Benthic invaders control the phosphorus cycle in the world's largest freshwater ecosystem.

The productivity of aquatic ecosystems depends on the supply of limiting nutrients. The invasion of the Laurentian Great Lakes, the world's largest freshwater ecosystem, by dreissenid (zebra and quagga) mussels has dramatically altered the ecology of these lakes. A key open question is how dreissenids affect the cycling of phosphorus (P), the nutrient that limits productivity in the Great Lakes. We show that a single species, the quagga mussel, is now the primary regulator of P cycling in the lower four Great Lakes. By virtue of their enormous biomass, quagga mussels sequester large quantities of P in their tissues and dramatically intensify benthic P exchanges. Mass balance analysis reveals a previously unrecognized sensitivity of the Great Lakes ecosystem, where P availability is now regulated by the dynamics of mussel populations while the role of the external inputs of phosphorus is suppressed. Our results show that a single invasive species can have dramatic consequences for geochemical cycles even in the world's largest aquatic ecosystems. The ongoing spread of dreissenids across a multitude of lakes in North America and Europe is likely to affect carbon and nutrient cycling in these systems for many decades, with important implications for water quality management.

Biogeochemical and physical controls on methane fluxes from two ferruginous meromictic lakes.

Meromictic lakes with anoxic bottom waters often have active methane cycles whereby methane is generally produced biogenically under anoxic conditions and oxidized in oxic surface waters prior to reaching the atmosphere. Lakes that contain dissolved ferrous iron in their deep waters (i.e., ferruginous) are rare, but valuable, as geochemical analogues of the conditions that dominated the Earth's oceans during the Precambrian when interactions between the iron and methane cycles could have shaped the greenhouse regulation of the planet's climate. Here, we explored controls on the methane fluxes from Brownie Lake and Canyon Lake, two ferruginous meromictic lakes that contain similar concentrations (max. >1 mM) of dissolved methane in their bottom waters. The order Methanobacteriales was the dominant methanogen detected in both lakes. At Brownie Lake, methanogen abundance, an increase in methane concentration with respect to depths closer to the sediment, and isotopic data suggest methanogenesis is an active process in the anoxic water column. At Canyon Lake, methanogenesis occurred primarily in the sediment. The most abundant aerobic methane-oxidizing bacteria present in both water columns were associated with the Gammaproteobacteria, with little evidence of anaerobic methane oxidizing organisms being present or active. Direct measurements at the surface revealed a methane flux from Brownie Lake that was two orders of magnitude greater than the flux from Canyon Lake. Comparison of measured versus calculated turbulent diffusive fluxes indicates that most of the methane flux at Brownie Lake was non-diffusive. Although the turbulent diffusive methane flux at Canyon Lake was attenuated by methane oxidizing bacteria, dissolved methane was detected in the epilimnion, suggestive of lateral transport of methane from littoral sediments. These results highlight the importance of direct measurements in estimating the total methane flux from water columns, and that non-diffusive transport of methane may be important to consider from other ferruginous systems.

Organic sulfur was integral to the Archean sulfur cycle.

The chemistry of the Early Earth is widely inferred from the elemental and isotopic compositions of sulfidic sedimentary rocks, which are presumed to have formed globally through the reduction of seawater sulfate or locally from hydrothermally supplied sulfide. Here we argue that, in the anoxic Archean oceans, pyrite could form in the absence of ambient sulfate from organic sulfur contained within living cells. Sulfides could be produced through mineralization of reduced sulfur compounds or reduction of organic-sourced sulfite. Reactive transport modeling suggests that, for sulfate concentrations up to tens of micromolar, organic sulfur would have supported 20 to 100% of sedimentary pyrite precipitation and up to 75% of microbial sulfur reduction. The results offer an alternative explanation for the low range of δ34S in Archean sulfides, and raise a possibility that sulfate scarcity delayed the evolution of dissimilatory sulfate reduction until the initial ocean oxygenation around 2.7 Ga.

Sedimentary sulfur isotopes and Neoarchean ocean oxygenation.

Abrupt disappearance of mass-independent fractionation of sulfur isotopes (MIF-S) from the geologic record and an apparent ingrowth in seawater sulfate around 2.45 billion years ago (Ga) signal the first large-scale oxygenation of the atmosphere [the Great Oxygenation Event (GOE)]. Pre-GOE O2 production is evident from multiple other terrestrial and marine proxies, but oceanic O2 concentrations remain poorly constrained. Furthermore, current interpretations of S isotope records do not explain a concurrent expansion in the range of both MIF-S-diagnostic for low atmospheric O2-and δ34S beginning at 2.7 Ga. To address these unknowns, we developed a reaction-transport model to analyze the preservation patterns of sulfur isotopes in Archean sedimentary pyrites, one of the most robust and widely distributed proxies for early Earth biogeochemistry. Our modeling, paradoxically, reveals that micromolar levels of O2 in seawater enhance the preservation of large MIF-S signals, whereas concomitant ingrowth of sulfate expands the ranges in pyrite δ34S. The 2.7- to 2.45-Ga expansion in both Δ33S and δ34S ranges thus argues for a widespread and protracted oxygenation of seawater, at least in shallow marine environments. At the micromolar levels predicted, the surface oceans would support a strong flux of O2 to the atmosphere, where O2 sinks balanced these fluxes until the GOE. This microoxic seawater would have provided habitat for early aerobic microorganisms and supported a diversity of new O2-driven biogeochemical cycles in the Neoarchean.

Novel anammox bacteria and nitrogen loss from Lake Superior.

Anaerobic ammonium oxidizing (anammox) bacteria own a central position in the global N-cycle, as they have the ability to oxidize NH4+ to N2 under anoxic conditions using NO2-. They are responsible for up to 50% of all N2 released from marine ecosystems into the atmosphere and are thus indispensible for balancing the activity of N-fixing bacteria and completing the marine N-cycle. The contribution, diversity, and impact of anammox bacteria in freshwater ecosystems, however, is largely unknown, confounding assessments of their role in the global N-cycle. Here we report the activity and diversity of anammox bacteria in the world's largest freshwater lake-Lake Superior. We found that anammox performed by previously undiscovered bacteria is an important contributor to sediment N2 production. We observed striking differences in the anammox bacterial populations found at different locations within Lake Superior and those described from other locations. Our data thus reveal that novel anammox bacteria underpin N-loss from Lake Superior, and if more broadly distributed across inland waters would play an important role in continental N-cycling and mitigation of fixed nitrogen transfer from land to the sea.

Integrating biogeochemistry with multiomic sequence information in a model oxygen minimum zone.

Microorganisms are the most abundant lifeform on Earth, mediating global fluxes of matter and energy. Over the past decade, high-throughput molecular techniques generating multiomic sequence information (DNA, mRNA, and protein) have transformed our perception of this microcosmos, conceptually linking microorganisms at the individual, population, and community levels to a wide range of ecosystem functions and services. Here, we develop a biogeochemical model that describes metabolic coupling along the redox gradient in Saanich Inlet-a seasonally anoxic fjord with biogeochemistry analogous to oxygen minimum zones (OMZs). The model reproduces measured biogeochemical process rates as well as DNA, mRNA, and protein concentration profiles across the redox gradient. Simulations make predictions about the role of ubiquitous OMZ microorganisms in mediating carbon, nitrogen, and sulfur cycling. For example, nitrite "leakage" during incomplete sulfide-driven denitrification by SUP05 Gammaproteobacteria is predicted to support inorganic carbon fixation and intense nitrogen loss via anaerobic ammonium oxidation. This coupling creates a metabolic niche for nitrous oxide reduction that completes denitrification by currently unidentified community members. These results quantitatively improve previous conceptual models describing microbial metabolic networks in OMZs. Beyond OMZ-specific predictions, model results indicate that geochemical fluxes are robust indicators of microbial community structure and reciprocally, that gene abundances and geochemical conditions largely determine gene expression patterns. The integration of real observational data, including geochemical profiles and process rate measurements as well as metagenomic, metatranscriptomic and metaproteomic sequence data, into a biogeochemical model, as shown here, enables holistic insight into the microbial metabolic network driving nutrient and energy flow at ecosystem scales.

Sulfate was a trace constituent of Archean seawater.

In the low-oxygen Archean world (>2400 million years ago), seawater sulfate concentrations were much lower than today, yet open questions frustrate the translation of modern measurements of sulfur isotope fractionations into estimates of Archean seawater sulfate concentrations. In the water column of Lake Matano, Indonesia, a low-sulfate analog for the Archean ocean, we find large (>20 per mil) sulfur isotope fractionations between sulfate and sulfide, but the underlying sediment sulfides preserve a muted range of δ(34)S values. Using models informed by sulfur cycling in Lake Matano, we infer Archean seawater sulfate concentrations of less than 2.5 micromolar. At these low concentrations, marine sulfate residence times were likely 10(3) to 10(4) years, and sulfate scarcity would have shaped early global biogeochemical cycles, possibly restricting biological productivity in Archean oceans.

Recent warming of lake Kivu.

Lake Kivu in East Africa has gained notoriety for its prodigious amounts of dissolved methane and dangers of limnic eruption. Being meromictic, it is also expected to accumulate heat due to rising regional air temperatures. To investigate the warming trend and distinguish between atmospheric and geothermal heating sources, we compiled historical temperature data, performed measurements with logging instruments, and simulated heat propagation. We also performed isotopic analyses of water from the lake's main basin and isolated Kabuno Bay. The results reveal that the lake surface is warming at the rate of 0.12°C per decade, which matches the warming rates in other East African lakes. Temperatures increase throughout the entire water column. Though warming is strongest near the surface, warming rates in the deep waters cannot be accounted for solely by propagation of atmospheric heat at presently assumed rates of vertical mixing. Unless the transport rates are significantly higher than presently believed, this indicates significant contributions from subterranean heat sources. Temperature time series in the deep monimolimnion suggest evidence of convection. The progressive deepening of the depth of temperature minimum in the water column is expected to accelerate the warming in deeper waters. The warming trend, however, is unlikely to strongly affect the physical stability of the lake, which depends primarily on salinity gradient.

Photoferrotrophs thrive in an Archean Ocean analogue.

Considerable discussion surrounds the potential role of anoxygenic phototrophic Fe(II)-oxidizing bacteria in both the genesis of Banded Iron Formations (BIFs) and early marine productivity. However, anoxygenic phototrophs have yet to be identified in modern environments with comparable chemistry and physical structure to the ancient Fe(II)-rich (ferruginous) oceans from which BIFs deposited. Lake Matano, Indonesia, the eighth deepest lake in the world, is such an environment. Here, sulfate is scarce (<20 micromol x liter(-1)), and it is completely removed by sulfate reduction within the deep, Fe(II)-rich chemocline. The sulfide produced is efficiently scavenged by the formation and precipitation of FeS, thereby maintaining very low sulfide concentrations within the chemocline and the deep ferruginous bottom waters. Low productivity in the surface water allows sunlight to penetrate to the >100-m-deep chemocline. Within this sulfide-poor, Fe(II)-rich, illuminated chemocline, we find a populous assemblage of anoxygenic phototrophic green sulfur bacteria (GSB). These GSB represent a large component of the Lake Matano phototrophic community, and bacteriochlorophyll e, a pigment produced by low-light-adapted GSB, is nearly as abundant as chlorophyll a in the lake's euphotic surface waters. The dearth of sulfide in the chemocline requires that the GSB are sustained by phototrophic oxidation of Fe(II), which is in abundant supply. By analogy, we propose that similar microbial communities, including populations of sulfate reducers and photoferrotrophic GSB, likely populated the chemoclines of ancient ferruginous oceans, driving the genesis of BIFs and fueling early marine productivity.

Autocatalytic model of oscillatory zoning in experimentally grown (Ba,Sr)SO4 solid solution.

Oscillatory zoning (OZ) is a phenomenon common to many natural minerals whereby the mineral composition varies more or less regularly from the core of the crystal to its rim. Oscillatory zoned barite-celestite (Ba,Sr)SO4 crystals are one of the very few examples of the OZ phenomenon that were obtained under controlled laboratory conditions. It is known that such crystals can be synthesized by precipitation from an aqueous solution during counterdiffusion in a gel column connecting two reservoirs. We present here a model of oscillatory zoning in such a binary solid solution grown from an aqueous solution. By expanding on a previously suggested model, we obtain oscillatory dynamical solutions for two limit cases: the growth of a flat crystal face and the growth of a spherical crystallite. We consider an autocatalytic dependence between the crystal growth rate and the crystal surface composition. The oscillatory patterns then arise as a kinetic effect due to the coupling between the diffusion field around the crystal and the fast crystal growth under far-from-equilibrium conditions. The effects of fluctuations in the aqueous solution concentrations are also considered. It is shown that they may lead to noisy oscillatory patterns.