Carbon isotopes of dissolved inorganic carbon reflect utilization of different carbon sources by microbial communities in two limestone aquifer assemblages

Nowak, Martin; Schwab, Valérie F.; Lazar, Cassandre Sara; Behrendt, Thomas; Kohlhepp, Bernd; Totsche, Kai Uwe; Küsel, Kirsten; Trumbore, Susan E.

doi:10.5194/hess-21-4283-2017

Cited by 42 publications

(20 citation statements)

References 49 publications

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“…Similar losses of aromatic constituents have been described for soils and rivers by other techniques (Creed et al, 2015;Klotzbücher et al, 2016). This implies that freshly decomposing materials can be traced by their contribution of aromatic-and phenolic-type formulae (Roth et al, 2013(Roth et al, , 2014(Roth et al, , 2016Nowak et al, 2017;Schwab et al, 2017). In short, Roth et al (2014) described several trends in a study including different sets of ecosystem samples.…”

Section: Retrieval Of Discriminating Information and Biogeochemical Tsupporting

confidence: 61%

“…We found reproducible separation of a subset of these samples (water samples from forest soils, grassland soil, bogs, and rivers) on both instruments. This encompassed (a) differentiation of surface and soil water samples, which were paralleled by changes in pH and vegetation type (clusters A and B in Figure 5A; Roth et al, 2013Roth et al, , 2014, (b) retrieval of a depth trend found for grassland soils (JE-2-5 samples) including an increase in molecular similarity to river and marine samples with depth mainly due to vanishing aromatic-type formulae in the lower mass range (cluster C) (Roth et al, 2016), and (c) discrimination of anoxic (H5-3a) and oxic (H3-2b) aquifer environments (cluster D, Nowak et al, 2017;Schwab et al, 2017). Unique formulae of forest sites showed a higher aromaticity compared to unique formulae found in less acidic grassland sites, supporting the finding that aromatic signals < m/z 300 might be linked to fresh and less decomposed organic matter inputs (Roth et al, 2014(Roth et al, , 2016.…”

Section: Retrieval Of Discriminating Information and Biogeochemical Tmentioning

confidence: 97%

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Molecular Signals of Heterogeneous Terrestrial Environments Identified in Dissolved Organic Matter: A Comparative Analysis of Orbitrap and Ion Cyclotron Resonance Mass Spectrometers

et al. 2018

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Terrestrial dissolved organic matter (DOM) interlinks large carbon reservoirs of soils, sediments, and marine environments but remains largely uncharacterized on the molecular level. Fourier transform mass spectrometry (FTMS) has proven to be a powerful technique to reveal DOM chemodiversity and potential information encrypted therein. State-of-the-art FT-ICR MS (ion cyclotron resonance) instruments are yet inaccessible for most researchers. To evaluate the performance of the most recent Orbitrap analyzer as a more accessible alternative, we compared our method to an established 15 T FT-ICR MS on a diverse suite of 17 mainly terrestrial DOM samples regarding (1) ion abundance patterns, (2) differential effects of DOM type on information loss, and (3) derived biogeochemical information. We show that the Orbitrap provides similar information as FT-ICR MS, especially for compound masses below 400 m/z, and is mainly limited by its actual resolving power rather than its sensitivity. Ecosystems that are dominated by inputs of plant-derived material, like DOM from soil, bog, lake, and rivers, showed remarkably low average mass to charge ratios, making them also suitable for Orbitrap measurements. The additional information gained from FT-ICR MS was highest in heteroatom-rich (N, S, P) samples from systems dominated by internal cycling, like DOM from groundwater and the deep sea. Here FT-ICR MS detected 37% more molecular formulae and 11% higher ion abundance. However, the overall information content, which was analyzed by multivariate statistical methods, was comparable for both data sets. Mass spectra-derived biogeochemical trends, for example, the decrease of DOM aromaticity during the passage through terrestrial environments, were retrieved by both instruments. We demonstrate the growing potential of the Orbitrap as an alternative FTMS analyzer in the context of challenging analyses of DOM complexity, origin, and fate.

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Section: Retrieval Of Discriminating Information and Biogeochemical Tsupporting

confidence: 61%

Section: Retrieval Of Discriminating Information and Biogeochemical Tmentioning

confidence: 97%

Molecular Signals of Heterogeneous Terrestrial Environments Identified in Dissolved Organic Matter: A Comparative Analysis of Orbitrap and Ion Cyclotron Resonance Mass Spectrometers

et al. 2018

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“…The medium 14 C-depleted wells H42, H43, and H52 share low-permeable rocks in laying and hanging strata (Lazar et al, 2019) and are therefore most likely cut off from direct surface-derived inputs, resulting in the moderate 14 C values of DOM in the water from these wells. While H53 had similar characteristics to H52 regarding the 14 C of inorganic carbon (Nowak et al, 2017) and major ion composition (Kohlhepp et al, 2017), DOM showed strong 14 C depletion of in H53 relative to H52. The strong 14 C depletion of DOM in H53 supported the indicated ecosystem compartmentalization by Lehmann and Totsche (2019), who described those zones as hydrogeologically isolated within the shallow groundwater flow system.…”

Section: Resultsmentioning

confidence: 90%

Fueling Diversity in the Subsurface: Composition and Age of Dissolved Organic Matter in the Critical Zone

et al. 2019

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Surface ecosystems are rapidly changing on a global scale and it is important to understand how this influences aquifers in the subsurface, as groundwater quality is a major concern for future generations. Dissolved organic matter (DOM) contains molecular and isotopic signals from surface-derived inputs as well as from the biotic and abiotic subsurface environment and is therefore ideal to study the connectivity between both environments. We evaluated a 3-year time series of DOM composition using ultrahigh resolution mass spectrometry and age using 14 C accelerator mass spectrometry along a hillslope well transect in the fractured bedrock of the Hainich Critical Zone Exploratory, Germany. We found a wide range of DOM 14 C depletion, from 14 C = −47.9 to 14 C = −782.4, within different zones of the shallow groundwater. The 14 C content of DOM mirrored the connectivity of the aquifers to the surface. The composition of DOM was highly interrelated with its 14 C age. The proportions of surface-derived DOM components decreased with DOM age, whereas microorganismderived DOM components increased. The intensity of surface-sourced DOM signals differed between the wells and likely reflected the hydrological complexity of fracturedrock environments. During recharge, DOM was more enriched in 14 C, contained more surface-derived molecular components and was more diverse. As a potential response to the varying DOM substrate, bacterial 16S rRNA gene analysis revealed community evolution and increased bacterial diversity during recharge. The influx of diverse, surface-derived DOM potentially fueled evolution within the autochthonous bacterial communities, as in contrast to DOM, the bacterial community did not retreat to the initial diversity and community composition during the recession period. Our results demonstrate on the one hand that combined analyses of the composition and age of groundwater DOM strongly contribute to the understanding of interconnections, community evolution and the functioning of subsurface ecosystems and on the other hand that changes in surface ecosystems have an imprint on subsurface ecosystems.

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“…Consequently, limitation by labile organic carbon was most likely a key factor underlying the observed high relevance of anammox vs. denitrification in the oligotrophic carbonate-rock aquifers of the Hainich CZE. In fact, carbon isotope-based studies in the groundwater of wells H52 and H53 pointed to a tight internal cycling of carbon including oxidation of sedimentary old organic matter depleted in both 13 C and 14 C, and subsequent refixation of 13 C- and 14 C-depleted CO 2 by chemolithoautotrophs (Nowak et al, 2017 ). For the same groundwater sampling wells, Schwab et al ( 2017 ) found a strong depletion of phospholipid [3]- and [5]-ladderanes in 13 C (δ 13 C values ranging from –48.0 ± 10.5 to –45.9 ± 11.7%0), indicative of active CO 2 -fixation via the acetyl-CoA-pathway and characteristic of anammox bacteria (Schouten et al, 2004 ), confirming the substantial contribution of the anammox process to in situ autotrophic CO 2 -fixation.…”

Section: Discussionmentioning

confidence: 99%

“…For the same groundwater sampling wells, Schwab et al ( 2017 ) found a strong depletion of phospholipid [3]- and [5]-ladderanes in 13 C (δ 13 C values ranging from –48.0 ± 10.5 to –45.9 ± 11.7%0), indicative of active CO 2 -fixation via the acetyl-CoA-pathway and characteristic of anammox bacteria (Schouten et al, 2004 ), confirming the substantial contribution of the anammox process to in situ autotrophic CO 2 -fixation. Disconnection of these groundwater wells from surface-derived organic carbon input further appeared likely due to thick overlying soils, low infiltration potential, and low hydraulic conductivities with estimated groundwater travel times ranging from 295 to 587 years (Kohlhepp et al, 2016 ; Nowak et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

Nitrogen Loss from Pristine Carbonate-Rock Aquifers of the Hainich Critical Zone Exploratory (Germany) Is Primarily Driven by Chemolithoautotrophic Anammox Processes

et al. 2017

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Despite the high relevance of anaerobic ammonium oxidation (anammox) for nitrogen loss from marine systems, its relative importance compared to denitrification has less been studied in freshwater ecosystems, and our knowledge is especially scarce for groundwater. Surprisingly, phospholipid fatty acids (PLFA)-based studies identified zones with potentially active anammox bacteria within two superimposed pristine limestone aquifer assemblages of the Hainich Critical Zone Exploratory (CZE; Germany). We found anammox to contribute an estimated 83% to total nitrogen loss in suboxic groundwaters of these aquifer assemblages at rates of 3.5–4.7 nmol L−1 d−1, presumably favored over denitrification by low organic carbon availability. Transcript abundances of hzsA genes encoding hydrazine synthase exceeded nirS and nirK transcript abundances encoding denitrifier nitrite reductase by up to two orders of magnitude, providing further support of a predominance of anammox. Anammox bacteria, dominated by groups closely related to Cand. Brocadia fulgida, constituted up to 10.6% of the groundwater microbial community and were ubiquitously present across the two aquifer assemblages with indication of active anammox bacteria even in the presence of 103 μmol L−1 oxygen. Co-occurrence of hzsA and amoA gene transcripts encoding ammonia mono-oxygenase suggested coupling between aerobic and anaerobic ammonium oxidation under suboxic conditions. These results clearly demonstrate the relevance of anammox as a key process driving nitrogen loss from oligotrophic groundwater environments, which might further be enhanced through coupling with incomplete nitrification.

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Carbon isotopes of dissolved inorganic carbon reflect utilization of different carbon sources by microbial communities in two limestone aquifer assemblages

Cited by 42 publications

References 49 publications

Molecular Signals of Heterogeneous Terrestrial Environments Identified in Dissolved Organic Matter: A Comparative Analysis of Orbitrap and Ion Cyclotron Resonance Mass Spectrometers

Molecular Signals of Heterogeneous Terrestrial Environments Identified in Dissolved Organic Matter: A Comparative Analysis of Orbitrap and Ion Cyclotron Resonance Mass Spectrometers

Fueling Diversity in the Subsurface: Composition and Age of Dissolved Organic Matter in the Critical Zone

Nitrogen Loss from Pristine Carbonate-Rock Aquifers of the Hainich Critical Zone Exploratory (Germany) Is Primarily Driven by Chemolithoautotrophic Anammox Processes

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