Interpreting lacustrine bulk sediment d15N values using metagenomics in a tropical hypersaline lake system

Authors: CHEN, MINGFEI - University Of Illinois; CONROY, JESSICA - University Of Illinois; SANFORD, ROBERT - University Of Illinois; Chee Sanford, Joanne; Connor, Lynn

Submitted to: Journal of Paleolimnology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/23/2020
Publication Date: 10/14/2020
Citation: Chen, M., Conroy, J.L., Sanford, R.A., Chee-Sanford, J.C., Connor, L.M. 2020. Interpreting lacustrine bulk sediment d15N values using metagenomics in a tropical hypersaline lake system. Journal of Paleolimnology. 65:151-168. https://doi.org/10.1007/s10933-020-00157-7.
DOI: https://doi.org/10.1007/s10933-020-00157-7

Interpretive Summary: Nutrient cycling processes mediated by microorganisms in terrestrial and aquatic systems are crucial to the productivity and quality of these environments. In an era of climate change, there is a need to understand the effects caused by shifting patterns in microbial populations as they respond to environmental changes. Metagenomic analysis is currently the best technology to characterize the genetic potential (i.e. microbial genes) present in natural environmental samples, allowing observations that reveal changes in microbial populations and their potential activities. While metagenomic technology has rapidly advanced, challenges exist in analyzing the large datasets consisting of hundreds of millions of sequences. In this study, a geochemically well-characterized tropical lake sediment from Christmas Island was used as a model system for metagenomic analysis to determine if the variability in sediment stable isotope nitrogen ratios (d15N) across depth could be linked to signature microbial N-cycling processes. The results showed that the genetic potential displayed by the microbial taxa and the N-cycling genes in the metagenome point to processes of denitrification at the surface, while N-assimilation and ammonification occurred at depth, correlating within the ranges of 15N fractionation factors expected for the respective processes and measured in the corresponding sediment depths. The impact of this work showed the utility of metagenomics used in conjunction with geologic measurements to understand the link between microbial processes and site productivity. Further, the approach is applicable to any type of environmental sample including soils that are expected to be highly complex biologically and chemically across all dimensions.

Technical Abstract: Nitrogen (N) is a limiting nutrient in lacustrine systems, and bulk organic matter (OM) stable isotope ratios of N (d15N) are widely used in lake sediment studies to interpret N source inputs and lake trophic status. Although records of lacustrine sedimentary d15N can provide critical information relating to past environmental change, often productivity interpretations from d15N and lacustrine fossil records yield conflicting interpretations. Furthermore, components of the internal N-cycle have substantial isotopic fractionation factors, and likely wield an enormous influence on bulk lacustrine sedimentary d15N values. Yet apart from cyanobacteria N-fixation, few studies link specific microbial, N-related activity to d15N variability in lake sediment records. Here, we assess the relationship between lacustrine sedimentary d15N and microbiome profiles analyzed from extracted sediment DNA using metagenomics. In a ~1600 year-long sediment record from a hypersaline lake located on Kiritimati, Republic of Kiribati (2°N, 157°W), both d15N and the taxonomy annotations from five unique metagenomes vary with depth. Despite the relatively high abundance of Cyanobacteria, Bacteroidetes and N-fixation genes in the surface sediment, we find the highest d15N values of the sediment record there. These high values are likely due to denitrification, supported by a relatively high abundance of denitrification genes and taxa responsible for denitrification, such as family Chromatiaceae from Gammaproteobacteria. In the deep sediment, N-related biochemical processes are likely suppressed considering the low energy, low nutrient subsurface environment. Low d15N values observed in deeper sediments co-occur with genes for assimilatory nitrate reduction and ammonification. Thus, metagenomics provides greater clarity with respect to the specific, microbial processes that alter primary d15N signatures in the subsurface sediment.