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Unexpected Complex Metabolic Responses Between Iron-Cycling Microorganisms

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Unexpected Complex Metabolic Responses Between Iron-Cycling Microorganisms The ISME Journal (2020) 14:2675–2690 https://doi.org/10.1038/s41396-020-0718-z ARTICLE Iron is not everything: unexpected complex metabolic responses between iron-cycling microorganisms 1 1 1,2 2 3 Rebecca E. Cooper ● Carl-Eric Wegner ● Stefan Kügler ● Remington X. Poulin ● Nico Ueberschaar ● 1 2 2 2 1,4 Jens D. Wurlitzer ● Daniel Stettin ● Thomas Wichard ● Georg Pohnert ● Kirsten Küsel Received: 24 March 2020 / Revised: 30 June 2020 / Accepted: 8 July 2020 / Published online: 20 July 2020 © The Author(s) 2020. This article is published with open access Abstract Coexistence of microaerophilic Fe(II)-oxidizers and anaerobic Fe(III)-reducers in environments with fluctuating redox conditions is a prime example of mutualism, in which both partners benefit from the sustained Fe-pool. Consequently, the Fe-cycling machineries (i.e., metal-reducing or –oxidizing pathways) should be most affected during co-cultivation. However, contrasting growth requirements impeded systematic elucidation of their interactions. To disentangle underlying interaction mechanisms, we established a suboxic co-culture system of Sideroxydans sp. CL21 and Shewanella oneidensis. We showed that addition of the partner’s cell-free supernatant enhanced both growth and Fe(II)-oxidizing or Fe(III)-reducing 1234567890();,: 1234567890();,: activity of each partner. Metabolites of the exometabolome of Sideroxydans sp. CL21 are generally upregulated if stimulated with the partner´s spent medium, while S. oneidensis exhibits a mixed metabolic response in accordance with a balanced response to the partner. Surprisingly, RNA-seq analysis revealed genes involved in Fe-cycling were not differentially expressed during co-cultivation. Instead, the most differentially upregulated genes included those encoding for biopolymer production, lipoprotein transport, putrescine biosynthesis, and amino acid degradation suggesting a regulated inter-species biofilm formation. Furthermore, the upregulation of hydrogenases in Sideroxydans sp. CL21 points to competition for H2 as electron donor. Our findings reveal that a complex metabolic and transcriptomic response, but not accelerated formation of Fe-end products, drive interactions of Fe-cycling microorganisms. Introduction [1, 2]. The excreted metabolites can positively affect the growth of co-existing organisms by providing key meta- Chemical communication is often the driving force of bolites produced by one partner and needed by the other [3– mutualistic interactions within microbial communities 8]. The reciprocal benefits resulting from the excretion of metabolites indicate that while each partner invests meta- bolic resources, they both gain something from the other Supplementary information The online version of this article (https:// mutualistic partner [9–11]. Such mechanisms can not only doi.org/10.1038/s41396-020-0718-z) contains supplementary material, control growth but also spatial distribution within the which is available to authorized users. community in cases of heterogeneous environments. Syn- * Kirsten Küsel chronization of lifestyles is particularly important for [email protected] mutualism interaction based on the partner’s end products for energy production [7, 12, 13]. 1 Institute of Biodiversity, Aquatic Geomicrobiology, Friedrich Fe-cycling microorganisms are often found coexisting in Schiller University Jena, Dornburger Strasse 159, 07743 Jena, Germany nature. This is explained by the needs of both the ferrous 2 iron [Fe(II)] oxidizer and ferric iron [Fe(III)] reducer to Institute of Inorganic and Analytical Chemistry, Friedrich Schiller fi University Jena, Lessingstr. 8, 07743 Jena, Germany have suf cient exposure to electron donors and acceptors. For lithoautotrophic Fe(II)-oxidizers, including Gallionella 3 Mass Spectrometry Platform, Faculty of Chemistry and Earth Sciences, Friedrich Schiller University Jena, Humboldstr. 8, 07743 sp. and Sideroxydans lithotrophicus ES-1, Fe(II) serves as Jena, Germany an electron donor under micro-oxic conditions, thereby 4 German Centre for Integrative Biodiversity Research (iDiv) providing ample reducing equivalents for the assimilation of Halle–Jena–Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany carbon [14–17]. Microbial Fe(II) oxidation facilitates the 2676 R. E. Cooper et al. rapid precipitation of Fe(III) oxy-hydroxide nanoparticles Materials and methods [18, 19], which are preferred by anaerobic heterotrophic Fe (III)-reducers, such as Shewanella spp. or Geobacter spp., Bacterial strains and cultivation conditions due to their small mineral size [20–23]. For Fe-cycling, at least temporary access to oxygen, or to oxidized com- Sideroxydans sp. CL21 and S. oneidensis were cultivated in pounds, is necessary for the renewal of the Fe(III) pool liquid supernatant exchange, monoculture, and co-culture [14, 16]. In wetlands or peatlands, this renewal is mediated incubations [15, 30–32] using ATCC medium 2672 (mod- by water table fluctuations, bioturbation, or the release of ified Wolfe’s minimal media (MWMM)) amended with 10 oxygen via plant roots [24] which allows interaction mM MES buffer (pH 6.3) unless otherwise noted. Side- between Fe-cycling microorganisms regardless of their roxydans sp. CL21 stock cultures grown in semi-solid different demands for O2. Production of Fe(III)-chelating gradient tubes containing 0.15% agarose-stabilized ligands like riboflavins by Shewanella spp. or the presence MWMM (Biozyme LE Agarose; Biozyme Scientific of natural organic matter with Fe-complexing or electron GmbH, Hessisch Oldendorf, DE) and zero-valent Fe (Fe(0)) shuttling properties can overcome spatial restrictions and were used as inoculum (1 mL inoculum 100 mL−1 media) in speed up microbial activities [25, 26]. these incubations. Zero-valent iron powder is often used as Interestingly, a shared homology is observed between the source of Fe(II) to cultivate Fe(II)-oxidizing bacteria the genes encoding the Fe(III) reduction machinery located [33], and we observed enhanced biomass during cultivation at the cell surface in S. oneidensis and the genes encoding of Sideroxydans sp. CL21 in semi-solid gradient tubes, in (0) the Fe(II) oxidation machinery of Sideroxydans litho- comparison to FeS or FeCl2.Fe also provided the best Fe trophicus ES-1 [17, 27]. In S. oneidensis,theMtr source for the liquid co-culture incubations. S. oneidensis machinery, comprised of the mtrABC gene cluster, is a overnight cultures were grown aerobically in Luria-Bertani porin–cytochrome complex in the outer membrane medium. 1 mL was transferred into 125 mL serum bottles enabling the electron transport through the outer membrane containing 60 mL MWMM amended with 18 mM lactate via various hemes to Fe(III) [28, 29]. The MtoAB complex and grown aerobically at room temperature. 2 mL of of Sideroxydans is homologous to MtrA and MtrB and MWMM-grown S. oneidensis was harvested after ~14 h functions in the same manner, forming a porin–cytochrome (late exponential growth), centrifuged (10,000 g, 5 min), complex. Thus, we hypothesized that in parallel to the washed twice, resuspended in 2 mL MWMM, and used as exchange of genetic information, additional mutualistic inoculum (final concentration: ~2 × 105 cells mL-1) for the interactions based on the exchange of each partner’s exo- above mentioned incubations. metabolites may have been established between these Fe- cycling partner organisms. Monoculture and co-culture incubations To elucidate these interaction mechanisms, co-culture systems are needed to facilitate downstream analytics on Monocultures and co-cultures were set up in triplicates in both the transcriptome and metabolome levels. But, co- 125 mL serum bottles with an Fe(0)-containing bottom-layer cultivation of Fe-cycling microorganisms is very chal- plug (10 mL MWMM, 3% agarose (Biozyme LE Agarose), −1 (0) lenging due to their different lifestyles for O2. We selected 1gL Fe ). Following solidification, 60 mL MWMM two model microorganisms, the microaerophilic, auto- amended with 1 mM lactate was dispensed on top and trophic Fe(II)-oxidizer Sideroxydans sp. CL21 isolated continuously flushed with an N2:CO2:O2, 78:20:2, (flow from Schlöppnerbrunnen fen [15] and closely related to rate: 300 mL min−1) gas mixture to maintain a micro-oxic Sideroxydans lithotrophicus ES-1 [17], and the facultative environment (Fig. 1a). Cells were harvested at four time- anaerobic Fe(III)-reducer S. oneidensis isolated from Lake points (6 h, 3 d, 6 d, 9 d), centrifuged) and stored at −80 °C. Oneida, NY [30]. First, we optimized incubation condi- 6 d samples were selected for RNA-Seq. tions that allow both partners to thrive simultaneously. The co-cultivation design allowed us to explore the Cell-free supernatant exchange experiment influence of exposure to the partner’s end product for energy production by analyzing changes in 16S rRNA Supernatant exchange experiments were set up in triplicates gene copies, RNA-seq analysis, and metabolomics. We according to Mori et al. [34], with the following modifica- hypothesized that co-cultivation will lead to an acceler- tions: Sideroxydans sp. CL21 and S. oneidensis cultures ated iron wheel (Fe(II) ↔ Fe(III)), because the Fe-cycling were grown in 200 mL MWMM amended with 1 mM machinery would be the most affected during co- lactate and 1.2 mM FeSO4 or 10 mM hydrous Fe(III) cultivation. In addition, we tested the effect of the exo- oxyhydroxide, respectively, for 4 days with shaking at metabolome of one partner organism on the activity of room temperature. Cultures were centrifuged,
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