Bacterial methanotrophs drive the formation of a seasonal anoxic benthic nepheloid layer in an alpine lake

Blees, Jan; Niemann, Helge; Wenk, Christine B.; Zopfi, Jakob; Schubert, Carsten J.; Jenzer, Joël S; Veronesi, Mauro; Lehmann, Moritz F.

doi:10.4319/lo.2014.59.4.1410

Cited by 30 publications

(39 citation statements)

References 43 publications

(56 reference statements)

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“…The development of a BNL is common for lakes, but the identity of the suspended particles is often uncertain. In the Lake Lugano south basin, compelling evidence indicates that the suspended particles of the BNL are of bacterial origin (Lehmann et al 2004;Blees et al 2014), and our hydrochemical profiles indicate that intensive N cycling occurs within the BNL. In the next sections, we will first discuss the seasonal variations in benthic solute fluxes and sedimentary N transformation pathways and rates.…”

Section: Discussionmentioning

confidence: 68%

“…The rise of the oxycline into the water column was paralleled by NH z 4 accumulation in the anoxic bottom water (Fig. 3c,g) and the development of a bacterial benthic nepheloid layer (BNL; Lehmann et al 2004;Blees et al 2014). Ammonium concentrations were always highest at the sediment-water interface (up to 80 mmol L 21 in November 2009) and decreased toward the oxic-anoxic interface, indicating turbulent diffusive mixing, its aerobic or anaerobic consumption, or uptake by microorganisms within the BNL.…”

Section: Resultsmentioning

confidence: 93%

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Partitioning between benthic and pelagic nitrate reduction in the Lake Lugano south basin

Wenk

Zopfi

Gardner

et al. 2014

Limnology & Oceanography

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We evaluated the seasonal variation of denitrification, anaerobic ammonium oxidation (anammox), and dissimilatory nitrate reduction to ammonium (DNRA) rates in the sediments and the integrative N (and O) isotopic signatures of dissolved inorganic nitrogen (DIN) compounds in the overlying water column of the monomictic Lake Lugano south basin. Denitrification was the dominant NO { 3 reduction pathway, whereas the contribution of anammox and DNRA to total benthic NO { 3 reduction was , 6% and , 12%, respectively. Sedimentary denitrification rates were highest (up to 57.2 6 16.8 mmol N m 22 h 21 ) during fully oxic bottom water conditions. With the formation of seasonal bottom water anoxia, NO { 3 reduction was partitioned between water column and sedimentary processes. Total benthic NO { 3 reduction rates determined in 15 N-label experiments and sediment-water interface N 2 fluxes as calculated from water column N 2 : Ar gradients revealed that sedimentary denitrification still accounted for , 40% of total N 2 production during bottom water anoxia. The partitioning between water column and sedimentary denitrification was further evaluated by the natural abundance stable N isotope composition of dissolved NO from approximately 7% to 20% and from 2% to 14%, respectively. Using a closed-system (Rayleigh) model, the N and O isotope effects associated with community NO { 3 consumption were 15 e < 13.7% and 18 e < 11.3%, respectively. With the assumptions of a relatively low net N isotope effect associated with sedimentary denitrification (i.e., 15 e sed 5 1.5-3%) vs. a fully expressed biological N isotope fractionation during water column denitrification (i.e., 15 e water 5 20-25%), our results confirm that 36-51% of NO { 3 reduction occurred within the sediment. The general agreement between the indirect (isotopic) approach and the flux and rate measurements suggests that water column nitrate isotope measurements can be used to distinguish between benthic and pelagic denitrification quantitatively.

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Section: Discussionmentioning

confidence: 68%

Section: Resultsmentioning

confidence: 93%

Partitioning between benthic and pelagic nitrate reduction in the Lake Lugano south basin

Wenk

Zopfi

Gardner

et al. 2014

Limnology & Oceanography

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“…With the onset of seasonal anoxia in the south basin of Lake Lugano (Lehmann et al, 2004; Blees et al, 2014), the sediments (95 m) and deep redox transition zone (70–90 m) become important in the production and consumption of deep N 2 O in this system (Freymond et al, 2013; Wenk et al, 2016). Here we have restricted our discussion to the top 50 m of the water column.…”

Section: Resultsmentioning

confidence: 99%

Acidification Enhances Hybrid N2O Production Associated with Aquatic Ammonia-Oxidizing Microorganisms

et al. 2017

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Ammonia-oxidizing microorganisms are an important source of the greenhouse gas nitrous oxide (N2O) in aquatic environments. Identifying the impact of pH on N2O production by ammonia oxidizers is key to understanding how aquatic greenhouse gas fluxes will respond to naturally occurring pH changes, as well as acidification driven by anthropogenic CO2. We assessed N2O production rates and formation mechanisms by communities of ammonia-oxidizing bacteria (AOB) and archaea (AOA) in a lake and a marine environment, using incubation-based nitrogen (N) stable isotope tracer methods with 15N-labeled ammonium (15NH4+) and nitrite (15NO2−), and also measurements of the natural abundance N and O isotopic composition of dissolved N2O. N2O production during incubations of water from the shallow hypolimnion of Lake Lugano (Switzerland) was significantly higher when the pH was reduced from 7.54 (untreated pH) to 7.20 (reduced pH), while ammonia oxidation rates were similar between treatments. In all incubations, added NH4+ was the source of most of the N incorporated into N2O, suggesting that the main N2O production pathway involved hydroxylamine (NH2OH) and/or NO2− produced by ammonia oxidation during the incubation period. A small but significant amount of N derived from exogenous/added 15NO2− was also incorporated into N2O, but only during the reduced-pH incubations. Mass spectra of this N2O revealed that NH4+ and 15NO2− each contributed N equally to N2O by a “hybrid-N2O” mechanism consistent with a reaction between NH2OH and NO2−, or compounds derived from these two molecules. Nitrifier denitrification was not an important source of N2O. Isotopomeric N2O analyses in Lake Lugano were consistent with incubation results, as 15N enrichment of the internal N vs. external N atoms produced site preferences (25.0–34.4‰) consistent with NH2OH-dependent hybrid-N2O production. Hybrid-N2O formation was also observed during incubations of seawater from coastal Namibia with 15NH4+ and NO2−. However, the site preference of dissolved N2O here was low (4.9‰), indicating that another mechanism, not captured during the incubations, was important. Multiplex sequencing of 16S rRNA revealed distinct ammonia oxidizer communities: AOB dominated numerically in Lake Lugano, and AOA dominated in the seawater. Potential for hybrid N2O formation exists among both communities, and at least in AOB-dominated environments, acidification may accelerate this mechanism.

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“…Lakes represent an important source of CH 4 to the atmosphere (Bastviken et al ; Borrel et al ) and most of the lacustrine methane is produced by methanogenic microorganisms within anoxic sediments. Yet, a large fraction (57–100%) of the biogenic CH 4 produced is oxidized by methanotrophic microorganisms within anoxic or oxic sediments, or in the water column (Bastviken et al ; Schubert et al ; Blees et al , b ). The anaerobic oxidation of methane (AOM) has mostly been studied in benthic marine environments and it is typically coupled to sulfate reduction (Boetius et al ; Knittel and Boetius ), but other electron acceptors are possible (Ettwig et al , ; Sivan et al ; Haroon et al ; Deutzmann et al ; Cai et al ).…”

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confidence: 99%

“…Evidence for AOM in freshwater environments is rare and not always conclusive (Crowe et al ; Schubert et al ; Bray et al ). In contrast, there is multiple evidence for aerobic methane oxidation (MOx) in lakes, and a great diversity of bacteria and niches of the different aerobic methanotrophs were described (Hanson and Hanson ; Blees et al , b ; Oswald et al , b ). Independent of the mode of methane oxidation, microbes play a pivotal role in modulating lacustrine methane fluxes and mitigating CH 4 emissions to the atmosphere, with important implications for the global CH 4 budget (Reeburgh ).…”

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confidence: 99%

Evaluating radioisotope‐based approaches to measure anaerobic methane oxidation rates in lacustrine sediments

Niemann

Steinle

et al. 2019

Limnology & Ocean Methods

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The microbial anaerobic oxidation of methane (AOM) is the dominant sink for methane in anoxic sediments. AOM rate measurements are essential for assessing the efficacy of the benthic methane filter to mitigate the evasion of this potent greenhouse gas to the atmosphere. Incubation techniques with trace amounts of radiolabeled substrate (typically 14 CH 4 ) represent the most sensitive approach for methane oxidation rate measurements. Yet, radiotracer application can be performed in different ways, rendering the comparability of AOM rate measurements in field and laboratory investigations problematic. We compared four different 14 CH 4 -based shortterm incubation approaches to quantify methane turnover rates in lake sediments. Three of the applied methods yielded similar and reliable downcore rate profiles. They provided clear evidence for AOM with maximum rates of 15 nmol cm −3 d −1 at~17 cm sediment depth. Using the short-term slurry incubation (SL) method, however, we were unable to detect the AOM activity maximum that we observed with the other approaches. We hypothesize that changes in the microbial structure and disruption of physical interactions due to mixing of sediments negatively affected the activity of AOM communities and longer incubation times are necessary to enhance the sensitivity of this approach. Minor variabilities in rate measurement that we found in the non-SL incubations may be related to small-scale sediment heterogeneity, differential partial methane loss during sample handling, and/or an uneven application of the radiotracer. Whole-core incubations interfere the least with the in situ conditions, but the ultimate choice of the AOM rate measurement method will depend on the individual sampling requirements.

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Bacterial methanotrophs drive the formation of a seasonal anoxic benthic nepheloid layer in an alpine lake

Cited by 30 publications

References 43 publications

Partitioning between benthic and pelagic nitrate reduction in the Lake Lugano south basin

Partitioning between benthic and pelagic nitrate reduction in the Lake Lugano south basin

Acidification Enhances Hybrid N2O Production Associated with Aquatic Ammonia-Oxidizing Microorganisms

Evaluating radioisotope‐based approaches to measure anaerobic methane oxidation rates in lacustrine sediments

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