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Microbial and Environmental Processes Shape the Link between Organic Matter Functional Traits and Composition

  • Ang Hu
    Ang Hu
    College of Resources and Environment, Hunan Agricultural University, Changsha 410128, China
    State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academic of Sciences, Nanjing 210008, China
    More by Ang Hu
  • Kyoung-Soon Jang
    Kyoung-Soon Jang
    Bio-Chemical Analysis Team, Korea Basic Science Institute, Cheongju 28119, South Korea
  • Fanfan Meng
    Fanfan Meng
    State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academic of Sciences, Nanjing 210008, China
    University of Chinese Academy of Sciences, Beijing 100049, China
    More by Fanfan Meng
  • James Stegen
    James Stegen
    Pacific Northwest National Laboratory, 902 Battelle Boulevard, P.O. Box 999, Richland, Washington 99352, United States
    More by James Stegen
  • Andrew J. Tanentzap
    Andrew J. Tanentzap
    Ecosystems and Global Change Group, Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, U.K.
  • Mira Choi
    Mira Choi
    Bio-Chemical Analysis Team, Korea Basic Science Institute, Cheongju 28119, South Korea
    More by Mira Choi
  • Jay T. Lennon
    Jay T. Lennon
    Department of Biology, Indiana University, Bloomington, Indiana 47405, United States
  • Janne Soininen
    Janne Soininen
    Department of Geosciences and Geography, University of Helsinki, Helsinki, FIN 00014, Finland
  • , and 
  • Jianjun Wang*
    Jianjun Wang
    State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academic of Sciences, Nanjing 210008, China
    University of Chinese Academy of Sciences, Beijing 100049, China
    *Email: [email protected]
    More by Jianjun Wang
Cite this: Environ. Sci. Technol. 2022, 56, 14, 10504–10516
Publication Date (Web):June 23, 2022
https://doi.org/10.1021/acs.est.2c01432
Copyright © 2022 American Chemical Society

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    Abstract

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    Dissolved organic matter (DOM) is a large and complex mixture of molecules that fuels microbial metabolism and regulates biogeochemical cycles. Individual DOM molecules have unique functional traits, but how their assemblages vary deterministically under global change remains poorly understood. Here, we examine DOM and associated bacteria in 300 aquatic microcosms deployed on mountainsides that span contrasting temperatures and nutrient gradients. Based on molecular trait dimensions of reactivity and activity, we partition the DOM composition into labile-active, recalcitrant-active, recalcitrant-inactive, and labile-inactive fractions and quantify the relative influences of deterministic and stochastic processes governing the assembly of each. At both subtropical and subarctic study sites, the assembly of labile or recalcitrant molecules in active fractions is primarily governed by deterministic processes, while stochastic processes are more important for the assembly of molecules within inactive fractions. Surprisingly, the importance of deterministic selection increases with global change gradients for recalcitrant molecules in both active and inactive fractions, and this trend is paralleled by changes in the deterministic assembly of microbial communities and environmental filtering, respectively. Together, our results highlight the shift in focus from potential reactivity to realized activity and indicate that active and inactive fractions of DOM assemblages are structured by contrasting processes, and their recalcitrant components are consistently sensitive to global change. Our study partitions the DOM molecular composition across functional traits and links DOM with microbes via a shared ecological framework of assembly processes. This integrated approach opens new avenues to understand the assembly and turnover of organic carbon in a changing world.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.2c01432.

    • Additional information on the methods of bacterial and DOM analyses, data on the relationships between energy supply and two global change drivers, distribution of molecular biochemical transformations of DOM, ecological processes for DOM molecules with different transformations, ecological processes underlying DOM assemblages with elevations or nutrient enrichment, drivers for βNTI, pH distribution, ecological processes underlying DOM assemblages with pH, relative abundance of DOM molecules, networks of DOM molecules, molecular traits of DOM, variability of ecological processes under global change, molecular composition of DOM, drivers for DOM composition, and molecular trait with pH (PDF)

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    Cited By

    This article is cited by 7 publications.

    1. Jia Shi, Zi Wang, Yumei Peng, Zhongmin Fan, Ziyun Zhang, Xiang Wang, Kun Zhu, Jianying Shang, Jie Wang. Effects of Microplastics on Soil Carbon Mineralization: The Crucial Role of Oxygen Dynamics and Electron Transfer. Environmental Science & Technology 2023, 57 (36) , 13588-13600. https://doi.org/10.1021/acs.est.3c02133
    2. Wanzhu Li, Na Liu, Jianfeng Li, Baoli Wang, Xinjie Shi, Xia Liang, Meiling Yang, Sheng Xu, Cong-Qiang Liu. Chemodiversity of Dissolved Organic Matter Is Governed by Microbial Biogeography in Inland Waters. Environmental Science & Technology 2023, 57 (20) , 7753-7763. https://doi.org/10.1021/acs.est.3c00896
    3. Junzhuo Liu, Lirong Wu, Lina Gong, Yonghong Wu, Andrew J. Tanentzap. Phototrophic Biofilms Transform Soil-Dissolved Organic Matter Similarly Despite Compositional and Environmental Differences. Environmental Science & Technology 2023, 57 (11) , 4679-4689. https://doi.org/10.1021/acs.est.2c08541
    4. Ang Hu, Fanfan Meng, Andrew J. Tanentzap, Kyoung-Soon Jang, Jianjun Wang. Dark Matter Enhances Interactions within Both Microbes and Dissolved Organic Matter under Global Change. Environmental Science & Technology 2023, 57 (1) , 761-769. https://doi.org/10.1021/acs.est.2c05052
    5. Yuanze Sun, Xinfei Li, Xiaomin Li, Jie Wang. Deciphering the Fingerprint of Dissolved Organic Matter in the Soil Amended with Biodegradable and Conventional Microplastics Based on Optical and Molecular Signatures. Environmental Science & Technology 2022, 56 (22) , 15746-15759. https://doi.org/10.1021/acs.est.2c06258
    6. Zhuang Wang, Le Yu, De-Gao Wang. Dissolved Organic Matter and Lignin Modulate Aquatic Toxicity and Oxidative Stress Response Activated by Layered Double Hydroxides Nanomaterials. Archives of Environmental Contamination and Toxicology 2023, 18 https://doi.org/10.1007/s00244-023-00985-4
    7. Yuanze Sun, Jianghao Ji, Jianguo Tao, Yuyi Yang, Dong Wu, Lanfang Han, Si Li, Jie Wang. Current advances in interactions between microplastics and dissolved organic matters in aquatic and terrestrial ecosystems. TrAC Trends in Analytical Chemistry 2023, 158 , 116882. https://doi.org/10.1016/j.trac.2022.116882

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