Microbial labilization and diversification of pyrogenic dissolved organic matter

Aleksandar I Goranov,Andrew R Zimmerman,Siddhartha Mitra,Kyle W Bostick,Patrick G Hatcher,Andrew S Wozniak

doi:10.5194/bg-19-1491-2022

Abstract

Abstract. With the increased occurrence of wildfires around the world, interest in the chemistry of pyrogenic organic matter (pyOM) and its fate in the environment has increased. Upon leaching from soils by rain events, significant amounts of dissolved pyOM (pyDOM) enter the aquatic environment and interact with microbial communities that are essential for cycling organic matter within the different biogeochemical cycles. To evaluate the biodegradability of pyDOM, aqueous extracts of laboratory-produced biochars were incubated with soil microbes, and the molecular changes to the composition of pyDOM were probed using ultrahigh-resolution mass spectrometry (Fourier transform–ion cyclotron resonance–mass spectrometry). Given that solar irradiation significantly affects the composition of pyDOM during terrestrial-to-marine export, the effects of photochemistry were also evaluated in the context of pyDOM biodegradability. Ultrahigh-resolution mass spectrometry revealed that many different (both aromatic and aliphatic) compounds were biodegraded. New labile compounds were produced, 22 %–40 % of which were peptide-like. These results indicated that a portion of pyDOM has been labilized into microbial biomass during the incubations. Fluorescence excitation–emission matrix spectra revealed that some fraction of these new bio-produced molecules is associated with proteinaceous fluorophores. Two-dimensional 1H–1H total correlation nuclear magnetic resonance (NMR) spectroscopy identified a peptidoglycan-like backbone within the microbially produced compounds. These results are consistent with previous observations of peptidoglycans within the soil and ocean nitrogen cycles where remnants of biodegraded pyDOM are expected to be observed. Interestingly, the exact nature of the bio-produced organic matter was found to vary drastically among samples indicating that the microbial consortium used may produce different exudates based on the composition of the initial pyDOM. Another potential explanation for the vast diversity of molecules is that microbes only consume low molecular-weight compounds, but they also produce reactive oxygen species (ROS), which initiate oxidative and recombination reactions that degrade high molecular-weight compounds and produce new molecules. Some of the bio-produced molecules (212–308 molecular formulas) were identified in estuarine and marine (surface and abyssal oceanic), and 81–192 of these formulas were of molecular composition attributed to carboxyl-rich alicyclic molecules (CRAM). These results indicate that some of the pyDOM biodegradation products have an oceanic fate and can be sequestered into the deep ocean. The observed microbially mediated diversification of pyDOM suggests that pyDOM contributes to the observed large complexity of natural organic matter observed in riverine and oceanic systems. More broadly, our research shows that pyDOM can be substrate for microbial growth and be incorporated into environmental food webs within the global carbon and nitrogen cycles.

Highlights

Pyrogenic organic matter, the carbonaceous solid residue that is left after biomass burning, has been gaining attention in recent years as an important active component of the global biogeochemical cycles
It is important to note that the electrospray ionization (ESI) source is prone to biases, and the analytical window of FT-ICR-MS depends most critically on it
This study probing the molecular changes occurring after biotic degradation of pyrogenic dissolved organic matter (pyDOM) revealed that soil microbes can effectively recycle and transform a significant portion of pyDOM molecules into labile microbial biomass

Summary

Introduction

Pyrogenic organic matter (pyOM), the carbonaceous solid residue that is left after biomass burning (e.g., wildfires, biochar production), has been gaining attention in recent years as an important active component of the global biogeochemical cycles. More and more studies report the presence of pyrogenic molecules in different aquatic environments (Hockaday et al, 2006; Dittmar and Paeng, 2009; Roebuck et al, 2017; Wagner et al, 2017; Li et al, 2019). These studies support the proposition that pyOM can be solubilized upon rain events and be leached as pyrogenic dissolved organic matter (pyDOM) resulting in large annual riverine fluxes of pyDOM from global riverine systems to the open ocean (Dittmar et al, 2012; Jaffé et al, 2013; Wang et al, 2016; Marques et al, 2017; Jones et al, 2020). Using laboratory-prepared biochars and conservative assumptions, Bostick et al (2018) approximated that > 85 % of the leached pyDOM is degradable (e.g., mineralizable to CO2), which indicates that pyDOM is a very active component within the global carbon cycle, as previously suggested (Druffel, 2004; Lehmann, 2007; Riedel et al, 2016)

Methods

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Discussion

Conclusion