Today, the metabolic activity of single-celled microorganisms, despite their small size, plays a major role in regulating global biogeochemical cycling, impacting nutrient availability, ocean and atmospheric chemistry, and climate.  Early in Earth’s history, the role of microbial ecosystems is likely to have been of even more importance.  Despite many decades of investigation, there are still many unanswered questions regarding microbial community organization and metabolism in a range of microbially dominated environments. Sulfur cycling, particularly the coupling between two important metabolisms (sulfate reduction and sulfide oxidation), is one of the dominant geochemical pathways within many diverse microbial ecosystems, the oxidative side of which is catalyzed through a number of distinct pathways, including photosynthetic and chemosynthetic microbes, as well as abiotic mechanisms. 

In this study, we used a multi-disciplinary, micro-scale approach, coupling geochemical and molecular biological investigation of closely coupled sulfur cycling in three distinctive, globally relevant microbial systems, which differ both in terms of their biological complexity and in the major sulfur cycling pathways, in an effort to resolve the mechanisms and possible biosignatures variations associated with biological sulfate-reduction coupled to various oxidative processes (i.e., anoxygenic and oxygenic biological oxidation and abiotic sulfide oxidation). The resulting research highlighted the value of the approach pursued here – measuring geochemical signatures at the micron spatial scale, which is most relevant to investigating the chemical conditions that drive (and in turn are impacted by) the metabolic activity of individual microbes.

The goals of this multi-disciplinary project centered on improving our understanding of microbial mat ecosystems and their associated metabolic activity through microscale geochemical and molecular investigations. We specifically investigated the spatial structure of microbial community organization and the role of environmental conditions and ambient chemistry in regulating both the types metabolic activity present in these environments and the specific rates of metabolic activity. In a series of papers focusing on carbon and sulfur cycling in these systems, we were able to gain significant insights into the spatial organization of different metabolisms in microbial ecosystems, including both carbon fixation (Houghton et al. 2014) and sulfur cycling (Wilbanks et al. 2014) pathways. 

One key outcome with regards to microbial sulfur cycling is the persistent existence of particular stable isotopic signatures, based on metabolism-specific preferences for different kinds of sulfur (e.g., ³²S or ³⁴S, sulfur atoms which contain the same number of protons, but different numbers of neutrons in the nucleus).  These isotope ‘biosignatures’ allow us to infer the spatial distribution and importance of different sulfur cycling metabolisms.  In microbial systems, we found a minimum in the isotopic differences between two sulfur species (sulfate and hydrogen sulfide) at the interface between oxic environments and anoxic (lacking oxygen) environments (Wilbanks et al. 2014). This suggests minimal activity of a particular metabolism known as sulfur disproportionation, which has been previously invoked as a key tracer of the increase in oxygen in the ocean-atmosphere system over Earth history (based on sulfur isotope measurements).  Instead, we infer that disproportionation was not a key metabolism driving the large-scale isotopic patterns in sulfur cycling associated with increasing oxygen levels.  Instead, these isotope signatures most likely reflect changes in organic matter availability (and carbon cycling) associated with increasingly oxic environment...

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