Nutrient Acquisition and the Metabolic Potential of Photoferrotrophic Chlorobi

Anoxygenic photosynthesis evolved prior to oxygenic photosynthesis and harnessed energy from sunlight to support biomass production on the early Earth. Models that consider the availability of electron donors predict that anoxygenic photosynthesis using Fe(II), known as photoferrotrophy, would have supported most global primary production before the proliferation of oxygenic phototrophs at approximately 2.3 billion years ago. These photoferrotrophs have also been implicated in the deposition of banded iron formations, the world’s largest sedimentary iron ore deposits that formed mostly in late Archean and early Proterozoic Eons. In this work we present new data and analyses that illuminate the metabolic capacity of photoferrotrophy in the phylum Chlorobi. Our laboratory growth experiments and biochemical analyses demonstrate that photoferrotrophic Chlorobi are capable of assimilatory sulfate reduction and nitrogen fixation under sulfate and nitrogen limiting conditions, respectively. Furthermore, the evolutionary histories of key enzymes in both sulfur (CysH and CysD) and nitrogen fixation (NifDKH) pathways are convoluted; protein phylogenies, however, suggest that early Chlorobi could have had the capacity to assimilate sulfur and fix nitrogen. We argue, then, that the capacity for photoferrotrophic Chlorobi to acquire these key nutrients enabled them to support primary production and underpin global biogeochemical cycles in the Precambrian

Oxidative elemental cycling under the low O₂ Eoarchean atmosphere

The Great Oxidation Event signals the first large-scale oxygenation of the atmosphere roughly 2.4 Gyr ago. Geochemical signals diagnostic of oxidative weathering, however, extend as far back as 3.3–2.9 Gyr ago. 3.8–3.7 Gyr old rocks from Isua, Greenland stand as a deep time outpost, recording information on Earth’s earliest surface chemistry and the low oxygen primordial biosphere. Here we find fractionated Cr isotopes, relative to the igneous silicate Earth reservoir, in metamorphosed banded iron formations (BIFs) from Isua that indicate oxidative Cr cycling 3.8–3.7 Gyr ago. Elevated U/Th ratios in these BIFs relative to the contemporary crust, also signal oxidative mobilization of U. We suggest that reactive oxygen species were present in the Eoarchean surface environment, under a very low oxygen atmosphere, inducing oxidative elemental cycling during the deposition of the Isua BIFs and possibly supporting early aerobic biology

Mixing and its effects on biogeochemistry in the persistently stratified, deep, tropical Lake Matano, Indonesia

This is the publisher's version, also available electronically from http://www.aslo.orgIn the > 590-m deep, tropical Lake Matano (Indonesia), stratification is characterized by weak thermal gradients (< 2°C per 500 m) and weak salinity gradients (< 0.14% per 500 m). These gradients persist over seasons, decades, and possibly centuries. Under these nearly steady-state conditions, vertical eddy diffusion coefficients (Kz) cannot be estimated by conventional methods that rely on time derivatives of temperature distributions. We use and compare several alternative methods: one-dimensional k-ε modeling, three-dimensional hydrodynamic modeling, correlation with the size of Thorpe instabilities, and correlation with the stability frequency. In the thermocline region, at 100-m depth, the Kz is ~ 5 × 10-6 m2 s-1, but, below 300 m, the small density gradient results in large (20 m) vertical eddies and high mixing rates (Kz ~ 10-2 m2 s-1). The estimated timescale of water renewal in the monimolimnion is several hundred years. Intense evaporation depletes the surface mixed layer of 16O and 1H isotopes, making it isotopically heavier. The lake waters become progressively isotopically lighter with depth, and the isotopic composition in the deep waters is close to those of the ground and tributary waters. The vertical distribution of Kz is used in a biogeochemical reaction-transport model. We show that, outside of a narrow thermocline region, the vertical distributions of dissolved oxygen, iron, methane, and phosphorus are shaped by vertical variations in transport rates, rather than by sources or sinks

A Mg(OH)2 coprecipitation method for determining chromium speciation and isotopic composition in seawater

Chromium (Cr) stable isotopes have emerged as a powerful tool for tracking environmental redox transfor- mations. This is because Cr isotopes are fractionated during redox reactions between Cr(III) and Cr(VI). In order to fully exploit the information recorded within Cr isotope compositions, we must be able to track changes in Cr speciation throughout the environment and, in particular, the changes in speciation between input to the ocean and eventual deposition in sediments. We must also be able to access the isotope compositions of each Cr species, rather than only total dissolved Cr. We have thus developed a magnesium hydroxide coprecipitation method that meets these objectives. This method achieves complete recovery and has a typical precision on concentration measurements of !8% (1σ). It was tested using seawater collected from Saanich Inlet, a persis- tently anoxic fjord on the Pacific coast of Canada. Chromium speciation profiles and proof-of-concept isotope ratio measurements on selected samples indicate that isotopically lighter Cr(III) can be isolated from coexisting isotopically heavier Cr(VI), effectively resolving species-specific Cr isotope compositions. While the oxygenated surface waters of Saanich Inlet follow the generally observed correlation between seawater Cr concentration and its isotopic composition, seawater from anoxic depths diverges from this array, indicating that different pro- cesses are responsible for setting the isotope composition of these deeper waters. Broader application of Mg(OH)2 coprecipitation has strong potential to yield new insights into the fractionation of Cr isotopes in the oceans and the pathways that ultimately set the Cr isotopic composition of marine sediments and sedimentary archives

The biogeochemistry of tropical lakes: A case study from Lake Matano, Indonesia

This is the publisher's version, also available electronically from http://onlinelibrary.wiley.comWe examined the chemical composition of the water column of Lake Matano, Sulawesi Island, Indonesia, to document how the high abundances of Fe (hydr)oxides in tropical soils and minimal seasonal temperature variability affect biogeochemical cycling in lakes. Lake Matano exhibits weak thermal stratification, yet a persistent pycnocline separates an oxic epilimnion from anoxic meta- and hypolimnions. The concentration of soluble P in the epilimnetic waters is very low and can be attributed to scavenging by Fe (hydr)oxides. Chromium concentrations in the epilimnion are high (up to 180 nmol L−1), but below U.S. Environmental Protection Agency guidelines for aquatic ecosystems. The concentration of chromium decreases sharply across the oxic-anoxic boundary, revealing that the hypolimnion is a sink for Cr. Flux calculations using a one-dimensional transportreaction model for the water column fail to satisfy mass balance requirements and indicate that sediment transport and diagenesis play an important role in the exchange of Fe, Mn, P, and Cr between the epilimnion and hypolimnion. Exchange of water between the epilimnion and hypolimnion is slow and on a time scale similar to temperate meromictic lakes. This limits recycling of P and N to the epilimnion and removal of Cr to the hypolimnion, both of which likely restrict primary production in the epilimnion. Owing to the slow exchange, steep concentration gradients in Fe and Mn species develop in the metalimnion. These concentration gradients are conducive to the proliferation of chemoautotrophic and anoxygenic phototrophic microbial communities, which may contribute a significant fraction to the total primary production in the lake

Biogeochemistry of manganese in ferruginous Lake Matano, Indonesia

This study explores Mn biogeochemistry in a stratified, ferruginous lake, a modern analogue to ferruginous oceans. Intense Mn cycling occurs in the chemocline where Mn is recycled at least 15 times before sedimentation. The product of biologically catalyzed Mn oxidation in Lake Matano is birnessite. Although there is evidence for abiotic Mn reduction with Fe(II), Mn reduction likely occurs through a variety of pathways. The flux of Fe(II) is insufficient to balance the reduction of Mn at 125 m depth in the water column, and Mn reduction could be a significant contributor to CH&lt;sub&gt;4&lt;/sub&gt; oxidation. By combining results from synchrotron-based X-ray fluorescence and X-ray spectroscopy, extractions of sinking particles, and reaction transport modeling, we find the kinetics of Mn reduction in the lake's reducing waters are sufficiently rapid to preclude the deposition of Mn oxides from the water column to the sediments underlying ferruginous water. This has strong implications for the interpretation of the sedimentary Mn record

Sampling and Processing Methods Impact Microbial Community Structure and Potential Activity in a Seasonally Anoxic Fjord: Saanich Inlet, British Columbia

The Scientific Committee on Oceanographic Research (SCOR) Working Group 144 Microbial Community Responses to Ocean Deoxygenation workshop held in Vancouver, B.C on July 2014 had the primary objective of initiating a process to standardize operating procedures for compatible process rate and multi-omic (DNA, RNA, protein, and metabolite) data collection in marine oxygen minimum zones and other oxygen depleted waters. Workshop attendees participated in practical sampling and experimental activities in Saanich Inlet, British Columbia, a seasonally anoxic fjord. Experiments were designed to compare and cross-calibrate in situ versus bottle sampling methods to determine effects on microbial community structure and potential activity when using different filter combinations, filtration methods, and sample volumes. Resulting biomass was preserved for small subunit ribosomal RNA (SSU or 16S rRNA) and SSU rRNA gene (rDNA) amplicon sequencing followed by downstream statistical and visual analyses. Results from these analyses showed that significant community shifts occurred between in situ versus on ship processed samples. For example, Bacteroidetes, Alphaproteobacteria, and Opisthokonta associated with on-ship filtration onto 0.4 μm filters increased fivefold compared to on-ship in-line 0.22 μm filters or 0.4 μm filters processed and preserved in situ. In contrast, Planctomycetes associated with 0.4 μm in situ filters increased fivefold compared to on-ship filtration onto 0.4 μm filters and on-ship in-line 0.22 μm filters. In addition, candidate divisions and Chloroflexi were primarily recovered when filtered onto 0.4 μm filters in situ. Results based on rRNA:rDNA ratios for microbial indicator groups revealed previously unrecognized roles of candidate divisions, Desulfarculales, and Desulfuromandales in sulfur cycling, carbon fixation and fermentation within anoxic basin waters. Taken together, filter size and in situ versus on-ship filtration had the largest impact on recovery of microbial groups with the potential to influence downstream metabolic reconstruction and process rate measurements. These observations highlight the need for establishing standardized and reproducible techniques that facilitate cross-scale comparisons and more accurately assess in situ activities of microbial communities

Rates and Pathways of N2 Production in a Persistently Anoxic Fjord: Saanich Inlet, British Columbia

Marine oxygen minimum zones (OMZs) support 30–50% of global fixed-nitrogen (N) loss but comprise only 7% of total ocean volume. This N-loss is driven by canonical denitrification and anaerobic ammonium oxidation (anammox), and the distribution and activity of these two processes vary greatly in space and time. Factors that regulate N-loss processes are complex, including organic matter availability, oxygen concentrations, and NO2− and NH4+ concentrations. While both denitrification and anammox produce N2, the overall geochemical outcome of these processes are different, as incomplete denitrification, for example, produces N2O, which is a potent greenhouse gas. Information on rates of anammox and denitrification and more detailed ecophysiological knowledge of the microorganisms catalyzing these processes are needed to develop more robust models of N-loss in OMZs. To this end, we conducted monthly incubations with 15N-labeled N during under anoxic conditions and during a deep water renewal cycle in Saanich Inlet, British Columbia, a persistently anoxic fjord. Both denitrification and anammox operated throughout the low oxygen water column with depth integrated rates of anammox and denitrification ranging from 0.15 ± 0.03 to 3.4 ± 0.3 and 0.02 ± 0.006 to 14 ± 2 mmol N2 m−2 d−1, respectively. Most N2 production in Saanich Inlet was driven by denitrification, with high rates developing in response to enhanced substrate supply from deep water renewal. Dynamics in rates of denitrification were linked to shifts in microbial community composition. Notably, periods of intense denitrification were accompanied by blooms in an Arcobacter population against a background community dominated by SUP05 and Marinimicrobia. Rates of N2 production through denitrification and anammox, and their dynamics, were then explored through flux-balance modeling with higher rates of denitrification linked to the physiology of substrate uptake. Overall, both denitrification and anammox operated throughout the year, contributing to an annual N-loss of 2 × 10−3 Tg N2 yr−1, 37% of which we attribute to anammox and 63% to complete denitrification. Extrapolating these rates from Saanich Inlet to all similar coastal inlets in BC (2478 km2), we estimate that these inlets contribute 0.1% to global pelagic N-loss