Microbe-clay interactions as a mechanism for the preservation of organic matter and trace metal biosignatures in black shales
Introduction
The lithology of organic-rich, black shales consist of quartz, feldspars, carbonates, sulfides, clay minerals, and at least 1 wt% organic material (Arthur and Sageman, 1994, Aplin and Macquaker, 2011). The organic-rich nature of these rocks requires one of, or a combination of, the following conditions: (i) high primary production rates in the water column (Macquaker et al., 2010), (ii) sedimentation rates high enough to induce rapid burial of organic matter (Betts and Holland, 1991, Canfield, 1994, Tyson, 2001), and/or (iii) low organic matter respiration rates (Smith and Hollibaugh, 1993, Kristensen, 2000, Piper and Calvert, 2009). The latter can occur in several ways, including: (i) limited aerobic respiration due to low O2 penetration into the sediment (Kristensen, 2000); (ii) reduced anaerobic respiration due to a lack of pore-water sulfate (Canfield et al., 1993a, Canfield et al., 1993b); or (iii) the sorption of organic material onto clay particles in the water column preventing its degradation by heterotrophic bacteria (Pedersen and Calvert, 1990, Hedges and Keil, 1995, Ransom et al., 1997, Ransom et al., 1998, Bennett et al., 1999, Lünsdorf et al., 2000, Tyson, 2001, Kennedy et al., 2002, Macquaker et al., 2010, Aplin and Macquaker, 2011).
In recent years, black shale deposits have been studied extensively to interpret the seawater trace metal concentrations and redox state of the ancient oceans and atmosphere (e.g., Tribovillard et al., 2006, Anbar and Rouxel, 2007, Scott et al., 2008, Scott et al., 2013, Partin et al., 2013, Reinhard et al., 2013, Swanner et al., 2014). This is because the size of a given trace metal seawater reservoir is determined by the weathering flux from land and the relative influence of the sulfidic and oxic sinks (e.g., Algeo and Maynard, 2004, Scott et al., 2008). Moreover, the clay and organic fractions in these fine-grained sediments are highly reactive, and as such, they capture and preserve the trace element availability in the seawater from which the aggregates settled.
Planktonic cyanobacteria, such as Synechococcus and Prochlorococcus, are widely distributed throughout the ocean and can occur in cell densities ranging from 103 to 108 cells per milliliter, with the highest concentrations occurring during the summer months (e.g., Waterbury et al., 1979, Miyazono et al., 1992, Jacquet et al., 1998, Ohkouchi et al., 2006). They have been observed to contribute significantly to the carbon biomass of the water column, and in some cases, they constitute the majority of the biomass (Campbell et al., 1997). Indeed, biomarker analysis (indicating the presence of 2-methylhopanoids or their diagenetic derivatives, C35 homohopanoids) and stable carbon isotopic signatures suggest that cyanobacteria have been major contributors to shale deposition from the Neoproterozoic through to the Phanerozoic (Bechtel and Püttmann, 1997, Köster et al., 1998, Kuypers et al., 2004, Dumitrescu and Brassell, 2005, Olcott et al., 2005, Ohkouchi et al., 2006, Duque-Botero and Maurrasse, 2008, Kashiyama et al., 2008). Recent studies have also demonstrated that planktonic cyanobacterial cell surfaces are highly reactive (Lalonde et al., 2008a, Lalonde et al., 2008b, Liu et al., 2015) and thus capable of accumulating trace metals from solution (e.g., Dittrich and Sibler, 2005, Hadjoudja et al., 2010). That same reactivity has also been shown to facilitate the adsorption of detrital clay particles and the nucleation of authigenic clay phases (e.g., Konhauser et al., 1993, Konhauser et al., 1998). In this regard, we propose that live, planktonic cyanobacteria (and indeed any reactive microbial cell), such as Synechococcus, could increase clay flocculation, thereby facilitating more rapid deposition of cell-clay aggregates to the seafloor. If rapid burial promotes greater preservation of organic carbon, then this mechanism may very well underpin the formation and preservation of black shale deposits in the rock record, and explain their enrichment in trace metals (e.g. Calvert and Pedersen, 1993, Algeo and Maynard, 2004) as being sourced from the remnants of cell biomass. Furthermore, the increased preservation potential of these cell-clay aggregates suggests that the trace metal signatures of reactive bacterial biomass may become incorporated into the sediments over geologic time-scales.
We test this hypothesis by: (1) observing the depositional rates of Synechococcus in the presence of clay (kaolinite and montmorillonite); (2) assessing if clay deposition is influenced by cell metabolism; (3) determining the morphology of the clay-cell aggregates and their preservation potential; and ultimately (4) measuring the trace element composition of Synechococcus for the purpose of defining their contribution to the trace metal composition of black shales. These clays were chosen because they are common in near-shore, marine (kaolinite; Thiry, 2000) and fluvial/deltaic (montmorillonite; e.g., Taggart and Kaiser, 1960) environments and encompass both a 1:1 (kaolinite) and 2:1 (montmorillonite) tetrahedral structure. Importantly, these clays encompass a range of structural composition and environments of natural occurrence.
Section snippets
Culturing
Flocculation experiments (n = 18) were performed using Synechococcus sp. PCC 7002 (hereafter simply referred to as Synechococcus), a sheathless, planktonic, coccoid marine species. Axenic populations were grown in liquid A + media (Stevens and Porter, 1980), while stock populations were maintained on A + agar plates at 30 °C. Experimental cultures were grown in liquid media, shaken at 150 rpm and bubbled with filtered and humidified air (Chamot and Owttrim, 2000). Growth was monitored by measuring
Chl a measurements
Fig. 1 shows concentrations of the photosynthetic pigment Chl a over 18 successive 240-minute growth experiments with Synechococcus supplemented with either kaolinite or montmorillonite clay. Chl a concentration was used as a measure of cyanobacterial abundance remaining 5 cm below the water surface. In control samples (non-clay supplemented cultures), Chl a increased over time, as would be expected from the cells in exponential growth phase (Fig. 1), or, in the case of darkness, remained
Microbe-clay aggregation
Bacterial cells are negatively-charged over a wide range of pH due to the deprotonation of amphoteric organic ligands contained within the polymers of the cell walls (Flemming et al., 1990, Beveridge and Graham, 1991, Fein et al., 1997, Cox et al., 1999, Phoenix et al., 2002, Lalonde et al., 2008a, Lalonde et al., 2008b, Pokrovsky et al., 2008, Liu et al., 2015). These ligands bind metal cations and serve as nucleation sites for mineral authigenesis (Beveridge, 1989, Beveridge and Graham, 1991,
Conclusions
This study had a number of aims, one of which was to investigate the role that clay minerals have in flocculating microbial cells from suspension. The addition of montmorillonite or kaolinite (in 5 g/L or 50 g/L concentrations) to a suspension of Synechococcus cells was found to dramatically increase settling rates of both cells and clay; cells were brought out of suspension within 15 min. In contrast, live Synechococcus cells were found to increase in concentration when no clay was added. Cell
Acknowledgements
This research was made possible by support received from the Natural Sciences and Engineering Research Council of Canada (165831 and 213411). AB acknowledges the support from the Society of Independent Thinkers. The authors would like to thank the following people who contributed to the work: Sarah Schultz, Denise Whitford, and Schafer Montgomery. Additional thanks are due Guangcheng Chen, at the University of Alberta, who completed all ICP-MS measurements. The authors would like to thank
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- 1
Present address: Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada.
- 2
Present address: Earth Sciences Department, University of Toronto, Toronto, Ontario M5S 3B1, Canada.