Advanced Search

Indexed by SCI、CA、РЖ、PA、CSA、ZR、etc .

Turn off MathJax
Article Contents
Journal of Earth Science  > 2025  > Accepted Manuscript
Muhammad Inayat Ullah Khan, Liuqin Huang, Geng Wu, Jian Yang, Xiangyu Guan, Hongchen Jiang. GeoChip-based microbial functions in biogeochemical cycles and their responses to environmental factors in Tengchong hot springs. Journal of Earth Science. doi: 10.1007/s12583-024-0009-0
Citation: Muhammad Inayat Ullah Khan, Liuqin Huang, Geng Wu, Jian Yang, Xiangyu Guan, Hongchen Jiang. GeoChip-based microbial functions in biogeochemical cycles and their responses to environmental factors in Tengchong hot springs. Journal of Earth Science. doi: 10.1007/s12583-024-0009-0
shu

GeoChip-based microbial functions in biogeochemical cycles and their responses to environmental factors in Tengchong hot springs

doi: 10.1007/s12583-024-0009-0

  • 1. School of Environmental Studies, China University of Geosciences Wuhan, China;

  • 2. State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences Wuhan, China;

  • 3. School of Ocean Sciences, China University of Geosciences, Beijing, 100083, China

Funds:

This research was supported by grants from the National Natural Science Foundation of China (Grant No. 42172339, 91951205). We thank Ms. Xiaoling Chen from the Rehai National Geological Park for the assistant of the field trip.

  • Received Date: 10 Apr 2023
    Available Online: 04 Jan 2025
    Abstract
  • Microorganisms actively participate in biogeochemical cycling processes and play a crucial role in maintaining the dynamic balance of hot spring ecosystems. However, the distribution of microbial functional genes and their influencing factors in hot springs remain largely unclear. Therefore, this study investigated the microbial functional genes and their potential for controlling biogeochemical cycles (C, N, S, and P) in the hot Springs of Tengchong, China, using the Geochip method, a functional gene microarray technology. The examined hot springs have very different microbial functional genes. A total of 22736 gene probe signals were identified, belonging to 567 functional genes and associated with 15 ecological functions, mainly involving stress response, carbon cycle, nitrogen cycle, sulfur cycle, phosphorus cycle and energy processes. The amyA, narG, dsrA and ppx genes were most abundant in carbon, nitrogen, sulfur and phosphorus cycles, respectively, and were significantly correlated with pH, temperature and SO42-. The diversity and abundance of detected gene probes were negatively correlated with temperature. The α-diversity (i.e., Shannon index) was high at low temperature and low pH. Molecular functional interactions revealed by the gene connectivity levels were negatively correlated with temperature, pH and SO42-. These results suggested that the abundance, diversity and interactions of microbial functional genes were significantly influenced by geochemical parameters ֿ . In addition, some genera possessed functional genes related to carbon, nitrogen, sulfur, and phosphorus cycles and can synergistically control the biogeochemical cycles of carbon, nitrogen, sulfur and phosphorus. These findings provide new insights into the functional potentials of microorganisms to participate in biogeochemical cycles and their responses to environmental factors in hot springs.

     

    • FullText(HTML)
  • loading
    • References(63)
  • 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
    Alcamán, M. E., Alcorta, J., Bergman, B., et al., 2017. Physiological and gene expression responses to nitrogen regimes and temperatures in Mastigocladus sp. strain CHP1, a predominant thermotolerant cyanobacterium of hot springs. Systematic and Applied Microbiology, 40(2): 102-113. https://doi.org/10.1016/j.syapm.2016.11.007
    Aoshima, M., Ishii, M. ,Igarashi, Y., 2004. A novel enzyme, citryl‐CoA lyase, catalysing the second step of the citrate cleavage reaction in Hydrogenobacter thermophilus TK‐6. Molecular Microbiology, 52(3): 763-770. https://doi.org/10.1111/j.1365-2958.2004.04010.x
    Badhai, J., Ghosh, T. S. ,Das, S. K., 2015. Taxonomic and functional characteristics of microbial communities and their correlation with physicochemical properties of four geothermal springs in Odisha, India. Frontiers in Microbiology, 6: 1166. https://doi.org/10.3389/fmicb.2015.01166
    Bayer, K., Moitinho-Silva, L., Brümmer, F., et al., 2014. GeoChip-based insights into the microbial functional gene repertoire of marine sponges (high microbial abundance, low microbial abundance) and seawater. FEMS Microbiology Ecology, 90(3): 832-843. https://doi.org/10.1111/1574-6941.12441
    Bennett, A. C., Murugapiran, S. K., Kees, E. D., et al., 2022. Temperature and geographic location impact the distribution and diversity of photoautotrophic gene variants in alkaline Yellowstone hot springs. Microbiology Spectrum, 10(3): e01465-01421. https://doi.org/10.1128/spectrum.01465-21
    Chen, S., Peng, X., Xu, H., et al., 2016. Nitrification of archaeal ammonia oxidizers in a high-temperature hot spring. Biogeosciences, 13(7): 2051-2060. https://doi.org/10.5194/bg-13-2051-2016
    De Anda, V., Chen, L.-X., Dombrowski, N., et al., 2021. Brockarchaeota, a novel archaeal phylum with unique and versatile carbon cycling pathways. Nature Communications, 12(1): 2404. https://doi.org/10.1038/s41467-021-22736-6
    De Hoon, M. J., Imoto, S., Nolan, J., et al., 2004. Open source clustering software. Bioinformatics, 20(9): 1453-1454. https://doi.org/10.1093/bioinformatics/bth078
    De León, K. B., Gerlach, R., Peyton, B. M., et al., 2013. Archaeal and bacterial communities in three alkaline hot springs in Heart Lake Geyser Basin, Yellowstone National Park. Frontiers in Microbiology, 4: 330. https://doi.org/10.3389/fmicb.2013.00330
    Francheteau, J., Needham, H. D., Choukroune, P., et al., 1979. Massive deep-sea sulphide ore deposits discovered on the East Pacific Rise. Nature, 277(5697): 523-528. https://doi.org/10.1038/277523a0
    Hügler, M. ,Sievert, S. M., 2011. Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Annual Review of Marine Science, 3: 261-289. https://doi.org/10.1146/annurev-marine-120709-142712
    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
    Hazen, T. C., Dubinsky, E. A., DeSantis, T. Z., et al., 2010. Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science, 330(6001): 204-208. https://doi.org/10.1126/science.1195979
    He, Z., Deng, Y., Van Nostrand, J. D., et al., 2010. GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity. The ISME Journal, 4(9): 1167-1179. https://doi.org/10.1038/ismej.2010.46
    He, Z., Xiong, J., Kent, A. D., et al., 2014. Distinct responses of soil microbial communities to elevated CO2 and O3 in a soybean agro-ecosystem. The ISME Journal, 8(3): 714-726. https://doi.org/10.1038/ismej.2013.177
    Hou, W., Wang, S., Dong, H., et al., 2013. A comprehensive census of microbial diversity in hot springs of Tengchong, Yunnan Province China using 16S rRNA gene pyrosequencing. PloS One, 8(1): e53350. https://doi.org/10.1371/journal.pone.0053350
    Hua, Z.-S., Qu, Y.-N., Zhu, Q., et al., 2018. Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota. Nature Communications, 9(1): 2832. https://doi.org/10.1038/s41467-018-05284-4
    Hua, Z.-S., Wang, Y.-L., Evans, P. N., et al., 2019. Insights into the ecological roles and evolution of methyl-coenzyme M reductase-containing hot spring Archaea. Nature Communications, 10(1): 1-11. https://doi.org/10.1038/s41467-019-12574-y
    Jiang, H., Huang, Q., Dong, H., et al., 2010. RNA-based investigation of ammonia-oxidizing archaea in hot springs of Yunnan Province, China. Applied and Environmental Microbiology, 76(13): 4538-4541. https://doi.org/10.1128/AEM.00143-10
    Jiang, H., Huang, L., Yang, J., et al., 2018. A microbial analysis primer for biogeochemists. Environmental Geochemistry, Elsevier. 599-609
    Larimer, F. W., Chain, P., Hauser, L., et al., 2004. Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nature Biotechnology, 22(1): 55-61. https://doi.org/10.1038/nbt923
    Li, H., Yang, Q., Li, J., et al., 2015. The impact of temperature on microbial diversity and AOA activity in the Tengchong Geothermal Field, China. Scientific Reports, 5(1): 17056. https://doi.org/10.1038/srep17056
    Li, J.,Kusky, T. M., 2007. World's largest known Precambrian fossil black smoker chimneys and associated microbial vent communities, North China: Implications for early life. Gondwana Research, 12(1-2): 84-100. https://doi.org/10.1016/j.gr.2006.10.024
    Li, J., Zhang, Z., Liu, T., et al., 2022. Bacterial and archaeal water and sediment communities of two hot spring streams in Tengchong, Yunnan Province, China. Diversity, 14(5): 381. https://doi.org/10.3390/d14050381
    Li, Z., Tang, Z., Song, Z., et al., 2022. Variations and controlling factors of soil denitrification rate. Global change biology, 28(6): 2133-2145. https://doi.org/10.1111/gcb.16066
    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: 1-16. https://doi.org/10.1186/s12864-015-2230-9
    Lu, Z., He, Z., Parisi, V. A., et al., 2012. GeoChip-based analysis of microbial functional gene diversity in a landfill leachate-contaminated aquifer. Environmental Science & Technology, 46(11): 5824-5833. https://doi.org/10.1021/es300478j
    Luvizotto, D. M., Araujo, J. E., Silva, M. D. C. P., et al., 2018. The rates and players of denitrification, dissimilatory nitrate reduction to ammonia (DNRA) and anaerobic ammonia oxidation (anammox) in mangrove soils. Anais da Academia Brasileira de Ciências, 91 https://doi.org/10.1590/0001-3765201820180373
    Ma, L., She, W., Wu, G., et al., 2021. 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
    Meng, S., Peng, T., Liu, X., et al., 2022. Ecological role of bacteria involved in the biogeochemical cycles of mangroves based on functional genes detected through GeoChip 5.0. Msphere, 7(1): e00936-00921. https://doi.org/10.1128/msphere.00936-21
    Nakagawa, S.,Takai, K., 2008. Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiology Ecology, 65(1): 1-14. https://doi.org/10.1111/j.1574-6941.2008.00502.x
    Nishiyama, E., Higashi, K., Mori, H., et al., 2018. The relationship between microbial community structures and environmental parameters revealed by metagenomic analysis of hot spring water in the Kirishima Area, Japan. Frontiers in Bioengineering and Biotechnology, 6: 202. https://doi.org/10.3389/fbioe.2018.00202
    Panda, A. K., Bisht, S. S., Rana, M., et al., 2018. Biotechnological potential of thermophilic actinobacteria associated With Hot Springs. New and future developments in microbial biotechnology and bioengineering, Elsevier. 155-164
    Paul, S., Cortez, Y., Vera, N., et al., 2016. Metagenomic analysis of microbial community of an Amazonian geothermal spring in Peru. Genomics Data, 9: 63-66. https://doi.org/10.1016/j.gdata.2016.06.013
    Power, J. F., Carere, C. R., Lee, C. K., et al., 2018. Microbial biogeography of 925 geothermal springs in New Zealand. Nature communications, 9(1): 1-12. https://doi.org/10.1038/s41467-018-05020-y
    Preston, L. J.,Genge, M. J., 2010. The Rhynie Chert, Scotland, and the search for life on Mars. Astrobiology, 10(5): 549-560. https://doi.org/10.1089/ast.2008.0321
    Qi, Y.-L., Evans, P. N., Li, Y.-X., et al., 2021. Comparative genomics reveals thermal adaptation and a high metabolic diversity in “Candidatus Bathyarchaeia”. Msystems, 6(4): 10.1128/msystems. 00252-00221. https://doi.org/10.1128/msystems.00252-21
    Reuther, J.,Wohlleben, W., 2006. Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation. Microbial Physiology, 12(1-2): 139-146. https://doi.org/10.1159/000096469
    Rhee, S.-K., Liu, X., Wu, L., et al., 2004. Detection of genes involved in biodegradation and biotransformation in microbial communities by using 50-mer oligonucleotide microarrays. Applied and Environmental Microbiology, 70(7): 4303-4317. https://doi.org/10.1128/AEM.70.7.4303-4317.2004
    Sadeepa, D., Sirisena, K.,Manage, P. M., 2022. Diversity of microbial communities in hot springs of Sri Lanka as revealed by 16S rRNA gene high-throughput sequencing analysis. Gene, 812: 146103. https://doi.org/10.1016/j.gene.2021.146103
    Sharma, N., Kumar, J., Abedin, M., et al., 2020. Metagenomics revealing molecular profiling of community structure and metabolic pathways in natural hot springs of the Sikkim Himalaya. BMC Microbiology, 20(1): 1-17. https://doi.org/10.1186/s12866-020-01923-3
    Sharp, J., Beauregard, A., Burdige, D., et al., 2004. A direct instrument comparison for measurement of total dissolved nitrogen in seawater. Marine Chemistry, 84(3-4): 181-193. https://doi.org/10.1016/j.marchem.2003.07.003
    Sharp, J. H., Benner, R., Bennett, L., et al., 1993. Re‐evaluation of high temperature combustion and chemical oxidation measurements of dissolved organic carbon in seawater. Limnology and Oceanography, 38(8): 1774-1782. https://doi.org/10.4319/lo.1993.38.8.1774
    Silver, D. M., Kötting, O.,Moorhead, G. B., 2014. Phosphoglucan phosphatase function sheds light on starch degradation. Trends in Plant Science, 19(7): 471-478. https://doi.org/10.1016/j.tplants.2014.01.008
    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
    Song, Z.-Q., Wang, L.,Ma, Y., 2024. Hydrochemistry predominantly shapes the unique nitrogen-fixing bacterial communities in Tibetan hot springs. Journal of Earth Science, in press
    Song, Z. Q., Wang, F. P., Zhi, X. Y., et al., 2013. Bacterial and archaeal diversities in Yunnan and Tibetan hot springs, C hina. Environmental Microbiology, 15(4): 1160-1175. https://doi.org/10.1111/1462-2920.12025
    Thiel, V., Wood, J. M., Olsen, M. T., et al., 2016. The dark side of the mushroom spring microbial mat: life in the shadow of chlorophototrophs. I. Microbial diversity based on 16S rRNA gene amplicons and metagenomic sequencing. Frontiers in Microbiology, 7: 919. https://doi.org/10.3389/fmicb.2016.00919
    Tiquia, S. M., Wu, L., Chong, S. C., et al., 2004. Evaluation of 50-mer oligonucleotide arrays for detecting microbial populations in environmental samples. Biotechniques, 36(4): 664-675. https://doi.org/10.2144/04364RR02
    Van Nostrand, J. D., Wu, W. M., Wu, L., et al., 2009. GeoChip‐based analysis of functional microbial communities during the reoxidation of a bioreduced uranium‐contaminated aquifer. Environmental Microbiology, 11(10): 2611-2626. https://doi.org/10.1111/j.1462-2920.2009.01986.x
    Waldron, P. J., Wu, L., Nostrand, J. D. V., et al., 2009. Functional gene array-based analysis of microbial community structure in groundwaters with a gradient of contaminant levels. Environmental Science & Technology, 43(10): 3529-3534. https://doi.org/10.1021/es803423p
    Wang, S., Hou, W., Dong, H., 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.0099751
    Wu, G., Huang, L., Jiang, H., et al., 2017. Thioarsenate formation coupled with anaerobic arsenite oxidation by a sulfate-reducing bacterium isolated from a hot spring. Frontiers in Microbiology, 8: 1336. https://doi.org/10.3389/fmicb.2017.01336
    Wu, L., Liu, X., Schadt, C. W., et al., 2006. Microarray-based analysis of subnanogram quantities of microbial community DNAs by using whole-community genome amplification. Applied and Environmental Microbiology, 72(7): 4931-4941. https://doi.org/10.1128/AEM.02738-05
    Wu, L., Kellogg, L., Devol, A. H., et al., 2008. Microarray-based characterization of microbial community functional structure and heterogeneity in marine sediments from the Gulf of Mexico. Applied and Environmental Microbiology, 74(14): 4516-4529. https://doi.org/10.1128/AEM.02751-07
    Xie, W., Wang, F., Guo, L., et al., 2011. Comparative metagenomics of microbial communities inhabiting deep-sea hydrothermal vent chimneys with contrasting chemistries. The ISME Journal, 5(3): 414-426. https://doi.org/10.1038/ismej.2010.144
    Xu, M., Wu, W.-M., Wu, L., et al., 2010. Responses of microbial community functional structures to pilot-scale uranium in situ bioremediation. The ISME Journal, 4(8): 1060-1070. https://doi.org/10.1038/ismej.2010.31
    Zhang, Y., Lu, Z., Liu, S., et al., 2013. Geochip-based analysis of microbial communities in alpine meadow soils in the Qinghai-Tibetan plateau. BMC Microbiology, 13: 1-9. https://doi.org/10.1186/1471-2180-13-72
    Zhang, Y., Wu, G., Jiang, H., 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., Liu, T., Li, M.-M., et al., 2023. Hot spring distribution and survival mechanisms of thermophilic comammox Nitrospira. The ISME Journal: 1-11. https://doi.org/10.1038/s41396-023-01409-w
    Zhou, J., Bruns, M. A.,Tiedje, J. M., 1996. DNA recovery from soils of diverse composition. Applied and Environmental Microbiology, 62(2): 316-322. https://doi.org/10.1128/aem.62.2.316-322.1996
    Zierenberg, R. A., Adams, M. W.,Arp, A. J., 2000. Life in extreme environments: Hydrothermal vents. Proceedings of the National Academy of Sciences of the United States of America, 97(24): 12961-12962. https://doi.org/10.1073/pnas.210395997
    • Relative Articles
    • Supplements(0)
    • Cited By
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索
    Get Citation
    PDF
    XML

    Article Metrics

    Article views(11) PDF downloads(5) Cited by()
    Proportional views
    Related

    Copyright © 2013-2020 Journal of Earth Science 鄂ICP备15021562号-2

    Tel: +86-27-67885075 Fax: +86-27-67885075 E-mail: xbb@cug.edu.cn

    Address: Editorial Office of Journal, China University of Geosciences, Yujiashan, Wuhan, Hubei 430074, P. R. China

    Supported by: Beijing Renhe Information Technology Co. Ltd  E-mail: info@rhhz.net  

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return