Cédric Magen

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 μmol·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 lakes 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.

The methane cycle in ferruginous Lake Matano

In Lake Matano, Indonesia, the worlds largest known ferruginous basin, more than 50% of authigenic organic matter is degraded through methanogenesis, despite high abundances of Fe (hydr)oxides in the lake sediments. Biogenic CH₄ accumulates to high concentrations (up to 1.4 mmol L⁻¹) in the anoxic bottom waters, which contain a total of 7.4 × 10⁵ tons of CH₄. Profiles of dissolved inorganic carbon (ΣCO₂) and carbon isotopes (δ¹³C) show that CH₄ is oxidized in the vicinity of the persistent pycnocline and that some of this CH₄ is likely oxidized anaerobically. The dearth of NO₃⁻ and SO₄²⁻ in Lake Matano waters suggests that anaerobic methane oxidation may be coupled to the reduction of Fe (and/or Mn) (hydr)oxides. Thermodynamic considerations reveal that CH₄ oxidation coupled to Fe(III) or Mn(III/IV) reduction would yield sufficient free energy to support microbial growth at the substrate levels present in Lake Matano. Flux calculations imply that Fe and Mn must be recycled several times directly within the water column to balance the upward flux of CH₄. 16S gene cloning identified methanogens in the anoxic water column, and these methanogens belong to groups capable of both acetoclastic and hydrogenotrophic methanogenesis. We find that methane is important in C cycling, even in this very Fe-rich environment. Such Fe-rich environments are rare on Earth today, but they are analogous to conditions in the ferruginous oceans thought to prevail during much of the Archean Eon. By analogy, methanogens and methanotrophs could have formed an important part of the Archean Ocean ecosystem.

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.

Carbon cycling in Santa Barbara Basin sediments: A modeling study

The primary input of organic matter to almost all marine sediments comes from deposition at the sediment surface. However, in many continental margin settings, reduced carbon can also be added to sediments from below—for example, from “deep” geologic hydrocarbon reservoirs derived from ancient source rocks or from the decomposition of deeply buried gas hydrate deposits. To examine the impact of these two differing reduced carbon inputs on sediment biogeochemistry, a modified reaction-transport model for anoxic marine sediments is described here and applied to data from sediment cores in Santa Barbara Basin to a depth of 4.6 m. Excellent model fits yield results consistent with previous studies of Santa Barbara Basin and other continental margin sediments. These results indicate that authigenic carbonate precipitation in these sediments is not centered around the sulfatemethane transition zone (SMTZ), as is seen in many other sedimentary environments but occurs at shallower depths in the sediments and over a relatively broad depth range. Sulfate profiles are linear between the surface sediments (upper ∼20 cm) and the top of the SMTZ (∼105 cm) giving the appearance of refractory particulate organic carbon (POC) burial and conservative sulfate behavior in this intermediate region. However, model results show that linear profiles may also occur when high rates of sulfate reduction occur near the sediment surface (as organoclastic sulfate reduction [oSR]) and in the SMTZ (largely as anaerobic oxidation of methane) with low, but nonzero, rates of oSR inbetween. At the same time, linearity in the sulfate profile may also be related to downward pore-water advection by compaction and sedimentation plus a decrease with depth in sulfate diffusivity because of decreasing porosity. These model-determined rates of oSR and methanogenesis also result in a rate of POC loss that declines near-continuously in a logarithmic fashion over the entire sediment column studied. The results presented further here indicate the importance of a deep methane flux from below on sediment biogeochemistry in the shallower sediments, although the exact source of this methane flux is difficult to ascertain with the existing data.

Methane and microbial dynamics in the Gulf of Mexico water column

In contrast to other oligotrophic water bodies the Gulf of Mexico (GOM) hosts an abundance of hydrocarbon seeps, which likely influences the microbial assemblages it hosts particularly regarding the availability of labile carbon in the aphotic GOM. The aphotic zone receives direct injection of seep methane (CH4), but CH4 from an unknown source has been reported at supersaturated concentrations relative to the atmosphere in the GOM photic zone. Here we used iTag sequencing of 16S rRNA genes to characterize GOM microbial communities and to relate changes in microbial community structure to the properties inherent to their oceanic province-seafloor to the photic zone, seep and non-seep. Along this trajectory water column communities were distinct in the euphotic zone compared to the mesopelagic and deep-sea. In the euphotic zone the relative abundance of a cyanobacterial species (Prochlorococcus) was significantly correlated with both CH4 and chlorophyll a concentrations and was abundant in some deep-chlorophyll maximum (DCM) samples. The relative abundance of microorganisms related to known hydrocarbon degraders were also significantly correlated with CH4 in the euphotic zone, but no canonical methanotrophs were observed. In the mesopelagic to the seafloor canonical methanotrophs were identified, but only a Marine Group II Euryarchaeota was significantly correlated with CH4. Overall, depth and the associated environmental conditions were the primary drivers in structuring microbial communities over the GOM water column. Further, CH4 concentrations and relative microbial abundances covaried significantly from the seafloor to the photic zone in the GOM. The lack of a significant relationship between canonical methanotrophs and CH4 in the aphotic zone, even when sampling at seep sites, may suggest methane-oxidation by unknown microorganisms. Similarly their absence in the CH4 maximum and DCM suggested that CH4 is either oxidized by unrecognized methanotrophs or escapes the CH4 biofilter and fluxes to the atmosphere.

Preface to Bjørn Sundby’s Special Issue of Aquatic Geochemistry

This special issue of Aquatic Geochemistry is dedicated to the career of Bjorn Sundby (Fig. 1), Professor of Oceanography at the ‘‘Institut des Sciences de la Mer de Rimouski,’’ Canada. Bjorn earned his PhD in physical organic chemistry from the University of Bergen (Norway) in 1966. He started his professional career as an organic chemist for the ColgatePalmolive Company, where he worked to develop novel phosphate-free detergents in the face of the looming eutrophication crisis. Exploring his diverse interests while at Colgate, Bjorn enrolled in oceanography classes at Rutgers University and fell in love with the subject. In pursuit of a career in Oceanography, he then moved to Dalhousie University in Halifax to take on a postdoctoral position with Doug Loring. During this time, he met his wife Daniele Godbout. Ultimately, Bjorn took up a position as an oceanography research associate at the Universite du Quebec a Rimouski from 1974 to 1980, before becoming Professor of Oceanography from 1980 to 1984. He then returned to Europe to head the Department of Chemical Oceanography and Marine Pollution at the Netherlands Institute for Sea Research from 1984 to 1987, before coming back to Canada as Director of the Physical and Chemical Oceanography Branch at the Maurice Lamontagne Institute, Department of Fisheries and Oceans, Canada. With a mass of scientific achievements under his belt, Bjorn earned a prestigious Dr. Philos. Degree in aquatic geochemistry from the University of Bergen in 1987. From 1992 to his retirement in 2010, he was Professor of Oceanography at the Institut des Sciences de la Mer de Rimouski, QC. For nearly three decades, Bjorn has continued to challenge and change our view of sediment diagenesis, from the early models of a 1-dimensional steady-state system to our current picture of a 3D dynamic mosaic of biogeochemical reactions. One of his first major contributions was his work on manganese in the St. Lawrence Estuary. He was one of the

Methane dynamics in Santa Barbara Basin (USA) sediments as examined with a reaction-transport model

Here we describe a new reaction-transport model that quantitatively examines δ13C profiles of porewater methane and dissolved inorganic carbon (DIC) (δCCH4 and δCDIC) in the anoxic sediments of the Santa Barbara Basin (California Borderland region). Best-fit solutions of the model to these data suggest that CO2 reduction is the predominant form of methanogenesis in these sediments. These solutions also accurately reproduce the isotope depth profiles, including a broad minimum in the δCDIC profile and a much sharper (angular) minimum in the δCCH4 profile, both of which appear near the base of the transition zone in the sediments between sulfate reduction and methanogenesis (referred to here as the sulfate-methane transition zone, or SMTZ). Such minima in pore-water profiles of δCCH4 near the base of the SMTZ have been seen in a number of other marine sediments across a range of depth and timescales. We show here that this minimum in the δCCH4 profile in Santa Barbara Basin sediments results from the balance between (1) anaerobic oxidation of methane (AOM), which leads to an increase in δCCH4 with decreasing depth in the sediment column through and above the SMTZ; (2) methanogenesis, which produces 13C-depleted methane, both in and below the SMTZ; and (3) an upward flux of CH4 from depth that is relatively enriched in 13C as compared with the methane in these pore waters. Possible sources of this deep methane include the following: geologic hydrocarbon reservoirs derived from ancient source rocks; decomposition of buried gas hydrates; and biogenic (or perhaps thermogenic) methane produced hundreds of meters below the seafloor stimulated by increasing temperatures associated with the sediment geothermal gradient. Although we are unable to resolve these possible sources of deep methane, we believe that the significance of an upward methane flux as an explanation for minima in δCCH4 pore-water profiles may not be limited to Santa Barbara Basin sediments but may be common in many continental margin sediments.