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Growth rate-dependent coordination of catabolism and anabolism in the archaeon Methanococcus maripaludis under phosphate limitation

The ISME Journal (2022)Cite this article

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Abstract

Catabolic and anabolic processes are finely coordinated in microorganisms to provide optimized fitness under varying environmental conditions. Understanding this coordination and the resulting physiological traits reveals fundamental strategies of microbial acclimation. Here, we characterized the system-level physiology of Methanococcus maripaludis, a niche-specialized methanogenic archaeon, at different dilution rates ranging from 0.09 to 0.003 h−1 in chemostat experiments under phosphate (i.e., anabolic) limitation. Phosphate was supplied as the limiting nutrient, while formate was supplied in excess as the catabolic substrate and carbon source. We observed a decoupling of catabolism and anabolism resulting in lower biomass yield relative to catabolically limited cells at the same dilution rates. In addition, the mass abundance of several coarse-grained proteome sectors (i.e., combined abundance of proteins grouped based on their function) exhibited a linear relationship with growth rate, mostly ribosomes and their biogenesis. Accordingly, cellular RNA content also correlated with growth rate. Although the methanogenesis proteome sector was invariant, the metabolic capacity for methanogenesis, measured as methane production rates immediately after transfer to batch culture, correlated with growth rate suggesting translationally independent regulation that allows cells to only increase catabolic activity under growth-permissible conditions. These observations are in stark contrast to the physiology of M. maripaludis under formate (i.e., catabolic) limitation, where cells keep an invariant proteome including ribosomal content and a high methanogenesis capacity across a wide range of growth rates. Our findings reveal that M. maripaludis employs fundamentally different strategies to coordinate global physiology during anabolic phosphate and catabolic formate limitation.

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Fig. 1: Proteome allocation at different growth rates.
Fig. 2: Methane production rates and methanogenesis capacities at different growth rates.
Fig. 3: Macromolecular composition and cell size of M. maripaludis at different growth rates, showing data from chemostat-grown cells (filled diamonds) under phosphate- (gold, this study) and formate- (black, [10]) limited conditions and exponential phase batch culture samples (open diamonds).
Fig. 4: Ribosome activity of M. maripaludis at different growth rates, showing data from chemostat-grown cells (filled diamonds) under phosphate- (gold, this study) and formate- (black, [10]) limited conditions and exponential phase batch culture samples (open diamonds).
Fig. 5: Metabolic pathways and proteome allocation in M. maripaludis.

Data availability

The mass spectrometry proteomics data are available in the MassIVE database (https://massive.ucsd.edu) under accession number MSV000087621.

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Acknowledgements

We thank Dr. Vadim Patsalo for recording and analyzing the proteomic mass spectrometry data. This work is supported by grants from the US Army Research Office (W911NF2010111 to AMS) and National Science Foundation/University of Southern California, Center for Dark Energy Biosphere Investigations (OCE-0939564), and a grant from the National Institutes of Health (R35-GM136412 to JRW).

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  1. These authors contributed equally: Wenyu Gu, Albert L. Müller.

Authors and Affiliations

  1. Department of Civil and Environmental Engineering, Stanford University, Stanford, CA, USA

    Wenyu Gu, Albert L. Müller, Jörg S. Deutzmann & Alfred M. Spormann

  2. Department of Integrative Structural and Computational Biology, Department of Chemistry, The Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, CA, USA

    James R. Williamson

  3. Department of Chemical Engineering, Stanford University, Stanford, CA, USA

    Alfred M. Spormann

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WG, ALM, and AMS conceived and designed the experiments. WG and ALM performed the experiments and analyzed the data. All authors contributed materials/analysis tools. All authors contributed to the writing of the manuscript.

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Correspondence to Alfred M. Spormann.

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Gu, W., Müller, A.L., Deutzmann, J.S. et al. Growth rate-dependent coordination of catabolism and anabolism in the archaeon Methanococcus maripaludis under phosphate limitation. ISME J (2022). https://doi.org/10.1038/s41396-022-01278-9

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