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Title: Microbial Interactions With Dissolved Organic Matter Drive Carbon Dynamics and Community Succession

Abstract

Knowledge of dynamic interactions between natural organic matter (NOM) and microbial communities is critical not only to delineate the routes of NOM degradation/transformation and carbon (C) fluxes, but also to understand microbial community evolution and succession in ecosystems. Yet, these processes in subsurface environments are usually studied independently, and a comprehensive view has been elusive thus far. In this study, we fed sediment-derived dissolved organic matter (DOM) to groundwater microbes and continually analyzed microbial transformation of DOM over a 50-day incubation. To document fine-scale changes in DOM chemistry, we applied high-resolution Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR MS) and soft X-ray absorption spectroscopy (sXAS). We also monitored the trajectory of microbial biomass, community structure and activity over this time period. Together, these analyses provided an unprecedented comprehensive view of interactions between sediment-derived DOM and indigenous subsurface groundwater microbes. Microbial decomposition of labile C in DOM was immediately evident from biomass increase and total organic carbon (TOC) decrease. The change of microbial composition was closely related to DOM turnover: microbial community in early stages of incubation was influenced by relatively labile tannin- and protein-like compounds; while in later stages the community composition evolved to be most correlated with lessmore » labile lipid- and lignin-like compounds. These changes in microbial community structure and function, coupled with the contribution of microbial products to DOM pool affected the further transformation of DOM, culminating in stark changes to DOM composition over time. Our study demonstrates a distinct response of microbial communities to biotransformation of DOM, which improves our understanding of coupled interactions between sediment-derived DOM, microbial processes, and community structure in subsurface groundwater.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [1]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences
  2. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Division; Texas A & M Univ., College Station, TX (United States). Geochemical and Environmental Research Group
  4. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS); Shandong Univ., Jinan (China). Key Lab. of Particle Physics and Particle Irradiation (MOE). National Key Laboratory of Crystal Materials, School of Physics
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences; Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology; Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control, School of Environment
  7. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory
  8. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Civil and Environmental Engineering, Dept. of Microbiology, Dept. of Earth and Planetary Sciences, Inst. for a Secure and Sustainable Environment; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  9. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1460341
Alternate Identifier(s):
OSTI ID: 1474860; OSTI ID: 1581959
Report Number(s):
PNNL-SA-135810
Journal ID: ISSN 1664-302X; ark:/13030/qt3hk1f62c
Grant/Contract Number:  
AC02-05CH11231; AC05-00OR22725; AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 9; Journal Issue: JUN; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; natural organic matter (NOM); molecular-level characterization; dynamic interactions; microbial succession; labile carbon; recalcitrant carbon; subsurface carbon cycling; microbe-carbon interactions

Citation Formats

Wu, Xiaoqin, Wu, Liyou, Liu, Yina, Zhang, Ping, Li, Qinghao, Zhou, Jizhong, Hess, Nancy J., Hazen, Terry C., Yang, Wanli, and Chakraborty, Romy. Microbial Interactions With Dissolved Organic Matter Drive Carbon Dynamics and Community Succession. United States: N. p., 2018. Web. doi:10.3389/fmicb.2018.01234.
Wu, Xiaoqin, Wu, Liyou, Liu, Yina, Zhang, Ping, Li, Qinghao, Zhou, Jizhong, Hess, Nancy J., Hazen, Terry C., Yang, Wanli, & Chakraborty, Romy. Microbial Interactions With Dissolved Organic Matter Drive Carbon Dynamics and Community Succession. United States. doi:10.3389/fmicb.2018.01234.
Wu, Xiaoqin, Wu, Liyou, Liu, Yina, Zhang, Ping, Li, Qinghao, Zhou, Jizhong, Hess, Nancy J., Hazen, Terry C., Yang, Wanli, and Chakraborty, Romy. Fri . "Microbial Interactions With Dissolved Organic Matter Drive Carbon Dynamics and Community Succession". United States. doi:10.3389/fmicb.2018.01234. https://www.osti.gov/servlets/purl/1460341.
@article{osti_1460341,
title = {Microbial Interactions With Dissolved Organic Matter Drive Carbon Dynamics and Community Succession},
author = {Wu, Xiaoqin and Wu, Liyou and Liu, Yina and Zhang, Ping and Li, Qinghao and Zhou, Jizhong and Hess, Nancy J. and Hazen, Terry C. and Yang, Wanli and Chakraborty, Romy},
abstractNote = {Knowledge of dynamic interactions between natural organic matter (NOM) and microbial communities is critical not only to delineate the routes of NOM degradation/transformation and carbon (C) fluxes, but also to understand microbial community evolution and succession in ecosystems. Yet, these processes in subsurface environments are usually studied independently, and a comprehensive view has been elusive thus far. In this study, we fed sediment-derived dissolved organic matter (DOM) to groundwater microbes and continually analyzed microbial transformation of DOM over a 50-day incubation. To document fine-scale changes in DOM chemistry, we applied high-resolution Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR MS) and soft X-ray absorption spectroscopy (sXAS). We also monitored the trajectory of microbial biomass, community structure and activity over this time period. Together, these analyses provided an unprecedented comprehensive view of interactions between sediment-derived DOM and indigenous subsurface groundwater microbes. Microbial decomposition of labile C in DOM was immediately evident from biomass increase and total organic carbon (TOC) decrease. The change of microbial composition was closely related to DOM turnover: microbial community in early stages of incubation was influenced by relatively labile tannin- and protein-like compounds; while in later stages the community composition evolved to be most correlated with less labile lipid- and lignin-like compounds. These changes in microbial community structure and function, coupled with the contribution of microbial products to DOM pool affected the further transformation of DOM, culminating in stark changes to DOM composition over time. Our study demonstrates a distinct response of microbial communities to biotransformation of DOM, which improves our understanding of coupled interactions between sediment-derived DOM, microbial processes, and community structure in subsurface groundwater.},
doi = {10.3389/fmicb.2018.01234},
journal = {Frontiers in Microbiology},
number = JUN,
volume = 9,
place = {United States},
year = {2018},
month = {6}
}

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