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

• Published in: The ISME Journal Vol. 16; no. 4; pp. 1153 - 1162
• Main Authors: Taubert, Martin, Overholt, Will A., Heinze, Beatrix M., Matanfack, Georgette Azemtsop, Houhou, Rola, Jehmlich, Nico, von Bergen, Martin, Rösch, Petra, Popp, Jürgen, Küsel, Kirsten
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01-04-2022; Nature Publishing Group
• Subjects: 45/23; 631/326/171/1878; 704/158/855; 82/58; Abundance; Autotrophs; Biomedical and Life Sciences; Carbon; Carbon 13; Carbon dioxide; Carbon dioxide fixation; Cluster analysis; Ecology; Evolutionary Biology; Fitness; Fixation; Groundwater; Lakes; Life Sciences; Metagenomics; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Microbiota; Microcosms; Microorganisms; Organic carbon; Organic compounds; Photosynthesis; Primary production; Remineralization; Stable isotopes; Sulfur; Sulfur compounds; Upper ocean
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-021-01163-x

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 CO
2
fixation is an integral component of subsurface trophic webs. To understand the impact of autotrophically fixed carbon, the flux of CO
2
-derived carbon through various populations of subsurface microbiota must first be resolved, both quantitatively and temporally. Here we implement novel Stable Isotope Cluster Analysis to render a time-resolved and quantitative evaluation of
13
CO
2
-derived carbon flow through a groundwater community in microcosms stimulated with reduced sulfur compounds. We demonstrate that mixotrophs, not strict autotrophs, were the most abundant active organisms in groundwater microcosms. Species of
Hydrogenophaga
,
Polaromonas
,
Dechloromonas
, and other metabolically versatile mixotrophs drove the production and remineralization of organic carbon. Their activity facilitated the replacement of 43% and 80% of total microbial carbon stores in the groundwater microcosms with
13
C in just 21 and 70 days, respectively. The mixotrophs employed different strategies for satisfying their carbon requirements by balancing CO
2
fixation and uptake of available organic compounds. These different strategies might provide fitness under nutrient-limited conditions, explaining the great abundances of mixotrophs in other oligotrophic habitats, such as the upper ocean and boreal lakes.