Authigenic metastable iron sulfide minerals preserve microbial organic carbon in anoxic environments
Introduction
The burial of organic carbon (OC) in the sedimentary record over geologic time governs CO2 levels at the surface of modern Earth (Garrels and Perry, 1974; Berner, 1982; Burdige, 2007). Photosynthetic organisms fix CO2 at the surface of the ocean to produce OC, which is respired back to CO2 by heterotrophic microorganisms in the water column. Less than 1% of the OC produced at the surface escapes degradation and reaches the sediment, where it is further subjected to microbial decomposition (Burdige, 2007). Even though active aerobic microbial communities inhabit over a third of the global seafloor (D’Hondt et al., 2015), OC transformations in marine sediments are mainly driven by anaerobic microbial processes (Jørgensen, 1982; Canfield, 1989, 1994). Despite the generally efficient remineralization of OC by microbial processes in sediments, some OC is ultimately preserved and buried over timescales of millenia and longer (Baldock et al., 2004). The greatest sedimentary OC burial occurs along marine continental margins (Berner, 1982; Burdige, 2007; Keil, 2017) and is attributable to high sedimentation rates, to the presence of oxygen minimum zones in the overlying water that minimizes OC degradation during transport, and to the decrease in OC reactivity with increasing depth (Canfield, 1994; Hedges and Keil, 1995; Hartnett et al., 1998; Wakeham and Canuel, 2006; Arndt et al., 2013; Keil, 2017). Moreover, interactions between OC and terrigenous minerals during transport to and deposition on the seabed further lead to the preservation of OC in sediments (Hedges et al., 2001; Keil and Mayer, 2014). Specifically, sorption of OC to mineral surfaces can minimize biological and chemical degradation by slowing down remineralization, stabilizing organic molecules and preserving labile molecules in marine sediments (Hedges and Keil, 1995; Keil and Mayer, 2014). Because OC in sediments is often physically associated with clays and oxy-hydroxides (Ransom et al., 1997, 1999), the flux of minerals to coastal zones is assumed to be the predominant factor determining the amount of organic matter preserved in coastal sediments (Keil et al., 1994).
The role of authigenic mineral formation in the presence of microorganisms (in situ biomineralization) in preserving OC has been far less studied. Iron and manganese oxides precipitated during in situ biomineralization by Fe(II)-oxidizing and Mn(II)-oxidizing microorganisms, respectively, incorporate and preserve organic molecules in suboxic (<10 μM O2) and oxic environments (Chan et al., 2004, 2009; Estes et al., 2017). These metal oxides are stable over time at ambient conditions and are resistant to diagenetic alteration (Krepski et al., 2013; Picard et al., 2015; Estes et al., 2017). The role of in situ biomineralization in the preservation of organic carbon in anoxic environments, however, remains unknown. It has been observed that OC and iron sulfide minerals are often buried together in anoxic sediments (Berner, 1982; Berner and Raiswell, 1983), which begs the question as to whether direct organo-mineral interactions can form during authigenic iron sulfide mineral formation and participate in the preservation of OC. Iron sulfide minerals precipitate in anoxic environments where dissolved sulfide produced by sulfate-reducing microorganisms (SRM) interacts with soluble ferrous iron Fe(II) (Rickard, 2012c). Microbial sulfate reduction drives the biogeochemical sulfur cycle in a variety of sedimentary environments (Zopfi et al., 2004; Raven et al., 2016; Riedinger et al., 2017; Wehrmann et al., 2017; Shawar et al., 2018; Jørgensen et al., 2019). The complexities of the sulfur cycle, as well as the challenges of determining the composition of bulk organic matter, have limited our capacity to address critical questions about the relationship between the activity of SRM and the preservation of OC. Sulfide can react with organic matter via sulfurization to facilitate OC preservation (Sinninghe Damste and De Leeuw, 1990; Werne et al., 2004; Amrani, 2014; Raven et al., 2016). In this study, we investigated the potential for iron sulfide biomineralization to be a pathway for OC preservation.
Iron sulfide mineral formation has been extensively studied under abiotic conditions, but the specific role of microorganisms on the formation of iron sulfide minerals under anoxic conditions has only recently been explored (Picard et al., 2016a; Gorlas et al., 2018; Picard et al., 2018; Stanley and Southam, 2018; Mansor et al., 2019; Thiel et al., 2019). Microbial sulfate reduction is more than just the production of sulfide (Schoonen, 2004). Sulfate-reducing bacteria act as templates for the nucleation and growth of mackinawite and greigite, and influence the physical characteristics – particle size and aggregation – of these metastable iron sulfide minerals (Picard et al., 2018). Microbial sulfate reduction accounts for half of the oxidation of organic matter in anoxic marine sediments (Jørgensen, 1982), however, during this process SRM can also generate variable amounts of biomass and/or release organic molecules extracellularly, that can potentially associate with authigenic iron sulfide minerals. The heavy encrustation of SRM by iron sulfides, as reported in environment samples and in laboratory experiments (Ferris et al., 1987; Picard et al., 2016a, 2018), suggests that SRM might play an active role in associating Fe-S minerals and OC. In this study, we used scanning electron microscopy (SEM) with electron dispersive X-ray spectrometry (EDS), and scanning transmission X-ray microscopy (STXM) combining near-edge X-ray absorption fine structure (NEXAFS) spectroscopy with high resolution, and demonstrated that that organic compounds derived from microbial biomass associate with iron sulfide minerals when those were formed in the presence of both live and dead sulfate-reducing bacteria. The association of OC with authigenic, biogenic iron sulfide minerals potentially results in the effective preservation of organic matter in anoxic environments, which has marked, globally relevant implications for the fate of buried OC in past and modern Earth. Ultimately, the physical and chemical characteristics of iron sulfide biominerals could also be indicative parameters of depositional conditions, additionally to geochemical parameters such as sulfur isotopes and trace metal compositions of pyrite (Gregory et al., 2015; Large et al., 2017; Gregory et al., 2019).
Section snippets
Culture medium
Iron sulfide minerals were precipitated in an anoxic marine medium used for the cultivation of sulfate-reducing microorganisms (Widdel and Bak, 1992). The medium composition is given in Suppl. Table A1 (DSMZ medium 195c). The complete experimental procedure describing how to produce strict anoxic conditions was described elsewhere (Picard et al., 2018). A summary of the medium preparation is given here. The complete medium was prepared by mixing a mineral solution, a bicarbonate buffer
Composition of biogenic iron sulfide minerals
Fe, S, C and O were detected in all mineral aggregates precipitated in the presence of live and dead cells of the sulfate-reducing bacterium Desulfovibrio hydrothermalis AM13 (Fig. 1A). In comparison, only traces of O and no C were detected in abiotic mineral aggregates precipitated in the culture medium containing lactate (Fig. 1A). The strong Si signal observed in Fig. 1A originated from the Si wafer onto which the minerals were deposited. Fe and S were from mackinawite (FeS) that formed in
Preservation of labile OC by metastable iron sulfide minerals in anoxic conditions
Labile organic molecules were incorporated in iron sulfide minerals during their formation in the presence of live SRM and this association persisted for at least two years. Lactate was the only source of OC at the beginning of biotic experiments with live cells. Cell concentration increased from 106 cells/ml to 108 cells/ml within one week, concomitantly with the production of sulfide and mineral precipitation (Picard et al., 2018). No OC was detected in association with abiotic minerals
Conclusion
Iron sulfide minerals are central to our understanding of Earth’s past and modern biogeochemical cycles. This study demonstrates the concomitant precipitation of iron sulfide minerals with OC under anoxic conditions and the importance of iron sulfide minerals as reservoir for the preservation of OC in anoxic sediments. Future studies should aim to closer approximate natural conditions, where the biomass produced is much lower than in culture conditions (e.g. a few orders of magnitude in cell
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We would like to thank the editor and two reviewers for helping to improve the manuscript significantly. This work was performed in part at the Center for Nanoscale Systems (CNS), a member of the National Nanotechnology Coordinated Infrustructure Network (NNCI), which is supported by the National Science Foundation under NSF award no. 1541959. CNS is part of Harvard University. We thank the Harvard Center for Biological Imaging for infrastructure and support. We thank Shao-Liang Zheng for
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- 1
Present address: School of Life Sciences, University of Nevada Las Vegas, Las Vegas NV 89154, USA
- 2
Present address: Pacific Coastal and Marine Science Center, U.S. Geological Survey, Santa Cruz, CA 95060, USA
- 3
Present address: Department of Geosciences, The Pennsylvania State University, University Park, PA 16801, USA