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Versatile Mixotrophs Employ CO2 Fixation As Fill-Up Function

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Versatile Mixotrophs Employ CO2 Fixation As Fill-Up Function bioRxiv preprint doi: https://doi.org/10.1101/2021.01.26.428071; this version posted April 21, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Versatile mixotrophs employ CO2 fixation as 2 fill-up function to dominate in modern 3 groundwater 4 Martin Taubert1,+, Will A. Overholt1, Beatrix M. Heinze1, Georgette Azemtsop Matanfack2,5, Rola 5 Houhou2,5, Nico Jehmlich3, Martin von Bergen3,4, Petra Rösch2, Jürgen Popp2,5, Kirsten Küsel1,6 6 1Aquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University Jena, Dornburger Str. 7 159, 07743 Jena, Germany 8 2Institute of Physical Chemistry and Abbe Center of Photonics, Friedrich Schiller University Jena, 9 Helmholtzweg 4, 07743 Jena, Germany 10 3Department of Molecular Systems Biology, Helmholtz Centre for Environmental Research – UFZ, 11 Permoserstrasse 15, 04318 Leipzig, Germany 12 4Institute of Biochemistry, Faculty of Biosciences, Pharmacy and Psychology, University of Leipzig, 13 Brüderstraße 32, 04103 Leipzig, Germany 14 5Leibniz-Institute of Photonic Technology, Albert-Einstein-Straße 9, 07745 Jena, Germany 15 6German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5E, 16 04103 Leipzig, Germany 17 +Corresponding author: Martin Taubert; Tel.: +49 3641 949459; Fax: +49 3641 949402; E-mail: 18 [email protected] 13 19 Keywords: Chemolithoautotrophy, groundwater, CO2 stable isotope probing, genome-resolved 20 metaproteomics, metagenomics, Raman microspectroscopy 21 Short title: Chemolithoautotrophy in shallow groundwater 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.01.26.428071; this version posted April 21, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 22 Abstract 23 The processes for organic carbon inputs in ecosystems without photosynthetic primary production 24 are poorly constrained, by data almost entirely derived from metagenomics studies. In modern 25 groundwater, such studies reported a high abundance of putative chemolithoautotrophs. Here we 26 quantitatively and temporally tracked the flux of CO2-derived carbon in a groundwater microbial 13 27 community stimulated with reduced sulfur compounds, by combining CO2-stable isotope probing, 28 multi-omics and Raman microspectroscopy. We demonstrate that metabolically flexible mixotrophs 29 drove the recycling of organic carbon and supplemented their carbon requirements by 30 chemolithoautotrophy alongside the preferential uptake of available organic compounds. These 31 mixotrophs, including Hydrogenophaga, Polaromonas and Dechloromonas, dominated the microbial 32 community, being five times more abundant than strict autotrophs based on metagenomics 33 coverage. Due to their activity, 43% of total microbial carbon was replaced by 13C within 21 days, 34 increasing to 80% after 70 days. Sixteen of 31 taxa investigated, including both autotrophs and 35 heterotrophs, were supported by sulfur oxidation pathways, highlighting its importance as an energy 36 source in an environment with little available organic carbon. The versatile strategy employed by 37 these organisms might also be successful in other oligotrophic habitats, like the upper ocean or 38 boreal lakes, explaining the high abundance of mixotrophs found there. 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.01.26.428071; this version posted April 21, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 39 From soils to deep-sea sediments, the majority of cells on Earth have to survive in environments 40 without photosynthetic primary production [1]. To understand the global carbon cycle, it is critical to 41 know to what extent these cells depend on allochthonous carbon for a heterotrophic lifestyle, or on 42 chemolithoautotrophy. The determination of CO2 fixation rates and turnover is challenging in these 43 habitats, but metagenomics studies recovered thousands of metagenome-assembled genomes 44 (MAGs) from the organisms present to shed light on their metabolic capabilities [2-5]. 45 Modern groundwater, having entered the subsurface less than 50 years ago [6], represents a 46 transitionary ecosystem, connecting surface habitats dominated by photosynthetic carbon with the 47 deep subsurface that lacks this energy source [7-9]. There, metagenomics studies have unveiled the 48 presence of a variety of organisms with the metabolic potential for CO2 fixation and for the utilization 49 of inorganic electron donors [4, 10-13]. Such organisms with the ability to grow 50 chemolithoautotrophically constitute between 12 and 47% of the microbial communities in 51 groundwater [14-17]. These discoveries shake the paradigm that modern groundwater is primarily 52 fueled by surface input of organic material and dominated by heterotrophs. We thus hypothesize 53 that modern groundwater ecosystems are dominated by chemolithoautotrophic primary production. 54 For validating this hypothesis, we established Stable Isotope Cluster Analysis (SIsCA) to provide a 55 time-resolved and quantitative assessment of the flow of CO2-derived carbon through the 56 groundwater microbial food web. By combining stable isotope probing (SIP) [18, 19] with genome- 57 resolved metaproteomics, we leveraged the high sensitivity of Orbitrap mass spectrometry in SIP- 58 metaproteomics to acquire highly accurate quantitative data on 13C incorporation [20, 21]. The novel 59 SIsCA method then employs a dimensionality reduction approach to integrate the molecule-specific 60 temporal dynamics in the acquired isotopologue patterns from this 13C-SIP time-series experiment, to 61 discern trophic fluxes between individual members of a microbial community. 62 We employed this approach to unravel the role of chemolithoautotrophy for the groundwater 13 63 microbiome by amending groundwater microcosms with CO2. In modern groundwater, different 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.01.26.428071; this version posted April 21, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 64 inorganic electron donors like reduced nitrogen, iron and sulfur can fuel the chemolithoautotrophic 65 primary production, while hydrogen is rather of relevance in the deeper subsurface [9, 22-24]. 66 Reduced sulfur compounds released from aquifer rocks by weathering create an energy source 67 independent of surface inputs [25-27]. Organisms with the genetic potential to oxidize reduced sulfur 68 compounds are widespread in groundwater, but little is known about their lifestyle [12, 13, 28]. 69 Hence, we stimulated sulfur oxidizers in groundwater microcosms by the addition of thiosulfate, 70 which is commonly found in the environment [29]. Under these conditions favoring lithotrophic 71 growth, we expected chemolithoautotrophy to be the main source of organic carbon, and a 72 unidirectional carbon flux from autotrophs to heterotrophs in the groundwater microbiome. By 73 mapping the quantitative information derived from SIsCA to MAGs, we were able to characterize 74 carbon utilization and trophic interactions of the active autotrophic and heterotrophic key players in 75 the groundwater microbiome over a period of 70 days. This accurate resolution of the carbon fluxes 76 through a microbial community and the determination of taxon-specific microbial activities have the 77 power to provide novel insights into the metabolic strategies and trophic interactions of microbes. 78 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.01.26.428071; this version posted April 21, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 79 Materials and Methods 80 Groundwater sampling & setup of groundwater microcosms 81 Groundwater was obtained in June 2018 from the Hainich Critical Zone Exploratory (CZE) well H41 82 (51.1150842N, 10.4479713E), accessing an aquifer assemblage in 48 m depth in a trochite limestone 83 stratum. Groundwater from this well is oxic with average dissolved oxygen concentrations of 5.0 ± 84 1.5 mg L-1, pH 7.2, < 0.1 mg L-1 ammonium, 1.9 ± 1.5 mg L-1 dissolved organic carbon, and 70.8 ± 12.7 85 mg L-1 total inorganic carbon [27, 30]. The recharge area of this aquifer assemblage is located in a 86 beech forest (Fagus sylvatica). In total, 120 L of groundwater was sampled using a submersible pump 87 (Grundfos MP1, Grundfos, Bjerringbro, Denmark). To collect biomass from the groundwater, 5 L each 88 were filtered through twenty 0.2-µm Supor filters (Pall Corporation, Port Washington, NY, USA). To 89 replace the natural background of inorganic carbon in the groundwater by defined concentrations of 90 12C or 13C, two times 3 L of filtered groundwater were acidified to pH 4 in 5-L-bottles to remove the 91 bicarbonate
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