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A shotgun metabolomics approach to characterize the dissolved organic matter pool in the Samail Ophiolite aquifer

ABSTRACT: The process of serpentinization has been implicated in supporting life on both early Earth and other worlds in our Solar System. While numerous studies have provided clues to the survival strategies of microbial communities in serpentinizing environments on modern Earth, characterizing microbial activity in such environments remains challenging. Here, we use an untargeted metabolomics approach to characterize dissolved organic matter in groundwater in the Samail Ophiolite, the largest and best characterized example of an actively serpentinizing uplifted ocean crust and mantle. We found that dissolved organic matter composition strongly correlated to both fluid type and microbial community composition, and that the fluids that were most influenced by serpentinization contained the greatest number of unique compounds, none of which could be identified using the current metabolite databases. Using metabolomics in conjunction with metagenomic data, we detected numerous products and intermediates of microbial metabolic processes and identified potential biosignatures of microbial activity, including pigments, porphyrins, quinones, fatty acids, and metabolites involved in methanogenesis. Metabolomics techniques like the ones used in this study may be used to further our understanding of life in serpentinizing environments, and aid in the identification of biosignatures that can be used to search for life in serpentinizing systems on other worlds.

INSTRUMENT(S): Liquid Chromatography MS - negative - reverse phase

PROVIDER: MTBLS6081 | MetaboLights | 2023-03-02

REPOSITORIES: MetaboLights

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			Action	DRS
	XS1_2017_05_08_LS_001.mzML	Mzml
	XS1_2017_05_08_LS_001.raw.zip	Raw
	XS1_2017_05_08_LS_002.mzML	Mzml
	XS1_2017_05_08_LS_002.raw.zip	Raw
	XS1_2017_05_08_LS_003.mzML	Mzml

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Project description:Metagenome-assembled genomes (MAGs) have revealed the existence of novel bacterial and archaeal groups and provided insight into their genetic potential. However, metagenomics and even metatranscriptomics cannot resolve how the genetic potential translates into metabolic functions and physiological activity. Here, we present a novel approach for the quantitative and organism-specific assessment of the carbon flux through microbial communities with stable isotope probing-metaproteomics and integration of temporal dynamics in 13C incorporation by Stable Isotope Cluster Analysis (SIsCA). We used groundwater microcosms labeled with 13CO2 and D2O as model systems and stimulated them with reduced sulfur compounds to determine the ecosystem role of chemolithoautotrophic primary production. Raman microspectroscopy detected rapid deuterium incorporation in microbial cells from 12 days onwards, indicating activity of the groundwater organisms. SIsCA revealed that groundwater microorganisms fell into five distinct carbon assimilation strategies. Only one of these strategies, comprising less than 3.5% of the community, consisted of obligate autotrophs (Thiobacillus), with a 13C incorporation of approximately 95%. Instead, mixotrophic growth was the most successful strategy, and was represented by 12 of the 15 MAGs expressing pathways for autotrophic CO2 fixation, including Hydrogenophaga, Polaromonas and Dechloromonas, with varying 13C incorporation between 5% and 90%. Within 21 days, 43% of carbon in the community was replaced by 13C, increasing to 80% after 70 days. Of the 31 most abundant MAGs, 16 expressed pathways for sulfur oxidation, including strict heterotrophs. We concluded that chemolithoautotrophy drives the recycling of organic carbon and serves as a fill-up function in the groundwater. Mixotrophs preferred the uptake of organic carbon over the fixation of CO2, and heterotrophs oxidize inorganic compounds to preserve organic carbon. Our study showcases how next-generation physiology approach like SIsCA can move beyond metagenomics studies by providing information about expression of metabolic pathways and elucidating the role of MAGs in ecosystem functioning.

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A shotgun metabolomics approach to characterize the dissolved organic matter pool in the Samail Ophiolite aquifer

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