Acid-Tolerant Sulfate-Reducing Bacteria Play a Major Role in Iron Cycling in Acidic Iron Rich Sediments

Climate change drives drying and acidification of many rivers and lakes. Abundant sedimentary iron in these systems oxidizes chemically and biologically to form iron-ox(yhydrox)ide crusts and "hardpans". Given generally high sulfate concentrations, the mobilization and cycling of iron in these environments can be strongly influenced by bacterial sulfate reduction. Sulfate-reducing bacteria (SRB) induce reductive dissolution of oxidized iron phases by producing the reductant bisulfide as a metabolic product. These environmentally ubiquitous microbes also recycle much of the fixed carbon in sediment-hosted microbial mat communities. With prevalent drying, the buffering capacity for protons liberated from iron oxidation is exceeded, and the activity of sulfate-reducers is restricted to those species capable of tolerating low pH (and generally highly saline, i.e. sulfate-rich) conditions. These species will sustain the recycling of iron from more crystalline phases to more bioavailable species, as well as act as the only source of bisulfide for photosynthesizing microbial communities. The phylogeny and physiology of acid-tolerant SRB is therefore important to Fe, S and C cycling in iron-rich sedimentary environments, particularly those on a geochemical trajectory towards acidification. Previous studies have shown that these SRB species tend to be highly novel. We studied two distinct environments along a geochemical continuum towards acidification. In both settings, iron redox transformations exert a major, if not controlling, influence on reduction potential. An acidified, iron- rich tidal marsh receiving acid-mine drainage (San Francisco Bay, CA, USA) contained abundant textural evidence for reductive dissolution of Fe(III) in sediments with pH values varying from 2.4 - 3.8. From these sediments, full-length novel dsrAB gene sequences from acid-tolerant SRB were recovered, and sulfur isotope profiles reflected biological fractionation of sulfur under even the most acidic conditions. The dsrAB genes are related to other novel SRB lineages derived from acidic environments in previous reports, suggesting that these species have adapted to the acidity rather than colonized more circumneutral microenvironments. In an acidic hypersaline lake system in NW Victoria (Australia), previous studies suggested that pore water bisulfide derived from anoxic groundwater transported from distal locations. However, isolated potholes of oxic Fe(III)-rich springwater exhibited nearly a two-fold increase in conductivity and pH increase from 4.5 to 8.0 over time periods on the order of days; and biogeochemical and mineralogical observations were consistent with the presence of active acid- and halo-tolerant SRB. Furthermore, stratified active microbial mat communities, with zones of black FeS formation localized several millimeters below the sediment-air interface, were identified in cross-section from lakeshore sediments near groundwater discharge springs. Culture-independent and culture-based work to characterize the SRB population is ongoing at this site. We infer, from previous sulfur isotope tracer experiments at the lake, that overall sulfate reduction rates may be slow, but are nonetheless proceeding and contributing to the recycling of oxidized iron to a significant degree given the abundance of sulfate evidenced by widespread gypsum precipitation. We conclude from the two study-sites described above that acid-tolerant SRB species play an important role in the linked S, Fe and C cycles in acidifying, iron-rich environments, and their phylogenetic and physiological diversity should be further investigated.