiang Shen Appala Raju Badireddy Paula J. Mouser Salinity and hydraulic retention time induce membrane phospholipid acyl chain remodeling in Halanaerobium congolense WG10 and mixed cultures from hydraulically fractured shale wells Frontiers in Microbiology membrane adaptation Halanaerobium fractured shale lipids salinity hydraulic retention time |
| title | Salinity and hydraulic retention time induce membrane phospholipid acyl chain remodeling in Halanaerobium congolense WG10 and mixed cultures from hydraulically fractured shale wells |
| title_full | Salinity and hydraulic retention time induce membrane phospholipid acyl chain remodeling in Halanaerobium congolense WG10 and mixed cultures from hydraulically fractured shale wells |
| title_fullStr | Salinity and hydraulic retention time induce membrane phospholipid acyl chain remodeling in Halanaerobium congolense WG10 and mixed cultures from hydraulically fractured shale wells |
| title_full_unstemmed | Salinity and hydraulic retention time induce membrane phospholipid acyl chain remodeling in Halanaerobium congolense WG10 and mixed cultures from hydraulically fractured shale wells |
| title_short | Salinity and hydraulic retention time induce membrane phospholipid acyl chain remodeling in Halanaerobium congolense WG10 and mixed cultures from hydraulically fractured shale wells |
| title_sort | salinity and hydraulic retention time induce membrane phospholipid acyl chain remodeling in halanaerobium congolense wg10 and mixed cultures from hydraulically fractured shale wells |
| topic | membrane adaptation Halanaerobium fractured shale lipids salinity hydraulic retention time |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1023575/full |
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