Amino acid nitrogen isotopic composition patterns in lacustrine sedimenting matter

doi:10.1016/j.gca.2013.07.020

Geochimica et Cosmochimica Acta

Volume 121, 15 November 2013, Pages 328-338

https://doi.org/10.1016/j.gca.2013.07.020 Get rights and content

Abstract

Amino acids (AAs) comprise a large fraction of organic nitrogen (N) in plankton and sedimenting matter. Aquatic studies of organic N compounds in general and of AAs in particular, mostly concentrate on marine environments. In order to study the cycling and fate of organic N and AAs in lakes, we measured the N isotopic composition (δ¹⁵N) of bulk organic matter (OM) and of single hydrolysable AAs in sediment trap and sediment samples from two Swiss lakes with contrasting trophic state: Lake Brienz, an oligotrophic lake with an oxic water column, and Lake Zug a eutrophic, meromictic lake. We also measured the N isotopic composition of water column nitrate, the likely inorganic N source during biosynthesis in both lakes. The δ¹⁵N–AA patterns found for the sediment trap material were consistent with published δ¹⁵N–AA data for marine plankton. The AA composition and primary δ¹⁵N–AA signatures are preserved until burial in the sediments. During early sedimentary diagenesis, the δ¹⁵N values of single AAs appear to increase, exceeding those of the bulk OM. This increase in δ¹⁵N–AA is paralleled by a decreased contribution of AAs to the total OM pool with progressed degradation, suggesting preferential AA degradation associated with a significant N isotope fractionation. Indicators for trophic level based on δ¹⁵N–AAs were determined, for the first time in lacustrine systems. In our samples, the trophic AAs were generally enriched in ¹⁵N compared to source AAs and higher trophic δ¹⁵N–AA values in Lake Zug were consistent with a higher trophic level of the bulk biomass compared to Lake Brienz. Especially the difference between average trophic δ¹⁵N–AAs and average source δ¹⁵N–AAs was sensitive to the trophic states of the two lakes. A proxy for total heterotrophic AA re-synthesis (ΣV), which is strongly associated with heterotrophic microbial reworking of the OM, was calculated based on δ¹⁵N values of trophic AAs. Higher ΣV in Lake Brienz indicate enhanced heterotrophic bacterial reworking of AAs under oligotrophic conditions. Despite changes in the δ¹⁵N–AA values within the sediments, the proxies based on these values were consistent over the studied sediment profile, indicating the preservation of trophic signatures; therefore, our results underscore that δ¹⁵N–AA analysis of sedimentary records represents a promising tool to assess trophic levels and bacterial re-synthesis in lakes.

Introduction

Nitrogen (N) is a major component of biomass and settling organic matter (OM). The availability of N controls autotrophic production and hence OM fluxes, both in marine and fresh water environments. To study the sources, biosynthesis, trophic transfer, and processing of OM, bulk δ¹⁵N measurements have been broadly applied in marine systems (e.g. Altabet et al., 1999, Peterson, 1999, Meador et al., 2007), estuaries (e.g. Middelburg and Nieuwenhuize, 1998), and lakes (Bernasconi et al., 1997, Hodell and Schelske, 1998, Lehmann et al., 2004a, Lehmann et al., 2004b, Kumar et al., 2011). Hydrolysable amino acids (AAs; abbreviation used throughout the manuscript for hydrolysable amino acids) comprise a large fraction of the organic N in phyto- and zooplankton, as well as sedimenting matter (Lee, 1988, Cowie and Hedges, 1992). Additional insights into food webs and the cycling of N can be gained by the stable isotope analysis of these vitally important compounds. For example, AA isotope measurements have been applied in studies on plankton food webs and feeding ecology in marine systems (McClelland and Montoya, 2002, McClelland et al., 2003, Loick et al., 2007, Popp et al., 2007, Hannides et al., 2009, Loick-Wilde et al., 2012), as well as terrestrial food webs and foraging habitats (e.g. Lorrain et al., 2009, Chikaraishi et al., 2011). δ¹⁵N–AA analysis of non-living marine OM were performed by McCarthy et al. (2007) and Calleja et al. (2013) with the goal to examine its source and processing history, and most recently, Sherwood et al. (2011) measured the δ¹⁵N–AA of modern and fossil gorgonian deep-sea corals to study the control for variable trophic processing and nitrate source partitioning.

The δ¹⁵N–AA approach is based upon differences in the organism-internal N isotopic fractionation, which occur during metabolic processes. Glutamic acid (Glu) becomes enriched in ¹⁵N during transamination and deamination reactions, associated with the cleavage of a carbon–nitrogen bond. In contrast, N isotopes are barely fractionated during the conversion of phenylanaline (Phe) to tyrosine (Tyr), since no carbon–nitrogen bond has to be cleaved or formed (Chikaraishi et al., 2007). McClelland and Montoya (2002) found that the δ¹⁵N of some AAs (e.g. Glu and aspartic acid (Asp)) consistently increases with every trophic transfer, while the δ¹⁵N of other AAs (e.g. Phe, serine (Ser), threonine (Thr)) remains basically unchanged. The AAs whose δ¹⁵N remain unchanged during trophic transfer thus provide unbiased information on the δ¹⁵N of the sources at the base of the food web (“source AAs”), while the so-called “trophic AAs”, which display systematic enrichment in ¹⁵N with each trophic transfer, represent indicators for the trophic history (McClelland and Montoya, 2002, McClelland et al., 2003). Moreover, an index that describes the degree of total AA re-synthesis due to heterotrophic microbial reworking of the detrital OM (ΣV) was introduced by McCarthy et al. (2007) and is calculated based on the average deviation of single δ¹⁵N values of trophic AAs with respect to the average δ¹⁵N value of trophic AAs in a sample.

Essentially all studies thus far making use of compound-specific N isotope measurements to investigate N sources and the fate of N containing OM in aquatic systems concentrate on marine environments. In this study, we tested the AA-based geochemical approaches with proven value in marine studies for the first time in lacustrine settings. We measured the δ¹⁵N of single hydrolysable AAs and bulk δ¹⁵N of sediment trap and sediment samples, as well as the bulk δ¹⁵N of suspended POM and zooplankton samples in two Swiss lakes with different trophic state in order to study changes in the AA isotopic composition of the particulate matter with degradation and bacterial reworking. Furthermore, we wanted to test if the proxies based on δ¹⁵N–AA for trophic levels applied on sedimenting OM can reveal trophic levels of the lakes and whether the values of these proxies change during early degradation. In addition, we measured the δ¹⁵N of nitrate (NO₃⁻) in the water column with the goal to trace biogeochemical N transformations in the water column and to gain information on the δ¹⁵N of the inorganic N which is most likely taken up by the phytoplankton at the base of the food web.

Section snippets

Sampling sites

Lake Brienz is a peri-alpine lake in the northern ranges of the Swiss Alps, with an oxic water column. The lake has a surface area of 29.8 km² and a volume of 5.2 km³. The maximum depth of the lake is 259 m. The catchment is drained by the two main inflows, the Aare and the Lütschine, which together transport an annual average of 300,000 tons of suspended material into Lake Brienz (Anselmetti et al., 2007). In contrast to the particle load, the nutrient input is low, explaining the oligotrophic

Nitrate concentrations and isotopic composition

In Lake Brienz in spring, NO₃⁻ concentrations and δ¹⁵NO₃⁻ values were essentially invariant at 6.5 μmol L⁻¹ and 1–2‰, respectively, throughout the water column (Fig. 1). By autumn, a subtle decrease in NO₃⁻ concentration to 4.8 μmol L⁻¹ was observed in the surface waters, while in the hypolimnion the concentrations remained unchanged (Fig. 1). As in spring, δ¹⁵NO₃⁻ values were quite constant over the entire water column in autumn (0.6–1.8‰). In Lake Zug during the spring sampling, NO₃⁻

Acknowledgments

We are grateful to M. Schurter for help with sediment coring and the deployment of sediment traps. K. Köllner and T. Diem are gratefully acknowledged for plankton sampling. We would like to thank G. Nobbe whom we unfortunately lost from our lab due to severe illness for assistance in the lab. J. Bolotin is thanked for help with δ¹⁵N–AA analysis and R. Stierli for measuring NO₃⁻ concentrations. Many thanks to Dr. Y. Chikaraishi and an anonymous reviewer for their valuable and constructive

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The nitrogen isotopic composition of amino acids (δ¹⁵N_AA) is a promising tool for estimating the trophic position and nitrogen sources of organisms in grazing food webs. The utility of δ¹⁵N_AA analysis of microbial processes in the biogeochemistry remains uncertain, because information about the δ¹⁵N_AA values of chemotrophic microbes are still limited. In this study, we report the δ¹⁵N_AA values in five cultured heterotrophic or chemolithoautotrophic microbes (one fungus, one bacterium, and three archaea) with controlled nitrogen sources in synthetic media. When the microbes were grown on ammonium, the apparent nitrogen isotopic fractionation of amino acids relative to glutamic acid in the microbes (e.g., −3.0 ± 1.0‰ for phenylalanine) was similar to those in algae. When the microbes were grown on a free amino acid mixture, the δ¹⁵N offsets of amino acids in the microbial cells relative to the amino acids in the culture media (e.g., +8.2 ± 0.8‰ for glutamic acid and +0.1 ± 0.2‰ for phenylalanine) were close to the standard isotopic fractionation between animals and their diets. These results suggest that the δ¹⁵N_AA pattern can be used to distinguish two end-member metabolic modes in microbes (i.e., de novo synthesis of amino acids from inorganic nitrogen vs. assimilation of amino acids from environments). We also discussed the effects of metabolic pathways on the δ¹⁵N_AA values and their fractionation with respect to the diversity of amino acid metabolism in microbes. These findings will form an important baseline for interpreting the δ¹⁵N_AA values of organisms and detritus in natural environments.

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Amino acid nitrogen isotopic composition patterns in lacustrine sedimenting matter

Abstract

Introduction

Section snippets

Sampling sites

Nitrate concentrations and isotopic composition

Acknowledgments

Deep Sea Res. Part I

Org. Geochem.

Mar. Chem.

Geochim. Cosmochim. Acta

Org. Geochem.

Geochim. Cosmochim. Acta

Geochim. Cosmochim. Acta

Geochim. Cosmochim. Acta

Geochim. Cosmochim. Acta

Geochim. Cosmochim. Acta

Geochim. Cosmochim. Acta

Deep Sea Res. Part I

Mar. Chem.

Geochim. Cosmochim. Acta

Geochim. Cosmochim. Acta

Acta Oecol.

Effects of Alpine hydropower dams on particle transport and lacustrine sedimentation

Aquat. Sci.

Carbon and nitrogen isotope variations in sedimenting organic matter in Lake Lugano

Limnol. Oceanogr.

Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters

Limnol. Oceanogr.

Eine neue Netzgarnitur mit Kipp-Schliessmechanismus für quantitative Zooplanktonfänge in Seen

Schweiz. Z. Hydrol.

The relative importance of heterotrophic bacteria to pelagic ecosystem dynamics varies with reservoir trophic state

Limnol. Oceanogr.

Metabolic control of nitrogen isotope composition of amino acids in macroalgae and gastropods: implications for aquatic food web studies

Mar. Ecol. Prog. Ser.