Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

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.

This is a preview of subscription content, access via your institution

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

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.

References

  1. Hui S, Silverman JM, Chen SS, Erickson DW, Basan M, Wang J, et al. Quantitative proteomic analysis reveals a simple strategy of global resource allocation in bacteria. Mol Syst Biol. 2015;11:784.

    PubMed  PubMed Central  Google Scholar 

  2. You C, Okano H, Hui S, Zhang Z, Kim M, Gunderson CW, et al. Coordination of bacterial proteome with metabolism by cyclic AMP signalling. Nature. 2013;500:301–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Scott M, Gunderson CW, Mateescu EM, Zhang Z, Hwa T. Interdependence of cell growth and gene expression: origins and consequences. Science. 2010;330:1099–102.

    CAS  PubMed  Google Scholar 

  4. Makman RS, Sutherland EW. Adenosine 3’,5’-phosphate in Escherichia Coli. J Biol Chem. 1965;240:1309–14.

    CAS  PubMed  Google Scholar 

  5. Kochanowski K, Okano H, Patsalo V, Williamson J, Sauer U, Hwa T. Global coordination of metabolic pathways in Escherichia coli by active and passive regulation. Mol Syst Biol. 2021;17:1–14.

    Google Scholar 

  6. Basan M, Hui S, Okano H, Zhang Z, Shen Y, Williamson JR, et al. Overflow metabolism in Escherichia coli results from efficient proteome allocation. Nature. 2015;528:99–104.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Larsson C, Von Stockar U, Marison I, Gustafsson L. Growth and metabolism of Saccharomyces cerevisiae in chemostat cultures under carbon-, nitrogen-, or carbon- and nitrogen-limiting conditions. J Bacteriol. 1993;175:4809–16.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Dai X, Zhu M, Warren M, Balakrishnan R, Patsalo V, Okano H, et al. Reduction of translating ribosomes enables Escherichia coli to maintain elongation rates during slow growth. Nat Microbiol. 2016;2:1–9.

    Google Scholar 

  9. Basan M, Zhu M, Dai X, Warren M, Sévin D, Wang Y, et al. Inflating bacterial cells by increased protein synthesis. Mol Syst Biol. 2015;11:836.

    PubMed  PubMed Central  Google Scholar 

  10. Müller AL, Gu W, Patsalo V, Deutzmann JS, Williamson JR, Spormann AM. An alternative resource allocation strategy in the chemolithoautotrophic archaeon Methanococcus maripaludis. Proc Natl Acad Sci USA. 2021;118:1–8.

    Google Scholar 

  11. Smil V. Phosphorus in the environment: natural flows and human Interferences. Annual Review of Energy and the Environment; Palo Alto. 2000;25:53.

  12. Schindler DW. Evolution of phosphorus limitation in lakes. Science. 1977;195:260–2.

    CAS  PubMed  Google Scholar 

  13. Müller S, Mitrovic SM. Phytoplankton co-limitation by nitrogen and phosphorus in a shallow reservoir: progressing from the phosphorus limitation paradigm. Hydrobiologia. 2015;744:255–69.

    Google Scholar 

  14. Garcia NS, Bonachela JA, Martiny AC. Interactions between growth-dependent changes in cell size, nutrient supply and cellular elemental stoichiometry of marine. Synechococcus ISME J. 2016;10:2715–24.

    CAS  PubMed  Google Scholar 

  15. Arne Alphenaar P, Sleyster R, De Reuver P, Ligthart GJ, Lettinga G. Phosphorus requirement in high-rate anaerobic wastewater treatment. Water Res. 1993;27:749–56.

    Google Scholar 

  16. Miettinen IT, Vartiainen T, Martikainen PJ. Phosphorus and bacterial growth in drinking water. Appl Environ Microbiol. 1997;63:3242–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Shropshire H, Jones RA, Aguilo-Ferretjans MM, Scanlan DJ, Chen Y. Proteomics insights into the Burkholderia cenocepacia phosphorus stress response. Environ Microbiol. 2021;23:5069–86.

    CAS  PubMed  Google Scholar 

  18. Jones RA, Shropshire H, Zhao C, Murphy A, Lidbury I, Wei T, et al. Phosphorus stress induces the synthesis of novel glycolipids in Pseudomonas aeruginosa that confer protection against a last-resort antibiotic. ISME J. 2021;15:3303–14.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Li SHJ, Li Z, Park JO, King CG, Rabinowitz JD, Wingreen NS, et al. Escherichia coli translation strategies differ across carbon, nitrogen and phosphorus limitation conditions. Nat Microbiol. 2018;3:939–47.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Costa KC, Wong PM, Wang T, Lie TJ, Dodsworth JA, Swanson I, et al. Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase. Proc Natl Acad Sci USA. 2010;107:11050–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B. 1995;57:289–300.

    Google Scholar 

  22. Tyanova S, Temu T, Cox J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat Protoc. 2016;11:2301–19.

    CAS  PubMed  Google Scholar 

  23. De Poorter LMI, Geerts WJ, Keltjens JT. Coupling of Methanothermobacter thermautotrophicus methane formation and growth in fed-batch and continuous cultures under different H2 gassing regimens. Appl Environ Microbiol. 2007;73:740–9.

    PubMed  Google Scholar 

  24. Schönheit P, Moll J, Thauer RK. Growth parameters (Ks, μmax, Ys) of Methanobacterium thermoautotrophicum. Arch Microbiol. 1980;127:59–65.

    Google Scholar 

  25. Chaban B, Ng SYM, Kanbe M, Saltzman I, Nimmo G, Aizawa SI, et al. Systematic deletion analyses of the fla genes in the flagella operon identify several genes essential for proper assembly and function of flagella in the archaeon, Methanococcus maripaludis. Mol Microbiol. 2007;66:596–609.

    CAS  PubMed  Google Scholar 

  26. Albers SV, Jarrell KF. The archaellum: how Archaea swim. Front Microbiol. 2015;6:1–12.

    Google Scholar 

  27. Whitman WB, Shieh J, Sohn S, Caras DS, Premachandran U. Isolation and characterization of 22 mesophilic methanococci. Syst Appl Microbiol. 1986;7:235–40.

    Google Scholar 

  28. Kaster AK, Moll J, Parey K, Thauer RK. Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea. Proc Natl Acad Sci USA. 2011;108:2981–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Shieh J, Whitman WB. Autotrophic acetyl coenzyme A biosynthesis in Methanococcus maripaludis. J Bacteriol. 1988;170:3072–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Major TA, Liu Y, Whitman WB. Characterization of energy-conserving hydrogenase B in Methanococcus maripaludis. J Bacteriol. 2010;192:4022–30.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Lie TJ, Costa KC, Lupa B, Korpole S, Whitman WB, Leigh JA. Essential anaplerotic role for the energy-converting hydrogenase Eha in hydrogenotrophic methanogenesis. Proc Natl Acad Sci USA. 2012;109:15473–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Brauer M, Huttenhower C, Airoldi EM, Rosenstein R, Matese JC, Gresham D, et al. Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast. Mol Biol Cell. 2008;19:352–67.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Hendrickson EL, Liu Y, Rosas-Sandoval G, Porat I, Söll D, Whitman WB, et al. Global responses of Methanococcus maripaludis to specific nutrient limitations and growth rate. J Bacteriol. 2008;190:2198–205.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Archer DB. Uncoupling of methanogenesis from growth of Methanosarcina barkeri by phosphate limitation. Appl Environ Microbiol. 1985;50:1233–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Seely RJ, Fahrney DE. Levels of cyclic-2,3-diphosphoglycerate in Methanobacterium thermoautotrophicum during phosphate limitation. J Bacteriol. 1984;160:50–54.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Tommassen J, de Geus P, Lugtenberg B, Hackett J, Reeves P. Regulation of the pho regulon of Escherichia coli K-12: cloning of the regulatory genes phoB and phoR and identification of their gene products. J Mol Biol. 1982;157:265–74.

    CAS  PubMed  Google Scholar 

  37. Hulett FM. The signal-transduction network for Pho regulation in Bacillus subtilis. Mol Microbiol. 1996;19:933–9.

    CAS  PubMed  Google Scholar 

  38. Novak R, Cauwels A, Charpentier E, Tuomanen E. Identification of a Streptococcus pneumoniae gene locus encoding proteins of an ABC phosphate transporter and a two-component regulatory system. J Bacteriol. 1999;181:1126–33.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Kočan M, Schaffer S, Ishige T, Sorger-Herrmann U, Wendisch VF, Bott M. Two-component systems of Corynebacterium glutamicum: deletion analysis and involvement of the phoS-phoR system in the phosphate starvation response. J Bacteriol. 2006;188:724–32.

    PubMed  PubMed Central  Google Scholar 

  40. Wende A, Furtwängler K, Oesterhelt D. Phosphate-dependent behavior of the archaeon Halobacterium salinarum strain R1. J Bacteriol. 2009;191:3852–60.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Akinyemi TS, Shao N, Lyu Z, Drake IJ, Liu Y, Whitman WB. Tuning gene expression by phosphate in the methanogenic archaeon Methanococcus maripaludis. ACS Synth Biol. 2021;10:3028–39.

    CAS  PubMed  Google Scholar 

  42. Xia Q, Wang T, Hendrickson EL, Lie TJ, Hackett M, Leigh JA. Quantitative proteomics of nutrient limitation in the hydrogenotrophic methanogen Methanococcus maripaludis. BMC Microbiol. 2009;9:1–10.

    Google Scholar 

  43. Paula FS, Chin JP, Schnürer A, Müller B, Manesiotis P, Waters N, et al. The potential for polyphosphate metabolism in Archaea and anaerobic polyphosphate formation in Methanosarcina mazei. Sci Rep. 2019;9:1–12.

    Google Scholar 

  44. König H, Nusser E, Stetter KO. Glycogen in Methanolobus and Methanococcus. FEMS Microbiol Lett. 1985;28:265–9.

    Google Scholar 

  45. Rudnick H, Hendrich S, Pilatus U, Blotevogel KH. Phosphate accumulation and the occurrence of polyphosphates and cyclic 2,3-diphosphoglycerate in Methanosarcina frisia. Arch Microbiol. 1990;154:584–8.

    CAS  Google Scholar 

  46. Shalvarjian KE, Nayak DD. Transcriptional regulation of methanogenic metabolism in archaea. Curr Opin Microbiol. 2021;60:8–15.

    CAS  PubMed  Google Scholar 

  47. Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol. 2008;6:579–91.

  48. Goyal N, Zhou Z, Karimi IA. Metabolic processes of Methanococcus maripaludis and potential applications. Micro Cell Fact. 2016;15:1–19.

    Google Scholar 

  49. Simpson PG, Whitman WB. Anabolic pathways in methanogens. In: Methanogenesis. Boston, MA: Springer; 1993. p. 445–72.

  50. Dai X, Zhu M. Coupling of ribosome synthesis and translational capacity with cell growth. Trends Biochem Sci. 2020;45:681–92.

    CAS  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Alfred M. Spormann.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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 16, 2313–2319 (2022). https://doi.org/10.1038/s41396-022-01278-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41396-022-01278-9

Search

Quick links