Glycine betaine modulates extracellular polymeric substances to enhance microbial salinity tolerance
High salinity inhibits microbial activity in the bioremediation of saline wastewater. To alleviate osmotic stress, glycine betaine (GB), an osmoprotectant, is added to enhance the secretion of extracellular polymeric substances (EPS). These EPS are pivotal in withstanding environmental stressors, ye...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2024-07-01
|
| Series: | Environmental Science and Ecotechnology |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2666498424000206 |
| _version_ | 1827163423039815680 |
|---|---|
| author | Yan Xia Xinbai Jiang Shuaishuai Guo Yuxuan Wang Yang Mu Jinyou Shen |
| author_facet | Yan Xia Xinbai Jiang Shuaishuai Guo Yuxuan Wang Yang Mu Jinyou Shen |
| author_sort | Yan Xia |
| collection | DOAJ |
| description | High salinity inhibits microbial activity in the bioremediation of saline wastewater. To alleviate osmotic stress, glycine betaine (GB), an osmoprotectant, is added to enhance the secretion of extracellular polymeric substances (EPS). These EPS are pivotal in withstanding environmental stressors, yet the intricate interplay between GB supplementation and microbial responses through EPS modifications—encompassing composition, molecular architecture, and electrochemical features—remains elusive in hypersaline conditions. Here we show microbial strategies for salinity endurance by investigating the impact of GB on the dynamic alterations of EPS properties. Our findings reveal that GB supplementation at 3.5% salinity elevates the total EPS (T-EPS) content from 12.50 ± 0.05 to 24.58 ± 0.96 mg per g dry cell weight. The observed shift in zeta potential from −28.95 to −6.25 mV at 0% and 3.5% salinity, respectively, with GB treatment, indicates a reduction in electrostatic repulsion and compaction. Notably, the EPS protein secondary structure transition from β-sheet to α-helix, with GB addition, signifies a more compact protein configuration, less susceptible to salinity fluctuations. Electrochemical analyses, including cyclic voltammetry (CV) and differential pulse voltammetry (DPV), reveal GB's role in promoting the release of exogenous electron shuttles, such as flavins and c-type cytochromes (c-Cyts). The enhancement in DPV peak areas (QDPV) with GB addition implies an increase in available extracellular electron transfer sites. This investigation advances our comprehension of microbial adaptation mechanisms to salinity through EPS modifications facilitated by GB in saline habitats. |
| first_indexed | 2024-04-24T20:24:58Z |
| format | Article |
| id | doaj.art-965fbf62756a48868d789bc3761d9432 |
| institution | Directory Open Access Journal |
| issn | 2666-4984 |
| language | English |
| last_indexed | 2025-03-21T01:00:28Z |
| publishDate | 2024-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Environmental Science and Ecotechnology |
| spelling | doaj.art-965fbf62756a48868d789bc3761d94322024-08-03T04:25:05ZengElsevierEnvironmental Science and Ecotechnology2666-49842024-07-0120100406Glycine betaine modulates extracellular polymeric substances to enhance microbial salinity toleranceYan Xia0Xinbai Jiang1Shuaishuai Guo2Yuxuan Wang3Yang Mu4Jinyou Shen5Key Laboratory of Environmental Remediation and Ecological Health, Ministry of Industry and Information Technology, School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing, 210094, ChinaKey Laboratory of Environmental Remediation and Ecological Health, Ministry of Industry and Information Technology, School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing, 210094, China; Corresponding author.Key Laboratory of Environmental Remediation and Ecological Health, Ministry of Industry and Information Technology, School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing, 210094, ChinaKey Laboratory of Environmental Remediation and Ecological Health, Ministry of Industry and Information Technology, School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing, 210094, ChinaCAS Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science & Technology of China, Hefei, 230026, ChinaKey Laboratory of Environmental Remediation and Ecological Health, Ministry of Industry and Information Technology, School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing, 210094, China; Corresponding author.High salinity inhibits microbial activity in the bioremediation of saline wastewater. To alleviate osmotic stress, glycine betaine (GB), an osmoprotectant, is added to enhance the secretion of extracellular polymeric substances (EPS). These EPS are pivotal in withstanding environmental stressors, yet the intricate interplay between GB supplementation and microbial responses through EPS modifications—encompassing composition, molecular architecture, and electrochemical features—remains elusive in hypersaline conditions. Here we show microbial strategies for salinity endurance by investigating the impact of GB on the dynamic alterations of EPS properties. Our findings reveal that GB supplementation at 3.5% salinity elevates the total EPS (T-EPS) content from 12.50 ± 0.05 to 24.58 ± 0.96 mg per g dry cell weight. The observed shift in zeta potential from −28.95 to −6.25 mV at 0% and 3.5% salinity, respectively, with GB treatment, indicates a reduction in electrostatic repulsion and compaction. Notably, the EPS protein secondary structure transition from β-sheet to α-helix, with GB addition, signifies a more compact protein configuration, less susceptible to salinity fluctuations. Electrochemical analyses, including cyclic voltammetry (CV) and differential pulse voltammetry (DPV), reveal GB's role in promoting the release of exogenous electron shuttles, such as flavins and c-type cytochromes (c-Cyts). The enhancement in DPV peak areas (QDPV) with GB addition implies an increase in available extracellular electron transfer sites. This investigation advances our comprehension of microbial adaptation mechanisms to salinity through EPS modifications facilitated by GB in saline habitats.http://www.sciencedirect.com/science/article/pii/S2666498424000206High salinityExtracellular polymeric substancesGlycine betaineProtein secondary structureExtracellular electron transfer |
| spellingShingle | Yan Xia Xinbai Jiang Shuaishuai Guo Yuxuan Wang Yang Mu Jinyou Shen Glycine betaine modulates extracellular polymeric substances to enhance microbial salinity tolerance Environmental Science and Ecotechnology High salinity Extracellular polymeric substances Glycine betaine Protein secondary structure Extracellular electron transfer |
| title | Glycine betaine modulates extracellular polymeric substances to enhance microbial salinity tolerance |
| title_full | Glycine betaine modulates extracellular polymeric substances to enhance microbial salinity tolerance |
| title_fullStr | Glycine betaine modulates extracellular polymeric substances to enhance microbial salinity tolerance |
| title_full_unstemmed | Glycine betaine modulates extracellular polymeric substances to enhance microbial salinity tolerance |
| title_short | Glycine betaine modulates extracellular polymeric substances to enhance microbial salinity tolerance |
| title_sort | glycine betaine modulates extracellular polymeric substances to enhance microbial salinity tolerance |
| topic | High salinity Extracellular polymeric substances Glycine betaine Protein secondary structure Extracellular electron transfer |
| url | http://www.sciencedirect.com/science/article/pii/S2666498424000206 |
| work_keys_str_mv | AT yanxia glycinebetainemodulatesextracellularpolymericsubstancestoenhancemicrobialsalinitytolerance AT xinbaijiang glycinebetainemodulatesextracellularpolymericsubstancestoenhancemicrobialsalinitytolerance AT shuaishuaiguo glycinebetainemodulatesextracellularpolymericsubstancestoenhancemicrobialsalinitytolerance AT yuxuanwang glycinebetainemodulatesextracellularpolymericsubstancestoenhancemicrobialsalinitytolerance AT yangmu glycinebetainemodulatesextracellularpolymericsubstancestoenhancemicrobialsalinitytolerance AT jinyoushen glycinebetainemodulatesextracellularpolymericsubstancestoenhancemicrobialsalinitytolerance |