Abstract
Different microbial cell types typically specialize at performing different metabolic processes. A canonical example is substrate cross-feeding, where one cell type consumes a primary substrate into an intermediate and another cell type consumes the intermediate. While substrate cross-feeding is widely observed, its consequences on ecosystem processes is often unclear. How does substrate cross-feeding affect the rate or extent of substrate consumption? We hypothesized that substrate cross-feeding eliminates competition between different enzymes and reduces the accumulation of growth-inhibiting intermediates, thus accelerating substrate consumption. We tested this hypothesis using isogenic mutants of the bacterium Pseudomonas stutzeri that either completely consume nitrate to dinitrogen gas or cross-feed the intermediate nitrite. We demonstrate that nitrite cross-feeding eliminates inter-enzyme competition and, in turn, reduces nitrite accumulation. We further demonstrate that nitrite cross-feeding accelerates substrate consumption, but only when nitrite has growth-inhibiting effects. Knowledge about inter-enzyme competition and the inhibitory effects of intermediates could therefore be important for deciding how to best segregate different metabolic processes into different microbial cell types to optimize a desired biotransformation.
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Acknowledgements
We thank two anonymous reviewers for significantly improving the quality of this manuscript; Martin Ackermann, Sebastian Bonhoeffer, Jan Dolinsek, Felix Goldschmidt, Frank Schreiber and Simon van Vliet for useful discussions; William Metcalf for generously providing plasmids and strains used for this study; Anja Bernet and Selina Derksen-Müller for assistance with the genetic manipulations; and Thomas Fleischmann for assistance with the chemical analyses. This work was supported by a grant from the Swiss National Science Foundation (grant number 31003A_149304).
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Lilja, E., Johnson, D. Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates. ISME J 10, 1568–1578 (2016). https://doi.org/10.1038/ismej.2015.243
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DOI: https://doi.org/10.1038/ismej.2015.243
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