| Citation: | Zhao-Qi Song, Li Wang, Yaru Ma, Dandan Deng, Yang Song, Feng Liang, Xiangyu Guan, Wen-Jun Li, Hongchen Jiang. Hydrochemistry Predominantly Shapes the Unique Nitrogen-Fixing Bacterial Communities in Tibetan Hot Springs. Journal of Earth Science, 2025, 36(1): 134-145. doi: 10.1007/s12583-024-0147-4
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The Tibetan Plateau has a large number of hot springs with varying temperatures and hydrochemistry, high elevation, and limited nitrogenous nutrition. Nitrogen-fixing bacteria (NFB) can fix N2 to form ammonia and thus provide bioavailable nitrogen. However, there is limited knowledge about the distribution of NFB and its influencing factors in Tibetan hot springs. Here, we measured hydrochemical variables of the hot springs with a wide temperature range (32–77 ºC) in the Qucai and Daggyai geothermal zones on the Tibetan Plateau and investigated the composition of NFB using high-throughput sequencing of 16S rRNA and
| Alcamán-Arias, M. E., Pedrós-Alió, C., Tamames, J., et al., 2018. Diurnal Changes in Active Carbon and Nitrogen Pathways along the Temperature Gradient in Porcelana Hot Spring Microbial Mat. Frontiers in Microbiology, 9: 2353. https://doi.org/10.3389/fmicb.2018.02353 |
| Amenabar, M. J., Boyd, E. S., 2019. A Review of the Mechanisms of Mineral-Based Metabolism in Early Earth Analog Rock-Hosted Hydrothermal Ecosystems. World Journal of Microbiology & Biotechnology, 35(2): 29. https://doi.org/10.1007/s11274-019-2604-2 |
| Bertics, V., Sohm, J., Treude, T., et al., 2010. Burrowing Deeper into Benthic Nitrogen Cycling: The Impact of Bioturbation on Nitrogen Fixation Coupled to Sulfate Reduction. Marine Ecology Progress Series, 409: 1–15. https://doi.org/10.3354/meps08639 |
| Bolyen, E., Rideout, J. R., Dillon, M. R., et al., 2019. Reproducible, Interactive, Scalable and Extensible Microbiome Data Science Using QIIME 2. Nature Biotechnology, 37(8): 852–857. https://doi.org/10.1038/s41587-019-0209-9 |
| Caporaso, J. G., Kuczynski, J., Stombaugh, J., et al., 2010. QIIME Allows Analysis of High-Throughput Community Sequencing Data. Nature Methods, 7(5): 335–336. https://doi.org/10.1038/nmeth.f.303 |
|
Castenholz, R. W., Pierson, B. K., 1995. Ecology of Thermophilic Anoxygenic Phototrophs. In: Blankenship, R. E., Madigan, M. T., Bauer, C. E., eds. Anoxygenic Photosynthetic Bacteria. Kluwer Academic Publishers, Dordrecht. 87–103. |
| De'Ath, G., 2007. Boosted Trees for Ecological Modeling and Prediction. Ecology, 88(1): 243–251. https://doi.org/10.1890/0012-9658(2007)88[243: btfema]2.0.co;2 doi: 10.1890/0012-9658(2007)88[243:btfema]2.0.co;2 |
| Edgar, R. C., Haas, B. J., Clemente, J. C., et al., 2011. UCHIME Improves Sensitivity and Speed of Chimera Detection. Bioinformatics, 27(16): 2194–2200. https://doi.org/10.1093/bioinformatics/btr381 |
| Eichner, M., Kranz, S. A., Rost, B., 2014. Combined Effects of Different CO2 Levels and N Sources on the Diazotrophic Cyanobacterium Trichodesmium. Physiologia Plantarum, 152(2): 316–330. https://doi.org/10.1111/ppl.12172 |
| Estrella-Alcamán, M., Fernandez, C., Delgado, A., et al., 2015. The Cyanobacterium Mastigocladus Fulfills the Nitrogen Demand of a Terrestrial Hot Spring Microbial Mat. The ISME Journal, 9(10): 2290–2303. https://doi.org/10.1038/ismej.2015.63 |
| Feng, C., Yang, J., Jiang, H. C., 2018. Diversity and Distribution of Nitrogen-Fixing Bacteria in Two Geothermal Channels in Tengchong Geothermal Zone, Yunnan Province. Earth Science, 43(Suppl. 1): 10–18 (in Chinese with English Abstract) |
| Feng, K., Peng, X., Zhang, Z., et al., 2022. INAP: An Integrated Network Analysis Pipeline for Microbiome Studies. iMeta, 1(2): e13. https://doi.org/10.1002/imt2.13 |
| Gaby, J. C., Buckley, D. H., 2012. A Comprehensive Evaluation of PCR Primers to Amplify the nifH Gene of Nitrogenase. PLoS One, 7(7): e42149. https://doi.org/10.1371/journal.pone.0042149 |
| Gier, J., Sommer, S., Löscher, C. R., et al., 2016. Nitrogen Fixation in Sediments along a Depth Transect through the Peruvianoxygen Minimum Zone. Biogeosciences, 13(14): 4065–4080. https://doi.org/10.5194/bg-13-4065-2016 |
| Gruber, N., Galloway, J. N., 2008. An Earth-System Perspective of the Global Nitrogen Cycle. Nature, 451(7176): 293–296. https://doi.org/10.1038/nature06592 |
| Guo, Q. H., Kirk Nordstrom, D., Blaine McCleskey, R., 2014. Towards Understanding the Puzzling Lack of Acid Geothermal Springs in Tibet (China): Insight from a Comparison with Yellowstone (USA) and Some Active Volcanic Hydrothermal Systems. Journal of Volcanology and Geothermal Research, 288: 94–104. https://doi.org/10.1016/j.jvolgeores.2014.10.005 |
| Guo, Q. H., Wang, Y. X., 2012. Geochemistry of Hot Springs in the Tengchong Hydrothermal Areas, Southwestern China. Journal of Volcanology and Geothermal Research, 215: 61–73. https://doi.org/10.1016/j.jvolgeores.2011.12.003 |
| Hall, J. R., Mitchell, K. R., Jackson-Weaver, O., et al., 2008. Molecular Characterization of the Diversity and Distribution of a Thermal Spring Microbial Community by Using rRNA and Metabolic Genes. Applied and Environmental Microbiology, 74(15): 4910–4922. https://doi.org/10.1128/AEM.00233-08 |
| Hamilton, T. L., Boyd, E. S., Peters, J. W., 2011. Environmental Constraints Underpin the Distribution and Phylogenetic Diversity of nifH in the Yellowstone Geothermal Complex. Microbial Ecology, 61(4): 860–870. https://doi.org/10.1007/s00248-011-9824-9 |
| Hamilton, T. L., Koonce, E., Howells, A., et al., 2014. Competition for Ammonia Influences the Structure of Chemotrophic Communities in Geothermal Springs. Applied and Environmental Microbiology, 80(2): 653–661. https://doi.org/10.1128/AEM.02577-13 |
| Huang, Q. Y., Dong, C. Z., Dong, R. M., et al., 2011. Archaeal and Bacterial Diversity in Hot Springs on the Tibetan Plateau, China. Extremophiles, 15(5): 549. https://doi.org/10.1007/s00792-011-0386-z |
| Jabir, T., Vipindas, P. V., Jesmi, Y., et al., 2021. Influence of Environmental Factors on Benthic Nitrogen Fixation and Role of Sulfur Reducing Diazotrophs in a Eutrophic Tropical Estuary. Marine Pollution Bulletin, 165: 112126. https://doi.org/10.1016/j.marpolbul.2021.112126 |
| Jiang, Z., Li, P., Tu, J., et al., 2018. Arsenic in Geothermal Systems of Tengchong, China: Potential Contamination on Freshwater Resources. International Biodeterioration & Biodegradation, 128: 28–35. https://doi.org/10.1016/j.ibiod.2016.05.013 |
| Klatt, C. G., Liu, Z. F., Ludwig, M., et al., 2013. Temporal Metatranscriptomic Patterning in Phototrophic Chloroflexi Inhabiting a Microbial Mat in a Geothermal Spring. The ISME Journal, 7(9): 1775–1789. https://doi.org/10.1038/ismej.2013.52 |
| Klingler, J. M., Mancinelli, R. L., White, M. R., 1989. Biological Nitrogen Fixation under Primordial Martian Partial Pressures of Dinitrogen. Advances in Space Research, 9(6): 173–176. https://doi.org/10.1016/0273-1177(89)90225-1 |
| Lehnen, N., Marchant, H. K., Schwedt, A., et al., 2016. High Rates of Microbial Dinitrogen Fixation and Sulfate Reduction Associated with the Mediterranean Seagrass Posidonia Oceanica. Systematic and Applied Microbiology, 39(7): 476–483. https://doi.org/10.1016/j.syapm.2016.08.004 |
| Li, R., Wu, G., Jones, B., et al., 2020. Microbial Fabrics of Geyserites around Hot Spring Pools in Daggyai, Tibet, China. Terra Nova, 32(5): 355–368. https://doi.org/10.1111/ter.12465 |
| Lin, K. H., Liao, B. Y., Chang, H. W., et al., 2015. Metabolic Characteristics of Dominant Microbes and Key Rare Species from an Acidic Hot Spring in Taiwan Revealed by Metagenomics. BMC Genomics, 16(1): 1029. https://doi.org/10.1186/s12864-015-2230-9 |
| Liu, M. L., Guo, Q. H., Wu, G., et al., 2019. Boron Geochemistry of the Geothermal Waters from Two Typical Hydrothermal Systems in Southern Tibet (China): Daggyai and Quzhuomu. Geothermics, 82: 190–202. https://doi.org/10.1016/j.geothermics.2019.06.009 |
| Loiacono, S. T., Meyer-Dombard, D. R., Havig, J. R., et al., 2012. Evidence for High-Temperature in situ nifH Transcription in an Alkaline Hot Spring of Lower Geyser Basin, Yellowstone National Park. Environmental Microbiology, 14(5): 1272–1283. https://doi.org/10.1111/j.1462-2920.2012.02710.x |
| Ma, L., Wu, G., Yang, J., et al., 2021a. Distribution of Hydrogen-Producing Bacteria in Tibetan Hot Springs, China. Frontiers in Microbiology, 12: 569020. https://doi.org/10.3389/fmicb.2021.569020 |
| Ma, L., She, W. Y., Wu, G., et al., 2021b. Influence of Temperature and Sulfate Concentration on the Sulfate/Sulfite Reduction Prokaryotic Communities in the Tibetan Hot Springs. Microorganisms, 9(3): 583. https://doi.org/10.3390/microorganisms9030583 |
| Magoč, T., Salzberg, S. L., 2011. FLASH: Fast Length Adjustment of Short Reads to Improve Genome Assemblies. Bioinformatics, 27(21): 2957–2963. https://doi.org/10.1093/bioinformatics/btr507 |
| Martinez, J. N., Nishihara, A., Lichtenberg, M., et al., 2019. Vertical Distribution and Diversity of Phototrophic Bacteria within a Hot Spring Microbial Mat (Nakabusa Hot Springs, Japan). Microbes and Environments, 34(4): 374–387. https://doi.org/10.1264/jsme2.ME19047 |
| Miller, S. R., Purugganan, M. D., Curtis, S. E., 2006. Molecular Population Genetics and Phenotypic Diversification of Two Populations of the Thermophilic Cyanobacterium Mastigocladus Laminosus. Applied and Environmental Microbiology, 72(4): 2793–2800. https://doi.org/10.1128/AEM.72.4.2793-2800.2006 |
| Newell, S. E., McCarthy, M. J., Gardner, W. S., et al., 2016. Sediment Nitrogen Fixation: A Call for re-Evaluating Coastal N Budgets. Estuaries and Coasts, 39(6): 1626–1638. https://doi.org/10.1007/s12237-016-0116-y |
| Newton, W. E., 2007. Physiology, Biochemistry, and Molecular Biology of Nitrogen Fixation. In: Biology of the Nitrogen Cycle. Elsevier, Amsterdam. 109–129. https://doi.org/10.1016/b978-044452857-5.50009-6 |
| Nishihara, A., Thiel, V., Matsuura, K., et al., 2018. Phylogenetic Diversity of Nitrogenase Reductase Genes and Possible Nitrogen-Fixing Bacteria in Thermophilic Chemosynthetic Microbial Communities in Nakabusa Hot Springs. Microbes and Environments, 33(4): 357–365. https://doi.org/10.1264/jsme2.ME18030 |
| Raymond, J., Siefert, J. L., Staples, C. R., et al., 2004. The Natural History of Nitrogen Fixation. Molecular Biology and Evolution, 21(3): 541–554. https://doi.org/10.1093/molbev/msh047 |
| Rui, J. P., Hu, J. J., Wang, F. X., et al., 2022. Altitudinal Niches of Symbiotic, Associative and Free-Living Diazotrophs Driven by Soil Moisture and Temperature in the Alpine Meadow on the Tibetan Plateau. Environmental Research, 211: 113033. https://doi.org/10.1016/j.envres.2022.113033 |
| Sayavedra, L., Li, T. Q., Bueno Batista, M., et al., 2021. Desulfovibrio Diazotrophicus Sp. Nov., a Sulfate-Reducing Bacterium from the Human Gut Capable of Nitrogen Fixation. Environmental Microbiology, 23(6): 3164–3181. https://doi.org/10.1111/1462-2920.15538 |
| Sekiguchi, Y., Muramatsu, M., Imachi, H., et al., 2008. Thermodesulfovibrio Aggregans Sp. Nov. and Thermodesulfovibrio Thiophilus Sp. Nov., Anaerobic, Thermophilic, Sulfate-Reducing Bacteria Isolated from Thermophilic Methanogenic Sludge, and Emended Description of the Genus Thermodesulfovibrio. International Journal of Systematic and Evolutionary Microbiology, 58(Pt 11): 2541–2548. https://doi.org/10.1099/ijs.0.2008/000893-0 |
| Shannon, P., Markiel, A., Ozier, O., et al., 2003. Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks. Genome Research, 13(11): 2498–2504. https://doi.org/10.1101/gr.1239303 |
| Silverman, S. N., Kopf, S. H., Bebout, B. M., et al., 2019. Morphological and Isotopic Changes of Heterocystous Cyanobacteria in Response to N2 Partial Pressure. Geobiology, 17(1): 60–75. https://doi.org/10.1111/gbi.12312 |
| Smith, A. C., Kostka, J. E., Devereux, R., et al., 2004. Seasonal Composition and Activity of Sulfate-Reducing Prokaryotic Communities in Seagrass Bed Sediments. Aquatic Microbial Ecology, 37: 183–195. https://doi.org/10.3354/ame037183 |
| Song, Z. Q., Wang, F. P., Zhi, X. Y., et al., 2013. Bacterial and Archaeal Diversities in Yunnan and Tibetan Hot Springs, China. Environmental Microbiology, 15(4): 1160–1175. https://doi.org/10.1111/1462-2920.12025 |
| Song, Z. Q., Wang, L., Liang, F., et al., 2022. nifH Gene Expression and Diversity in Geothermal Springs of Tengchong, China. Frontiers in Microbiology, 13: 980924. https://doi.org/10.3389/fmicb.2022.980924 |
| Sonne-Hansen, J., Ahring, B. K., 1999. Thermodesulfobacterium Hveragerdense Sp. nov., and Thermodesulfovibrio Islandicus Sp. nov., Two Thermophilic Sulfate Reducing Bacteria Isolated from a Icelandic Hot Spring. Systematic and Applied Microbiology, 22(4): 559–564. https://doi.org/10.1016/S0723-2020(99)80009-5 |
| Steunou, A. S., Bhaya, D., Bateson, M. M., et al., 2006. In Situ Analysis of Nitrogen Fixation and Metabolic Switching in Unicellular Thermophilic Cyanobacteria Inhabiting Hot Spring Microbial Mats. Proceedings of the National Academy of Sciences of the United States of America, 103(7): 2398–2403. https://doi.org/10.1073/pnas.0507513103 |
| Steunou, A. S., Jensen, S. I., Brecht, E., et al., 2008. Regulation of Nif Gene Expression and the Energetics of N2 Fixation over the Diel Cycle in a Hot Spring Microbial Mat. The ISME Journal, 2(4): 364–378. https://doi.org/10.1038/ismej.2007.117 |
| Tamburello, G., Chiodini, G., Ciotoli, G., et al., 2022. Global Thermal Spring Distribution and Relationship to Endogenous and Exogenous Factors. Nature Communications, 13(1): 6378. https://doi.org/10.1038/s41467-022-34115-w |
| Tan, H. B., Zhang, Y. F., Zhang, W. J., et al., 2014. Understanding the Circulation of Geothermal Waters in the Tibetan Plateau Using Oxygen and Hydrogen Stable Isotopes. Applied Geochemistry, 51: 23–32. https://doi.org/10.1016/j.apgeochem.2014.09.006 |
| Umezawa, K., Kojima, H., Kato, Y., et al., 2021. Dissulfurispira Thermophila Gen. Nov., Sp. Nov., a Thermophilic Chemolithoautotroph Growing by Sulfur Disproportionation, and Proposal of Novel Taxa in the Phylum Nitrospirota to Reclassify the Genus Thermodesulfovibrio. Systematic and Applied Microbiology, 44(2): 126184. https://doi.org/10.1016/j.syapm.2021.126184 |
| Wang, S., Hou, W. G., Dong, H. L., et al., 2013. Control of Temperature on Microbial Community Structure in Hot Springs of the Tibetan Plateau. PLoS One, 8(5): e62901. https://doi.org/10.1371/journal.pone.0062901 |
| Wang, X. J., Yin, Y., Yu, Z. Q., et al., 2023. Distinct Distribution Patterns of the Abundant and Rare Bacteria in High Plateau Hot Spring Sediments. Science of the Total Environment, 863: 160832. https://doi.org/10.1016/j.scitotenv.2022.160832 |
| Zehr, J. P., Jenkins, B. D., Short, S. M., et al., 2003. Nitrogenase Gene Diversity and Microbial Community Structure: A Cross-System Comparison. Environmental Microbiology, 5(7): 539–554. https://doi.org/10.1046/j.1462-2920.2003.00451.x |
| Zhang, Y. M., Wu, G., Jiang, H. C., et al., 2018. Abundant and Rare Microbial Biospheres Respond Differently to Environmental and Spatial Factors in Tibetan Hot Springs. Frontiers in Microbiology, 9: 2096. https://doi.org/10.3389/fmicb.2018.02096 |
| Zhang, Y. Y., Yang, Q. S., Ling, J., et al., 2017. Diversity and Structure of Diazotrophic Communities in Mangrove Rhizosphere, Revealed by High-Throughput Sequencing. Frontiers in Microbiology, 8: 2032. https://doi.org/10.3389/fmicb.2017.02032 |
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