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

Xiaoqin Wu,Nancy J Hess,Wanli Yang,Romy Chakraborty,Terry C Hazen,Yina Liu,Ping Zhang,Qinghao Li,Jizhong Zhou,Liyou Wu

doi:10.3389/fmicb.2018.01234

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 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.

Highlights

Natural organic matter (NOM) is the largest reactive reservoir of reduced carbon (C) on Earth (Bianchi, 2011), and transformation/decomposition of NOM is of fundamental interest due to its contributions to the global C cycle and C flux in ecosystems (Schlesinger and Andrews, 2000; Davidson and Janssens, 2006; Heimann and Reichstein, 2008)
Sediment sample was obtained from a borehole FW305, at Oak Ridge Reservation Field Research Center (ORR-FRC), Oak Ridge, TN, at the depth of 4.6–5 m below ground surface
The extracted dissolved organic matter (DOM) showed no significant absorbance across this range in Ultraviolet– visible spectroscopy (UV/Vis) spectrum, suggesting that low amounts of aromatic/unsaturated compounds existed in the sediment-derived DOM

Summary

Introduction

Natural organic matter (NOM) is the largest reactive reservoir of reduced carbon (C) on Earth (Bianchi, 2011), and transformation/decomposition of NOM is of fundamental interest due to its contributions to the global C cycle and C flux in ecosystems (Schlesinger and Andrews, 2000; Davidson and Janssens, 2006; Heimann and Reichstein, 2008). It was widely accepted that soil NOM persisted as chemically stable ‘humic substances,’ complex mixtures of high molecular weight biopolymers and their degradation products, and was unlikely to be substantially degraded by microbes (Kelleher and Simpson, 2006). Recent insights indicated that the persistence of NOM is not just dependent on its intrinsic molecular structure, and on other factors such as NOM concentration (Arrieta et al, 2015) and biophysico-chemical influences (e.g., microbial activity) drawn from the surrounding environment (Kleber, 2010; Schmidt et al, 2011; Kallenbach et al, 2016). NOM chemistry affects microbial community structure and metabolic potential, as recently elucidated in marine (McCarren et al, 2010), soil (Ding et al, 2015), and groundwater environments (Zhang et al, 2015b). Microbial community composition, ability of microbes to metabolize/transform NOM, and bioavailability of C substrates in NOM are intimately connected, but such interactions are not well documented in the environment

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