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 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.

Fueling Diversity in the Subsurface: Composition and Age of Dissolved Organic Matter in the Critical Zone

“…(2) Stimulation of the autochthonous bacterial community in response to influx of diverse DOM substrate from the surface (Zhang et al, 2015;Rajala and Bomberg, 2017;Wu et al, 2018). The two potential drivers are not mutually exclusive and could have a combined effect.…”

“…Specifically, the predominance of microorganismderived proteins and lipids are expected during the recession periods (Kallenbach et al, 2016;Kujawinski et al, 2016;Ding et al, 2018). Furthermore, the interactions of microorganisms with DOM can drive community succession (Li et al, 2013;Zhang et al, 2015;Wu et al, 2018). Previous investigations have indicated that aquifer-surface connection and recharge events are reflected in bacterial diversity and bacterial community composition (Kolehmainen et al, 2007;Li et al, 2012;Cooper et al, 2016;Hubalek et al, 2016).…”

The Contribution of Coniferous Canopy to the Molecular Diversity of Dissolved Organic Matter in Rainfall

“…These findings suggest that spatially heterogeneous molecular species in rainwater are converted into spatially homogeneous ones during the process where rainwater passes through the tree canopy of the conifer plantation and thereby dissolves and leaches plant-derived molecular species. Proteins are relatively labile and biodegradable compounds [37]. Given that the DOC flux and the number of proteins were much higher in throughfall than in rainfall, the spatially homogenized quality of throughfall water supports the indication of Qualls and Haines [10] that tree leaves leach readily-mineralisable DOM to the rainwater, which in turn can stimulate microbial activities in the forest floor.…”

Capturing the Diversity of Subsurface Microbiota – Choice of Carbon Source for Microcosm Enrichment and Isolation of Groundwater Bacteria

“…The small organic C only enriched a few phyla which are commonly isolated and already have diverse representative isolates (Figure 2). As the major naturally occurring C sources for microbes in the subsurface, sediment NOM are mixtures of heterogeneous organic substrates containing proteins, nucleic acids, lipids, carbohydrates, etc 41 . These undefined complex C support various subsurface bacteria in culture medium under laboratory condition, which may benefit for cultivation and isolation of key bacteria species from subsurface environment.…”

“…The sediment sample for NOM extraction was collected from a background well FW305 at ORR-FRC, at the depth of 0.3-1.1 m below ground surface. The potential bioavailable fraction of sediment NOM was extracted according to the method previously developed in our lab 28 . Briefly, the freeze-dried sediment sample was extracted with Milli-Q water via rotary shaking (170 rpm) overnight at 35 °C, and then sonicated in water bath for 2 hrs.…”