Dataset Information

Sulfur-fueled chemolithoautotrophs replenish organic carbon inventory in groundwater

ABSTRACT: 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.

INSTRUMENT(S): Q Exactive HF

ORGANISM(S): Escherichia Coli

SUBMITTER: Nico Jehmlich

LAB HEAD: Nico Jehmlich

PROVIDER: PXD024889 | Pride | 2022-05-20

REPOSITORIES: Pride

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			Action	DRS
	190615_NJ_Taubert_12CT1A.msf	Msf
	190615_NJ_Taubert_12CT1A.raw	Raw
	190615_NJ_Taubert_12CT1B.msf	Msf
	190615_NJ_Taubert_12CT1B.raw	Raw
	190615_NJ_Taubert_12CT1C.msf	Msf

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Publications

Bolstering fitness via CO2 fixation and organic carbon uptake: mixotrophs in modern groundwater.

Taubert Martin M Overholt Will A WA Heinze Beatrix M BM Matanfack Georgette Azemtsop GA Houhou Rola R Jehmlich Nico N von Bergen Martin M Rösch Petra P Popp Jürgen J Küsel Kirsten K

The ISME journal 20211207 4

Current understanding of organic carbon inputs into ecosystems lacking photosynthetic primary production is predicated on data and inferences derived almost entirely from metagenomic analyses. The elevated abundances of putative chemolithoautotrophs in groundwaters suggest that dark CO2 fixation is an integral component of subsurface trophic webs. To understand the impact of autotrophically fixed carbon, the flux of CO2-derived carbon through various populations of subsurfa ...[more]

PMID: 34876683

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Project description:Pelagic aggregates function as hotspots for microbial activity and biological carbon pumps for exporting OM fixed by photoautotrophs to sediments in lakes and oceans. In iron-rich (ferruginous) lakes, photoferrotrophic or chemolithoautotrophic bacteria appear to contribute to CO2 fixation by oxidizing reduced iron which leads to the formation of iron-rich pelagic aggregates called iron-snow. In acidic lakes, iron snow is colonized mainly by acidophilic iron-cycling microbes that can trigger interspecies aggregation mechanisms. However, the significance of iron oxidizers in carbon fixation, their general role in iron snow functioning, and the flow of carbon within iron snow is still unclear. Here, we combined a two-year metatranscriptome analysis with a 13CO2 metabolic labeling approach to determine general metabolic activities. Protein-based stable isotope probing (protein-SIP) was used to trace the 13CO2 incorporation in iron snow microcosms over time under both oxic and anoxic conditions. Analysis of our mRNA-derived metatranscriptome data identified four key players (Leptospirillum, Ferrovum, Acidithrix, Acidiphilium) with relative abundances (59.6%-85.7%) in iron snow encoding a variety of ecologically relevant pathways, including carbon fixation, polysaccharide biosynthesis, and flagellar-based motility. We did not detect transcriptional activity for carbon fixation from archaea or eukaryotes. The largest numbers of expressed genes (3008, 2991, 2936) matched to the genomes of our previously obtained iron snow isolates (Acidithrix sp. C25, Acidiphilium sp. C61, Acidocella sp. C78) separately. 13CO2 incorporation studies identified Leptospirillum and Ferrovum, as the main active chemolithoautotrophs under oxic conditions, and Ferrovum was the main active organism under anoxic conditions as well. Small amounts of labeled 13C (Relative isotope abundance: 1.0%-5.3%) were found in the heterotrophic Acidiphilium and Acidocella. Overall, our data show that iron oxidizers play an important role in the formation of iron minerals and CO2 fixation, but the majority of fixed C apparently did not reach other iron snow microbes. This finding suggests that most of the fixed C will be directly exported to the sediment without feeding heterotrophs in the water column in acidic ferruginous lakes.

Dataset Information

Sulfur-fueled chemolithoautotrophs replenish organic carbon inventory in groundwater

Dataset's files

Publications

Bolstering fitness via CO<sub>2</sub> fixation and organic carbon uptake: mixotrophs in modern groundwater.

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