Graphical abstract
Keywords
How to Cite
Abstract
Background: Hypersaline wastewater poses significant environmental challenges, necessitating efficient bioremediation strategies. This study investigates the hypersaline tolerance mechanisms of Pseudomonas stutzeri YXH-102, a heterotrophic nitrifying/aerobic denitrifying bacterium isolated from Yuncheng Salt Lake sediments, under high-salinity stress.
Results: Comparative transcriptomic analysis revealed 268 differentially expressed genes (DEGs) in response to a 10 % NaCl shock, with 86 upregulated and 182 downregulated. Key findings highlight the critical roles of oxidative stress mitigation, energy metabolism adaptation, and ion homeostasis. Salt stress triggered reactive oxygen species (ROS) accumulation, countered by upregulated cytochrome c oxidase (reducing ROS generation) and glutathione S-transferase (enhancing ROS scavenging). Concurrently, energy metabolism pathways, including fatty acid β-oxidation and acetyl-CoA production, were activated to sustain cellular energy demand. Notably, the electron transport chain (ETC) generated a robust proton motive force (PMF), which directly fueled potassium uptake via H+/K+ symporters to counteract osmotic imbalance. TonB-dependent transporters for nutrient uptake were also significantly upregulated, suggesting enhanced nutrient acquisition under salinity.
Conclusions: These findings elucidate how P. stutzeri YXH-102 combats salt stress through integrated ROS detoxification, energy optimization, and PMF-driven ion transport, providing molecular insights for its application in hypersaline wastewater bioremediation.
References
Srivastava A, Parida VK, Majumder A, et al. Treatment of saline wastewater using physicochemical, biological, and hybrid processes: Insights into inhibition mechanisms, treatment efficiencies and performance enhancement. J Environ Chem Eng, 2021;9(4):105775. https://doi.org/10.1016/j.jece.2021.105775
Shah A, Arjunan A, Baroutaji A, et al. A review of physicochemical and biological contaminants in drinking water and their impacts on human health. Water Sci Eng, 2023;16(4):333-344. https://doi.org/10.1016/j.wse.2023.04.003
Babuji P, Thirumalaisamy S, Duraisamy K, et al. Human health risks due to exposure to water pollution: A review. Water 2023;15(14):2532. https://doi.org/10.3390/w15142532
Ma X, Li Y, Wang L, et al. Hypoxia and salinity constrain the sediment microbiota-mediated N removal potential in an estuary: A multi-trophic interrelationship perspective. Water Res 2024;248:120872. https://doi.org/10.1016/j.watres.2023.120872 PMid: 38006831
Hu N, Li Y, Yin J, et al. A novel Zobellella endophytica W14 strain for nitrogen removal from hypersaline wastewater through simultaneous nitrification and denitrification. J Environ Manage 2024;371:123171. https://doi.org/10.1016/j.jenvman.2024.123171 PMid: 39500170
Williams WD. Salinity as a determinant of the structure of biological communities in salt lakes. Hydrobiologia 1998;381:191-201. https://doi.org/10.1023/A:1003287826503
Moussa MS, Sumanasekera DU, Ibrahim SH, et al. Long term effects of salt on activity, population structure and floc characteristics in enriched bacterial cultures of nitrifiers. Water Res 2006;40(7):1377-1388. https://doi.org/10.1016/j.watres.2006.01.029 PMid: 16530803
Yang J, Tian Z, Spanjers H, et al. Feasibility of using NaCl to reduce membrane fouling in anaerobic membrane bioreactors. Water Environ Res 2014;86(4):340-345. https://doi.org/10.2175/106143013X13807328849657 PMid: 24851330
Zhang C, Zhu Y, Li W, et al. Low-carbon and high-ammonia nitrogen dispersed wastewater treatment: From “normal-sludge” to “low-sludge” to “no-sludge” modes. Environ Res 2023;233:116498. https://doi.org/10.1016/j.envres.2023.116498 PMid: 37356528
Chen S, Liu C, Cao G, et al. Effect of salinity on biological nitrogen removal from wastewater and its mechanism. Environ Sci Pollut Res Int 2024;31:24713-24723. https://doi.org/10.1007/s11356-024-32417-8 PMid: 38499924
Van Niel CB, Allen MB. A note on Pseudomonas stutzeri. J Bacteriol 1952;64:413-422. https://doi.org/10.1128/jb.64.3.413-422.1952 PMid: 12980914
Lalucat J, Bennasar A, Bosch R, et al. Biology of Pseudomonas stutzeri. Microbiol Mol Biol Rev 2006;70(2):510-547. https://doi.org/10.1128/MMBR.00047-05 PMid: 16760312
Park SW, Back JH, Lee SW, et al. Successful antibiotic treatment of Pseudomonas stutzeri-induced peritonitis without peritoneal dialysis catheter removal in continuous ambulatory peritoneal dialysis. Kidney Res Clin Pract 2013;32(2):81-83. https://doi.org/10.1016/j.krcp.2013.04.004 PMid: 26877919
Fu W-l, Duan P-f, Wang Q, et al. Transcriptomics reveals the effect of ammonia nitrogen concentration on Pseudomonas stutzeri F2 assimilation and the analysis of amtB function. Synth Syst Biotechnol 2023;8(2):262-272. https://doi.org/10.1016/j.synbio.2023.03.002 PMid: 37033292
Zhang X, Wen H, Wang H, et al. RNA-Seq analysis of salinity stress-responsive transcriptome in the liver of spotted sea bass (Lateolabrax maculatus). PLoS ONE 2017;12(3):e0173238. https://doi.org/10.1371/journal.pone.0173238 PMid: 28253338
Dumas J-L, van Delden C, Perron K, et al. Analysis of antibiotic resistance gene expression in Pseudomonas aeruginosa by quantitative real-time-PCR. FEMS Microbiol Lett. 2006;254(2):217-225. https://doi.org/10.1111/j.1574-6968.2005.00008.x PMid: 16445748.
Ughy B, Nagyapati S, Lajko DB, et al. Reconsidering dogmas about the growth of bacterial populations. Cells 2023;12(10):1430. https://doi.org/10.3390/cells12101430 PMid: 37408264
Chakraborty S, Mondal S. Halotolerant Citrobacter sp. remediates salinity stress and promotes the growth of Vigna radiata (L) by secreting extracellular polymeric substances (EPS) and biofilm formation: a novel active cell for microbial desalination cell (MDC). Int Microbiol 2024;27:291-301. https://doi.org/10.1007/s10123-023-00386-6 PMid: 37329438
Allen KJ, Griffiths MW. Impact of hydroxyl- and superoxide anion-based oxidative stress on logarithmic and stationary phase Escherichia coli O157:H7 stress and virulence gene expression. Food Microbiol 2012;29(1):141-147. https://doi.org/10.1016/j.fm.2011.09.014 PMid: 22029928
Mortazavi A, Williams BA, McCue K, et al. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008;5:621-628. https://doi.org/10.1038/nmeth.1226 PMid: 18516045
Sies H, Belousov VV, Chandel NS, et al. Defining roles of specific reactive oxygen species (ROS) in cell biology and physiology. Nat Rev Mol Cell Biol 2022;23:499-515. https://doi.org/10.1038/s41580-022-00456-z PMid: 35190722
Singh N, Bhatla SC. Nitric oxide and iron modulate heme oxygenase activity as a long distance signaling response to salt stress in sunflower seedling cotyledons. Nitric Oxide 2016;53:54-64. https://doi.org/10.1016/j.niox.2016.01.003 PMid: 26778276
Hasanuzzaman M, Raihan MR, Nowroz F, et al. Insight into the mechanism of salt-induced oxidative stress tolerance in soybean by the application of Bacillus subtilis: Coordinated actions of osmoregulation, ion homeostasis, antioxidant defense, and methylglyoxal detoxification. Antioxidants 2022;11(10):1856. https://doi.org/10.3390/antiox11101856 PMid: 36290578
Hill BC. Electron transfer from cytochrome c to O2a. Ann NY Acad Sci 1988;550(1):98-104. https://doi.org/10.1111/j.1749-6632.1988.tb35326.x PMid: 2854415
Ramzan R, Vogt S, Kadenbach B. Stress-mediated generation of deleterious ROS in healthy individuals - role of cytochrome c oxidase. J Mol Med 2020;98:651-657. https://doi.org/10.1007/s00109-020-01905-y PMid: 32313986
Shamsad A, Gautam T, Singh R, et al. Association of mRNA expression and polymorphism of antioxidant glutathione-S-transferase (GSTM1 and GSTT1) genes with the risk of Gestational Diabetes Mellitus (GDM). Gene 2024;928:148746. https://doi.org/10.1016/j.gene.2024.148746 PMid: 39004322
Jena AB, Samal RR, Bhol NK, et al. Cellular Red-Ox system in health and disease: The latest update. Biomed Pharmacother 2023;162:114606. https://doi.org/10.1016/j.biopha.2023.114606 PMid: 36989716
Kedishvili N, Goodwin G, Popov K, et al. Mammalian methylmalonate-semialdehyde dehydrogenase. Methods Enzymol 2000;324:207-218. https://doi.org/10.1016/S0076-6879(00)24233-X PMid: 10989432
Diallinas G, Martzoukou O. Transporter membrane traffic and function: lessons from a mould. FEBS J 2019;286(24):4861-4875. https://doi.org/10.1111/febs.15078 PMid: 31583839
Tang K, Jiao N, Liu K, et al. Distribution and functions of TonB-dependent transporters in marine bacteria and environments: Implications for dissolved organic matter utilization. PLOS ONE 2012;7(7):e41204. https://doi.org/10.1371/journal.pone.0041204 PMid: 22829928
Samantarrai D, Lakshman Sagar A, Gudla R, et al. TonB-dependent transporters in sphingomonads: Unraveling their distribution and function in environmental adaptation. Microorganisms 2020;8(3):359. https://doi.org/10.3390/microorganisms8030359 PMid: 32138166
Epstein W. The roles and regulation of potassium in bacteria. Prog Nucleic Acid Res Mol Biol 2003;75:293-320. https://doi.org/10.1016/S0079-6603(03)75008-9 PMid: 14604015
Noinaj N, Guillier M, Barnard TJ, et al. TonB-dependent transporters: Regulation, structure, and function. Annu Rev Microbiol 2010;4:43-60. https://doi.org/10.1146/annurev.micro.112408.134247 PMid: 20420522
Ferguson AD, Deisenhofer J. TonB-dependent receptors—structural perspectives. Biochimica et Biophysica Acta (BBA) – Biomembranes 2002;1565(2):318-332. https://doi.org/10.1016/S0005-2736(02)00578-3
Hernández-Elvira M, Sunnerhagen P. Post-transcriptional regulation during stress. FEMS Yeast Res 2022;22(1):foac025. https://doi.org/10.1093/femsyr/foac025 PMid: 35561747
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.
Copyright (c) 2025 Electronic Journal of Biotechnology