Allan H. Devol

Influence of oxygen exposure time on organic carbon preservation in continental margin sediments

Today, over 90% of all organic carbon burial in the ocean occurs in continental margin sediments. This burial is intrinsically linked to the cycling of biogeochemically important elements (such as N, P, S, Fe and Mn) and, on geological timescales, largely controls the oxygen content of the atmosphere. Currently there is a volatile debate over which processes govern sedimentary organic carbon preservation. In spite of numerous studies demonstrating empirical relationships between organic carbon burial and such factors as primary productivity, the flux of organic carbon through the water column, sedimentation rate,, organic carbon degradation rate, and bottom-water oxygen concentration,, the mechanisms directly controlling sedimentary organic carbon preservation remain unclear. Furthermore, as organic carbon burial is the process that, along with pyrite burial, balances O2 concentrations in the atmosphere, it is desirable that any mechanism proposed to control organic carbon preservation include a feedback buffering atmospheric oxygen concentrations over geological time. Here we compare analyses of sediments underlying two regions of the eastern North Pacific Ocean, one which has oxygen-depleted bottom waters and one with typical oxygen distributions. Organic carbon burial efficiency is strongly correlated with the length of time accumulating particles are exposed to molecular oxygen in sediment pore waters. Oxygen exposure time effectively incorporates other proposed environmental variables, and may exert a direct control on sedimentary organic carbon preservation and atmospheric oxygen concentrations.

Effects of fungal degradation on the CuO oxidation products of lignin: A controlled laboratory study

Duplicate samples of birch wood were degraded for 0, 4, 8 and 12 weeks by the white-rot fungus, Phlebia tremellosus, and for 12 weeks by 6 other white-rot and brown-rot fungi. P. tremellosus caused progressive weight losses and increased the H/C and O/C of the remnant wood by preferentially degrading the lignin component of the middle lamellae. This fungus increased the absolute (weight loss-corrected) yield of the vanillic acid CuO reaction product above its initial level and exponentially decreased the absolute yields of all other lignin-derived phenols. Total yields of syringyl phenols were decreased 1.5 times as fast as total vanillyl phenol yields. Within both phenol families, aldehyde precursors were degraded faster than precursors of the corresponding ketones, which were obtained in constant proportion to the total phenol yield. Although two other white-rot fungi caused similar lignin compositional trends, a fourth white-rot species, Coriolus versicolor, simultaneously eroded all cell wall components and did not concentrate polysaccharides in the remnant wood. Wood degraded by the three brown-rot fungi exhibited porous cell walls with greatly reduced integrity. The brown-rot fungi also preferentially attacked syringyl structural units, but degraded all phenol precursors at a much slower rate than the white-rotters and did not produce excess vanillic acid. Degradation by P. tremellosus linearly increased the vanillic acid/vanillin ratio, (Ad/Al)v, of the remnant birch wood throughout the 12 week degradation study and exponentially decreased the absolute yields of total vanillyl phenols, total syringyl phenols and the syringyl/vanillyl phenol ratio, S/V. At the highest (Ad/Al)v of 0.50 (12 week samples), total yields of syringyl and vanillyl phenols were decreased by 65% and 80%, respectively, with a resulting reduction of 40% in the original S/V. Many of the diagenetically related compositional trends that have been previously reported for lignins in natural environments can be explained by white-rot fungal degradation.

Nitrite Reductase Genes (nirK and nirS) as Functional Markers To Investigate Diversity of Denitrifying Bacteria in Pacific Northwest Marine Sediment Communities

ABSTRACT Genetic heterogeneity of denitrifying bacteria in sediment samples from Puget Sound and two sites on the Washington continental margin was studied by PCR approaches amplifying nirK andnirS genes. These structurally different but functionally equivalent single-copy genes coding for nitrite reductases, a key enzyme of the denitrification process, were used as a molecular marker for denitrifying bacteria. nirS sequences could be amplified from samples of both sampling sites, whereas nirKsequences were detected only in samples from the Washington margin. To assess the underlying nir gene structure, PCR products of both genes were cloned and screened by restriction fragment length polymorphism (RFLP). Rarefraction analysis revealed a high level of diversity especially for nirS clones from Puget Sound and a slightly lower level of diversity for nirK andnirS clones from the Washington margin. One group dominated within nirK clones, but no dominance and only a few redundant clones were seen between sediment samples fornirS clones in both habitats. Hybridization and sequencing confirmed that all but one of the 228 putative nirS clones were nirS with levels of nucleotide identities as low as 45.3%. Phylogenetic analysis grouped nirS clones into three distinct subclusters within the nirS gene tree which corresponded to the two habitats from which they were obtained. These sequences had little relationship to any strain with knownnirS sequences or to isolates (mostly close relatives ofPseudomonas stutzeri) from the Washington margin sediment samples. nirK clones were more closely related to each other than were the nirS clones, with 78.6% and higher nucleotide identities; clones showing only weak hybridization signals were not related to known nirK sequences. AllnirK clones were also grouped into a distinct cluster which could not be placed with any strain with known nirKsequences. These findings show a very high diversity of nirsequences within small samples and that these novel nirclusters, some very divergent from known sequences, are not known in cultivated denitrifiers.

Denitrification as the dominant nitrogen loss process in the Arabian Sea

Primary production in over half of the world’s oceans is limited by fixed nitrogen availability. The main loss term from the fixed nitrogen inventory is the production of dinitrogen gas (N2) by heterotrophic denitrification or the more recently discovered autotrophic process, anaerobic ammonia oxidation (anammox). Oceanic oxygen minimum zones (OMZ) are responsible for about 35% of oceanic N2 production and up to half of that occurs in the Arabian Sea. Although denitrification was long thought to be the only loss term, it has recently been argued that anammox alone is responsible for fixed nitrogen loss in the OMZs. Here we measure denitrification and anammox rates and quantify the abundance of denitrifying and anammox bacteria in the OMZ regions of the Eastern Tropical South Pacific and the Arabian Sea. We find that denitrification rather than anammox dominates the N2 loss term in the Arabian Sea, the largest and most intense OMZ in the world ocean. In seven of eight experiments in the Arabian Sea denitrification is responsible for 87–99% of the total N2 production. The dominance of denitrification is reproducible using two independent isotope incubation methods. In contrast, anammox is dominant in the Eastern Tropical South Pacific OMZ, as detected using one of the isotope incubation methods, as previously reported. The abundance of denitrifying bacteria always exceeded that of anammox bacteria by up to 7- and 19-fold in the Eastern Tropical South Pacific and Arabian Sea, respectively. Geographic and temporal variability in carbon supply may be responsible for the different contributions of denitrification and anammox in these two OMZs. The large contribution of denitrification to N2 loss in the Arabian Sea indicates the global significance of denitrification to the oceanic nitrogen budget.

Community structure of denitrifiers, bacteria, and archaea along redox gradients in Pacific Northwest marine sediments by terminal restriction fragment length polymorphism analysis of amplified nitrite reductase (nirS) and 16S rRNA genes.

ABSTRACT Steep vertical gradients of oxidants (O2 and NO3−) in Puget Sound and Washington continental margin sediments indicate that aerobic respiration and denitrification occur within the top few millimeters to centimeters. To systematically explore the underlying communities of denitrifiers,Bacteria, and Archaea along redox gradients at distant geographic locations, nitrite reductase (nirS) genes and bacterial and archaeal 16S rRNA genes (rDNAs) were PCR amplified and analyzed by terminal restriction fragment length polymorphism (T-RFLP) analysis. The suitablility of T-RFLP analysis for investigating communities of nirS-containing denitrifiers was established by the correspondence of dominant terminal restriction fragments (T-RFs) of nirS to computer-simulated T-RFs ofnirS clones. These clones belonged to clusters II, III, and IV from the same cores and were analyzed in a previous study (G. Braker, J. Zhou, L. Wu, A. H. Devol, and J. M. Tiedje, Appl. Environ. Microbiol. 66:2096–2104, 2000). T-RFLP analysis ofnirS and bacterial rDNA revealed a high level of functional and phylogenetic diversity, whereas the level of diversity ofArchaea was lower. A comparison of T-RFLPs based on the presence or absence of T-RFs and correspondence analysis based on the frequencies and heights of T-RFs allowed us to group sediment samples according to the sampling location and thus clearly distinguish Puget Sound and the Washington margin populations. However, changes in community structure within sediment core sections during the transition from aerobic to anaerobic conditions were minor. Thus, within the top layers of marine sediments, redox gradients seem to result from the differential metabolic activities of populations of similar communities, probably through mixing by marine invertebrates rather than from the development of distinct communities.

Isotopic fractionation of oxygen and nitrogen in coastal marine sediments

Abstract The bulk and isotopic exchanges of O2, N2, NO3, and NH4+ between sediments and the overlying water (benthic flux) were measured at three shallow locations in Puget Sound using a benthic tripod. Oxygen consumption by the sediments averaged 4.4 mmol m−2 d−1, while N2 gas fluxes averaged 1.1 mmol M−2 d−1. The nitrogen gas flux out of the sediments was always greater than the corresponding NO3-flux into the sediments, indicating a large nitrification contribution to the N2 flux. Isotopic changes in overlying water δ18O of O2 were small, with an average apparent sediment respiration fractionation-factor, e, of 3. This fractionation-factor is much smaller than that measured in either the open ocean or in the laboratory. The low degree of fractionation is hypothesized to occur because of the interaction of diffusive layers around reactive microsites within these sediments. There was no apparent isotopic fractionation of downward-diffusing NO3− (e = 0), while the ammonium that diffused out of the sediments averaged 4.5%o heavier than both source organic matter within the sediments and overlying water NO3. The large discrepancy in isotopic composition between the source organic material and NH4+ can be attributed to significant isotopic fractionation of ammonium during nitrification in the oxic zone. Finally, the δ15N of N2 did not change significantly over the course of the incubations, in agreement with the nitrogen isotopic budget for these sediments.

Molecular Evidence for the Broad Distribution of Anaerobic Ammonium-Oxidizing Bacteria in Freshwater and Marine Sediments

ABSTRACT Previously available primer sets for detecting anaerobic ammonium-oxidizing (anammox) bacteria are inefficient, resulting in a very limited database of such sequences, which limits knowledge of their ecology. To overcome this limitation, we designed a new primer set that was 100% specific in the recovery of ∼700-bp 16S rRNA gene sequences with >96% homology to the “Candidatus Scalindua” group of anammox bacteria, and we detected this group at all sites studied, including a variety of freshwater and marine sediments and permafrost soil. A second primer set was designed that exhibited greater efficiency than previous primers in recovering full-length (1,380-bp) sequences related to “Ca. Scalindua,” “Candidatus Brocadia,” and “Candidatus Kuenenia.” This study provides evidence for the widespread distribution of anammox bacteria in that it detected closely related anammox 16S rRNA gene sequences in 11 geographically and biogeochemically diverse freshwater and marine sediments.

Budgetary and biogeochemical implications of N2O isotope signatures in the Arabian Sea

Nitrous oxide (N2O) is an important greenhouse gas that also plays a role in the chemistry of stratospheric ozone depletion, but its atmospheric budget has yet to be well-quantified. However, multi-isotope characterization of N2O emitted from various natural sources is a potentially powerful tool for providing the much-needed constraints. It is generally believed that production of isotopically light (low 15N/14N and 18O/16O ratios) N2O occurs in the upper ocean through nitrification process, and that the flux of this light N2O from sea to air isotopically counters the flux of heavy N2O from the stratosphere to the troposphere,. But eastern-boundary ocean-upwelling zones, which contain oxygen-depleted waters and are sites of intense N2O efflux, have not been adequately studied. We show here, using new isotope data, that in spite of huge denitrification-related enrichments of 15N and 18O in N2O at mid-depths in the Arabian Sea, N2O emitted from upwelled waters is only slightly enriched in 18O, and moderately depleted in 15N, relative to air. These opposing isotopic signatures and modest departures from the isotopic composition of tropospheric N2O indicate that air–sea exchange cannot — given the heavy isotopic signature of N2O derived from the stratosphere — allow the tropospheric budget of N2O to be closed without invoking hitherto-unknown N2O sources and sinks. Our oceanic data cannot be explained through either nitrification or denitrification alone, such that a coupling between the two processes may be an important mechanism of N2O production.

Benthic fluxes and nitrogen cycling in sediments of the continental margin of the eastern North Pacific

The exchange of Oz, Nz, NO;, NH:, Si(OH)d, and POi3 between the sediments and the overlying water (benthic flux) was determined at 18 locations on the Washington State continental margin using an in situ benthic tripod. Oxygen consumption by the sediments ranged from 21.2pmole cm-* s-l on the shelf to 2.85pmole cm-2 s-l on the slope. Nitrogen gas fluxes were from the sediments to the overlying water. They varied 5.5 to 1.2pmole-N cm-* SK* and were always greater than the corresponding NO; flux into the sediments. A nitrogen mass balance indicated that the difference between the N2 flux out and the NO; flux in could be accounted for by oxidation of NH: produced during aerobic and anaerobic carbon remineralization to NO; and subsequent denitrification to Nz, Comparison of the benthic fluxes of 02, NO; and Si(OH)4 with the fluxes predicted from molecular diffusion across the sediment water interface showed that for all three solutes the benthic fluxes were up to three times greater than the molecular fluxes and indicated the importance of macrobenthic irrigation in these sediments. However, several existing empirical irrigation models were not able to describe all three solutes. The overall carbon oxidation rate, as estimated from the sum of the O2 flux, the N2 flux and the measured SOT reduction rate, could be fit with a normalized power function; i.e., carbon oxidation rate (gC m-* y-l) = 110 . (z/~OO)-~,~*. The exponent describing the rate of attenuation with depth (-0.91) was similar to the carbon rain rate attenuation coefficient determined from sediment traps in the pelagic, eastern North Pacific.

Impact of suboxia on sinking particulate organic carbon: Enhanced carbon flux and preferential degradation of amino acids via denitrification

Fluxes of particulate organic carbon (POC) through the oxygen deficient waters in the eastern tropical North Pacific were found to be relatively less attenuated with depth than elsewhere in the eastern North Pacific. The attenuation coefficient (b) for the flux was found to be 0.40 versus the composite value of 0.86 determined by Martin et al. (1987). To examine this further, sinking POC was collected using sediment traps and allowed to degrade in oxic and suboxic experiments. Using a kinetic model, it was found that degradation proceeded at similar rates (roughly 0.8 day−1) under oxic and suboxic conditions, but a greater fraction of bulk POC was resistant to degradation in the suboxic experiments (61% vs. 23%). Amino acids accounted for 37% of POC collected at 75m, but following degradation the value dropped to 17% and 16% in the oxic and suboxic experiments respectively. POC collected from 500m was 10% amino acids. The non-AA component of POC collected at 75m was not degraded under suboxic conditions, while under oxic conditions it was. These results suggest that microbes degrading OC under suboxic conditions via denitrification preferentially utilize nitrogen-rich amino acids. This preferential degradation of amino acids suggests that 9% more nitrogen may be lost via water column denitrification than is accounted for when a more “Redfieldian” stoichiometry for POC is assumed.