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Microbial storage and its implications for soil ecology

Abstract

Organisms throughout the tree of life accumulate chemical resources, in particular forms or compartments, to secure their availability for future use. Here we review microbial storage and its ecological significance by assembling several rich but disconnected lines of research in microbiology, biogeochemistry, and the ecology of macroscopic organisms. Evidence is drawn from various systems, but we pay particular attention to soils, where microorganisms play crucial roles in global element cycles. An assembly of genus-level data demonstrates the likely prevalence of storage traits in soil. We provide a theoretical basis for microbial storage ecology by distinguishing a spectrum of storage strategies ranging from surplus storage (storage of abundant resources that are not immediately required) to reserve storage (storage of limited resources at the cost of other metabolic functions). This distinction highlights that microorganisms can invest in storage at times of surplus and under conditions of scarcity. We then align storage with trait-based microbial life-history strategies, leading to the hypothesis that ruderal species, which are adapted to disturbance, rely less on storage than microorganisms adapted to stress or high competition. We explore the implications of storage for soil biogeochemistry, microbial biomass, and element transformations and present a process-based model of intracellular carbon storage. Our model indicates that storage can mitigate against stoichiometric imbalances, thereby enhancing biomass growth and resource-use efficiency in the face of unbalanced resources. Given the central roles of microbes in biogeochemical cycles, we propose that microbial storage may be influential on macroscopic scales, from carbon cycling to ecosystem stability.

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Fig. 1: Known microbial storage by genera occurring in soil.
Fig. 2: Schematic of a dynamic microbial model that includes intracellular C storage.
Fig. 3: Modeled effects of storage on microbial processes.

References

  1. 1.

    Pond C. Storage. In: Townsend C, Calow P, editors. Physiological ecology. Oxford: Blackwell Scientific; 1981. p. 190–219.

  2. 2.

    Chapin FS, Schulze E, Mooney HA. The ecology and economics of storage in plants. Annu Rev Ecol Syst. 1990;21:423–47.

    Article  Google Scholar 

  3. 3.

    Moradali MF, Rehm BHA. Bacterial biopolymers: from pathogenesis to advanced materials. Nat Rev Microbiol. 2020;18:195–210.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  4. 4.

    Varpe Ø. Life history adaptations to seasonality. Integr Comp Biol. 2017;57:943–60.

    PubMed  Article  PubMed Central  Google Scholar 

  5. 5.

    Paul EA. Soil microbiology, ecology and biochemistry. 4th ed. Waltham, MA: Academic Press; 2015.

  6. 6.

    Becker KW, Collins JR, Durham BP, Groussman RD, White AE, Fredricks HF, et al. Daily changes in phytoplankton lipidomes reveal mechanisms of energy storage in the open ocean. Nat Commun. 2018;9:1–9.

    Article  CAS  Google Scholar 

  7. 7.

    Rothermich MM, Guerrero R, Lenz RW, Goodwin S. Characterization, seasonal occurrence, and diel fluctuation of poly(hydroxyalkanoate) in photosynthetic microbial mats. Appl Environ Microbiol. 2000;66:13.

    Article  Google Scholar 

  8. 8.

    Borzi A. Le comunicazioni intracellulari delle Nostochinee. Malpighia. 1887;1:28–74.

    Google Scholar 

  9. 9.

    Sherman LA, Meunier P, Colón-López MS. Diurnal rhythms in metabolism: a day in the life of a unicellular, diazotrophic cyanobacterium. Photosynth Res. 1998;58:25–42.

    CAS  Article  Google Scholar 

  10. 10.

    Stuart RK, Mayali X, Boaro AA, Zemla A, Everroad RC, Nilson D, et al. Light regimes shape utilization of extracellular organic C and N in a cyanobacterial biofilm. mBio. 2016;7:e00650–16.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. 11.

    Allen MM. Cyanobacterial cell inclusions. Annu Rev Microbiol. 1984;38:1–25.

    CAS  PubMed  Article  Google Scholar 

  12. 12.

    Sanz-Luque E, Bhaya D, Grossman AR. Polyphosphate: a multifunctional metabolite in cyanobacteria and algae. Front Plant Sci. 2020;11:938.

    PubMed  PubMed Central  Article  Google Scholar 

  13. 13.

    Martin P, Lauro FM, Sarkar A, Goodkin N, Prakash S, Vinayachandran PN. Particulate polyphosphate and alkaline phosphatase activity across a latitudinal transect in the tropical Indian Ocean: polyphosphate in the tropical Indian Ocean. Limnol Oceanogr. 2018;63:1395–406.

    CAS  Article  Google Scholar 

  14. 14.

    Diaz J, Ingall E, Benitez-Nelson C, Paterson D, de Jonge MD, McNulty I, et al. Marine polyphosphate: a key player in geologic phosphorus sequestration. Science. 2008;320:652–5.

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Godwin CM, Cotner JB. Aquatic heterotrophic bacteria have highly flexible phosphorus content and biomass stoichiometry. ISME J. 2015;9:2324–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. 16.

    Oehmen A, Lemos P, Carvalho G, Yuan Z, Keller J, Blackall L, et al. Advances in enhanced biological phosphorus removal: From micro to macro scale. Water Res. 2007;41:2271–300.

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Dorofeev AG, Nikolaev YuA, Mardanov AV, Pimenov NV. Role of phosphate-accumulating bacteria in biological phosphorus removal from wastewater. Appl Biochem Microbiol. 2020;56:1–14.

    CAS  Article  Google Scholar 

  18. 18.

    Carrondo MA. Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J. 2003;22:1959–68.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. 19.

    Canessa P, Larrondo LF. Environmental responses and the control of iron homeostasis in fungal systems. Appl Microbiol Biotechnol. 2013;97:939–55.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. 20.

    Harrison PM, Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta. 1996;1275:161–203.

    PubMed  Article  PubMed Central  Google Scholar 

  21. 21.

    Docampo R, Moreno SNJ. Acidocalcisomes. Cell Calcium. 2011;50:113–9.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    Tsednee M, Castruita M, Salomé PA, Sharma A, Lewis BE, Schmollinger SR, et al. Manganese co-localizes with calcium and phosphorus in Chlamydomonas acidocalcisomes and is mobilized in manganese-deficient conditions. J Biol Chem. 2019;294:17626–41.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Mojzeš P, Gao L, Ismagulova T, Pilátová J, Moudříková Š, Gorelova O, et al. Guanine, a high-capacity and rapid-turnover nitrogen reserve in microalgal cells. Proc Natl Acad Sci USA. 2020;117:32722–30.

  24. 24.

    Turner BL. Inositol phosphates in soil: Amounts, forms and significance of the phosphorylated inositol stereoisomers. In: Turner BL, Richardson AE, Mullaney EJ, editors. Inositol phosphates: linking agriculture and the environment. 2007. Wallingford: CABI; 2007. p. 186–206.

  25. 25.

    Flemming H-C, Wingender J. The biofilm matrix. Nat Rev Microbiol. 2010;8:623–33.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Otero A, Vincenzini M. Nostoc (Cyanophyceae) goes nude: Extracellular polysaccharides serve as a sink for reducing power under unbalanced C/N metabolism. J Phycol. 2004;40:74–81.

    CAS  Article  Google Scholar 

  27. 27.

    Wang J, Yu H-Q. Biosynthesis of polyhydroxybutyrate (PHB) and extracellular polymeric substances (EPS) by Ralstonia eutropha ATCC 17699 in batch cultures. Appl Microbiol Biotechnol. 2007;75:871–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  28. 28.

    Brangarí AC, Fernàndez-Garcia D, Sanchez-Vila X, Manzoni S. Ecological and soil hydraulic implications of microbial responses to stress—a modeling analysis. Adv Water Resour. 2018;116:178–94.

    Article  Google Scholar 

  29. 29.

    Pal S, Manna A, Paul AK. Production of poly(β-hydroxybutyric acid) and exopolysaccharide by Azotobacter beijerinckii WDN-01. World J Microbiol Biotechnol. 1999;15:11–6.

    Article  Google Scholar 

  30. 30.

    Kuzyakov Y, Blagodatskaya E. Microbial hotspots and hot moments in soil: Concept & review. Soil Biol Biochem. 2015;83:184–99.

    CAS  Article  Google Scholar 

  31. 31.

    Hauschild P, Röttig A, Madkour MH, Al-Ansari AM, Almakishah NH, Steinbüchel A. Lipid accumulation in prokaryotic microorganisms from arid habitats. Appl Microbiol Biotechnol. 2017;101:2203–16.

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Wang JG, Bakken LR. Screening of soil bacteria for poly-β-hydroxybutyric acid production and its role in the survival of starvation. Micro Ecol. 1998;35:94–101.

    CAS  Article  Google Scholar 

  33. 33.

    Hanzlíková A, Jandera A, Kunc F. Poly-3-hydroxybutyrate production and changes of bacterial community in the soil. Folia Microbiologica. 1985;30:58–64.

    Article  Google Scholar 

  34. 34.

    Iwahara S, Miki S. Production of α-α-trehalose by a bacterium isolated from soil. Agric Biol Chem. 1988;52:867–8.

    CAS  Google Scholar 

  35. 35.

    Treseder KK, Lennon JT. Fungal traits that drive ecosystem dynamics on land. Microbiol Mol Biol Rev. 2015;79:243–62.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  36. 36.

    López MF, Männer P, Willmann A, Hampp R, Nehls U. Increased trehalose biosynthesis in Hartig net hyphae of ectomycorrhizas. N Phytol. 2007;174:389–98.

    Article  CAS  Google Scholar 

  37. 37.

    Bünemann EK, Smernik RJ, Doolette AL, Marschner P, Stonor R, Wakelin SA, et al. Forms of phosphorus in bacteria and fungi isolated from two Australian soils. Soil Biol Biochem. 2008;40:1908–15.

    Article  CAS  Google Scholar 

  38. 38.

    Genet P, Prevost A, Pargney JC. Seasonal variations of symbiotic ultrastructure and relationships of two natural ectomycorrhizae of beech (Fagus sylvatica/Lactarius blennius var. viridis and Fagus sylvatica/Lactarius subdulcis). Trees. 2000;14:465–74.

    Article  Google Scholar 

  39. 39.

    Frey B, Brunner I, Walther P, Scheidegger C, Zierold K. Element localization in ultrathin cryosections of high-pressure frozen ectomycorrhizal spruce roots. Plant Cell Environ. 1997;20:929–37.

    CAS  Article  Google Scholar 

  40. 40.

    Hanzlíkova A, Jandera A, Kunc F. Formation of poly-3-hydroxybutyrate by a soil microbial community during batch and heterocontinuous cultivation. Folia Microbiol. 1984;29:233–41.

    Article  Google Scholar 

  41. 41.

    Mason-Jones K, Banfield CC, Dippold MA. Compound‐specific 13C stable isotope probing confirms synthesis of polyhydroxybutyrate by soil bacteria. Rapid Commun Mass Spectrom. 2019;33:795–802.

    CAS  PubMed  Article  Google Scholar 

  42. 42.

    Hedlund K. Soil microbial community structure in relation to vegetation management on former agricultural land. Soil Biol Biochem. 2002;34:1299–307.

    CAS  Article  Google Scholar 

  43. 43.

    White PM, Potter TL, Strickland TC. Pressurized liquid extraction of soil microbial phospholipid and neutral lipid fatty acids. J Agric Food Chem. 2009;57:7171–7.

    CAS  PubMed  Article  Google Scholar 

  44. 44.

    Xu X, Thornton PE, Post WM. A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems: Global soil microbial biomass C, N and P. Glob Ecol Biogeogr. 2013;22:737–49.

    Article  Google Scholar 

  45. 45.

    Bååth E. The use of neutral lipid fatty acids to indicate the physiological conditions of soil fungi. Micro Ecol. 2003;45:373–83.

    Article  CAS  Google Scholar 

  46. 46.

    Soliman AH, Radwan SS. Degradation of sterols, triacylglycerol, and phospholipids by soil microorganisms. Zbl Bakt II Abt. 1981;136:420–6.

    CAS  Google Scholar 

  47. 47.

    Diakhaté S, Gueye M, Chevallier T, Diallo NH, Assigbetse K, Abadie J, et al. Soil microbial functional capacity and diversity in a millet-shrub intercropping system of semi-arid Senegal. J Arid Environ. 2016;129:71–9.

    Article  Google Scholar 

  48. 48.

    Bölscher T, Wadsö L, Börjesson G, Herrmann AM. Differences in substrate use efficiency: impacts of microbial community composition, land use management, and substrate complexity. Biol Fertil Soils. 2016;52:547–59.

    Article  CAS  Google Scholar 

  49. 49.

    Mason-Jones K, Schmücker N, Kuzyakov Y. Contrasting effects of organic and mineral nitrogen challenge the N-Mining Hypothesis for soil organic matter priming. Soil Biol Biochem. 2018;124:38–46.

    CAS  Article  Google Scholar 

  50. 50.

    Muhammadi S, Afzal M, Hameed S. Bacterial polyhydroxyalkanoates-eco-friendly next generation plastic: Production, biocompatibility, biodegradation, physical properties and applications. Green Chem Lett Rev. 2015;8:56–77.

    Article  CAS  Google Scholar 

  51. 51.

    Jose NA, Lau R, Swenson TL, Klitgord N, Garcia-Pichel F, Bowen BP, et al. Flux balance modeling to predict bacterial survival during pulsed-activity events. Biogeosciences. 2018;15:2219–29.

    CAS  Article  Google Scholar 

  52. 52.

    Medeiros PM, Fernandes MF, Dick RP, Simoneit BRT. Seasonal variations in sugar contents and microbial community in a ryegrass soil. Chemosphere. 2006;65:832–9.

    CAS  PubMed  Article  Google Scholar 

  53. 53.

    Žifčáková L, Větrovský T, Lombard V, Henrissat B, Howe A, Baldrian P. Feed in summer, rest in winter: microbial carbon utilization in forest topsoil. Microbiome 2017;5:1–12.

    Article  Google Scholar 

  54. 54.

    Ratcliff WC, Denison RF. Individual-level bet hedging in the bacterium Sinorhizobium meliloti. Curr Biol. 2010;20:1740–4.

    CAS  PubMed  Article  Google Scholar 

  55. 55.

    Schoch CL, Ciufo S, Domrachev M, Hotton CL, Kannan S, Khovanskaya R, et al. NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database. 2020;2020:baaa062.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. 56.

    Choi J, Kim S-H. A genome tree of life for the fungi kingdom. Proc Natl Acad Sci USA. 2017;114:9391–6.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. 57.

    Jun S-R, Sims GE, Wu GA, Kim S-H. Whole-proteome phylogeny of prokaryotes by feature frequency profiles: An alignment-free method with optimal feature resolution. Proc Natl Acad Sci USA. 2010;107:133–8.

    CAS  PubMed  Article  Google Scholar 

  58. 58.

    Elbahloul Y, Krehenbrink M, Reichelt R, Steinbuchel A. Physiological conditions conducive to high cyanophycin content in biomass of Acinetobacter calcoaceticus strain ADP1. Appl Environ Microbiol. 2005;71:858–66.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  59. 59.

    Lillie SH, Pringle JR. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol. 1980;143:1384–94.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. 60.

    Hall KD, Guo J. Obesity energetics: Body weight regulation and the effects of diet composition. Gastroenterology. 2017;152:1718–27.e3.

    PubMed  Article  Google Scholar 

  61. 61.

    Sala A, Woodruff DR, Meinzer FC. Carbon dynamics in trees: feast or famine? Tree Physiol. 2012;32:764–75.

    CAS  PubMed  Article  Google Scholar 

  62. 62.

    Varpe Ø, Ejsmond MJ. Trade-offs between storage and survival affect diapause timing in capital breeders. Evol Ecol. 2018;32:623–41.

    Article  Google Scholar 

  63. 63.

    Heilmeier H, Freund M, Steinlein T, Schulze E-D, Monson RK. The influence of nitrogen availability on carbon and nitrogen storage in the biennial Cirsium vulgare (Savi) Ten. I. Storage capacity in relation to resource acquisition, allocation and recycling. Plant Cell Environ. 1994;17:1125–31.

    CAS  Article  Google Scholar 

  64. 64.

    Pond CM. Ecology of storage. In: Levin SA, editor. Encyclopedia of biodiversity, 2nd ed. Amsterdam: Academic Press; 2013. p. 23–38.

  65. 65.

    McCue MD. Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A Mol Integr Physiol. 2010;156:1–18.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  66. 66.

    Donald J, Pannabecker TL. Osmoregulation in desert-adapted mammals. In: Hyndman KA, Pannabecker TL, editors. Sodium and water homeostasis. New York: Springer New York; 2015. p. 191–211.

  67. 67.

    Röttig A, Hauschild P, Madkour MH, Al-Ansari AM, Almakishah NH, Steinbüchel A. Analysis and optimization of triacylglycerol synthesis in novel oleaginous Rhodococcus and Streptomyces strains isolated from desert soil. J Biotechnol. 2016;225:48–56.

    PubMed  Article  CAS  Google Scholar 

  68. 68.

    Bailey AP, Koster G, Guillermier C, Hirst EMA, MacRae JI, Lechene CP, et al. Antioxidant role for lipid droplets in a stem cell niche of Drosophila. Cell. 2015;163:340–53.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  69. 69.

    Jenni-Eiermann S, Jenni L. Fasting in birds: general patterns and the special case of endurance flight. In: McCue MD, editor. Comparative physiology of fasting, starvation, and food limitation. 2012. Berlin: Springer; 2012. p. 171–92.

  70. 70.

    Fischer B, Dieckmann U, Taborsky B. When to store energy in a stochastic environment. Evolution. 2011;65:1221–32.

    PubMed  Article  PubMed Central  Google Scholar 

  71. 71.

    Bonnet X, Bradshaw D, Shine R. Capital versus income breeding: An ectothermic perspective. Oikos. 1998;83:333.

    Article  Google Scholar 

  72. 72.

    de Mazancourt C, Schwartz MW. Starve a competitor: evolution of luxury consumption as a competitive strategy. Theor Ecol. 2012;13:37–49.

    Article  Google Scholar 

  73. 73.

    Ejsmond MJ, Varpe Ø, Czarnoleski M, Kozłowski J. Seasonality in offspring value and trade-offs with growth explain capital breeding. Am Nat. 2015;186:E111–25.

    Article  Google Scholar 

  74. 74.

    Kourmentza C, Plácido J, Venetsaneas N, Burniol-Figols A, Varrone C, Gavala HN, et al. Recent advances and challenges towards sustainable polyhydroxyalkanoate (PHA) production. Bioengineering. 2017;4:55.

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  75. 75.

    Wilson WA, Roach PJ, Montero M, Baroja-Fernández E, Muñoz FJ, Eydallin G, et al. Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol Rev. 2010;34:952–85.

    CAS  PubMed  Article  Google Scholar 

  76. 76.

    Doi Y, Kawaguchi Y, Koyama N, Nakamura S, Hiramitsu M, Yoshida Y, et al. Synthesis and degradation of polyhydroxyalkanoates in Alcaligenes eutrophus. FEMS Microbiol Lett. 1992;103:103–8.

    CAS  Article  Google Scholar 

  77. 77.

    Alvarez AHM, Kalscheuer R, Steinbüchel A. Accumulation of storage lipids in species of Rhodococcus and Nocardia and effect of inhibitors and polyethylene glycol. Lipid. 1997;99:239–46.

    CAS  Article  Google Scholar 

  78. 78.

    Parrou JL, Enjalbert B, Plourde L, Bauche A, Gonzalez B, François J. Dynamic responses of reserve carbohydrate metabolism under carbon and nitrogen limitations in Saccharomyces cerevisiae. Yeast. 1999;15:191–203.

    CAS  PubMed  Article  Google Scholar 

  79. 79.

    Gebremariam SY, Beutel MW, Christian D, Hess TF. Research advances and challenges in the microbiology of enhanced biological phosphorus removal-A critical review. Water Environ Res. 2011;83:195–219.

    CAS  PubMed  Article  Google Scholar 

  80. 80.

    Ratledge C. Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie. 2004;86:807–15.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  81. 81.

    Matin A, Veldhuis C, Stegeman V, Veenhuis M. Selective advantage of a Spirillum sp. in a carbon-limited environment. Accumulation of poly-β-hydroxybutyric acid and its role in starvation. J Gen Microbiol. 1979;112:349–55.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  82. 82.

    Poblete-Castro I, Escapa IF, Jäger C, Puchalka J, Chi Lam C, Schomburg D, et al. The metabolic response of P. putida KT2442 producing high levels of polyhydroxyalkanoate under single- and multiple-nutrient-limited growth: Highlights from a multi-level omics approach. Micro Cell Fact. 2012;11:34.

    CAS  Article  Google Scholar 

  83. 83.

    Wilkinson JF, Munro ALS. The influence of growth limiting conditions on the synthesis of possible carbon and energy storage polymers in Bacillus megaterium. In: Powell EO, Evans CGT, Strange RE, Tempest DW, editors. Microbial physiology and continuous culture, Proceedings of the Third International Symposium. Salisbury, United Kingdom: Her Majesty’s Stationery Office; 1967. p. 173–85.

  84. 84.

    Alvarez HM, Mayer F, Fabritius D, Steinbüchel A. Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch Microbiol. 1996;165:377–86.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  85. 85.

    Orchard ED, Benitez-Nelson CR, Pellechia PJ, Lomas MW, Dyhrman ST. Polyphosphate in Trichodesmium from the low-phosphorus Sargasso Sea. Limnol Oceanogr. 2010;55:2161–9.

    CAS  Article  Google Scholar 

  86. 86.

    Li J, Mara P, Schubotz F, Sylvan JB, Burgaud G, Klein F, et al. Recycling and metabolic flexibility dictate life in the lower oceanic crust. Nature. 2020;579:250–5.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  87. 87.

    Preiss J, Romeo T. Molecular biology and regulatory aspects of glycogen biosynthesis in bacteria. Prog Nucleic Acid Res Mol Biol. 1994;47:299–329.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  88. 88.

    Mackerras AH, de Chazal NM, Smith GD. Transient accumulations of cyanophycin in Anabaena cylindrica and Synechocystis 6308. J Gen Microbiol. 1990;136:2057–65.

    CAS  Article  Google Scholar 

  89. 89.

    Parnas H, Cohen D. The optimal strategy for the metabolism of reserve materials in micro-organisms. J Theor Biol. 1976;56:19–55.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  90. 90.

    Dijkstra P, Salpas E, Fairbanks D, Miller EB, Hagerty SB, van Groenigen KJ, et al. High carbon use efficiency in soil microbial communities is related to balanced growth, not storage compound synthesis. Soil Biol Biochem. 2015;89:35–43.

    CAS  Article  Google Scholar 

  91. 91.

    Empadinhas N, da Costa MS. Osmoadaptation mechanisms in prokaryotes: distribution of compatible solutes. Int Microbiol. 2008;11:151–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  92. 92.

    Albi T, Serrano A. Inorganic polyphosphate in the microbial world. Emerging roles for a multifaceted biopolymer. World J Microbiol Biotechnol. 2016;32:27.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  93. 93.

    Sekar K, Linker SM, Nguyen J, Grünhagen A, Stocker R, Sauer U. Bacterial glycogen provides short-term benefits in changing environments. Appl Environ Microbiol. 2020;86:e00049–20.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  94. 94.

    Silljé HH, Paalman JW, ter Schure EG, Olsthoorn SQ, Verkleij AJ, Boonstra J, et al. Function of trehalose and glycogen in cell cycle progression and cell viability in Saccharomyces cerevisiae. J Bacteriol. 1999;181:396–400.

    PubMed  PubMed Central  Article  Google Scholar 

  95. 95.

    Jahid IK, Silva AJ, Benitez JA. Polyphosphate stores enhance the ability of Vibrio cholerae to overcome environmental stresses in a low-phosphate environment. Appl Environ Microbiol. 2006;72:7043–9.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  96. 96.

    Ramírez-Trujillo JA, Dunn MF, Suárez-Rodríguez R, Hernández-Lucas I. The Sinorhizobium meliloti glyoxylate cycle enzyme isocitrate lyase (AceA) is required for the utilization of poly-β-hydroxybutyrate during carbon starvation. Ann Microbiol. 2016;66:921–4.

    Article  CAS  Google Scholar 

  97. 97.

    Vagabov VM, Trilisenko LV, Kulaev IS. Dependence of inorganic polyphosphate chain length on the orthophosphate content in the culture medium of the yeast Saccharomyces cerevisiae. Biochemistry. 2000;65:6.

    Google Scholar 

  98. 98.

    Schimz K-L, Irrgang K, Overhoff B. Glycogen, a cytoplasmic reserve polysaccharide of Cellulomonas sp. (DSM20108): Its identification, carbon source-dependent accumulation, and degradation during starvation. FEMS Microbiol Lett. 1985;30:165–9.

    CAS  Article  Google Scholar 

  99. 99.

    Kalscheuer R, Stöveken T, Malkus U, Reichelt R, Golyshin PN, Sabirova JS, et al. Analysis of storage lipid accumulation in Alcanivorax borkumensis: Evidence for alternative triacylglycerol biosynthesis routes in bacteria. J Bacteriol. 2007;189:918–28.

    CAS  PubMed  Article  Google Scholar 

  100. 100.

    Busuioc M, Mackiewicz K, Buttaro BA, Piggot PJ. Role of intracellular polysaccharide in persistence of Streptococcus mutans. J Bacteriol. 2009;191:7315–22.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  101. 101.

    Ruiz JA, Lopez NI, Fernandez RO, Mendez BS. Polyhydroxyalkanoate degradation Is associated with nucleotide accumulation and enhances stress resistance and survival of Pseudomonas oleovorans in natural water microcosms. Appl Environ Microbiol. 2001;67:225–30.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  102. 102.

    Klotz A, Georg J, Bučinská L, Watanabe S, Reimann V, Januszewski W, et al. Awakening of a dormant cyanobacterium from nitrogen chlorosis reveals a genetically determined program. Curr Biol. 2016;26:2862–72.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  103. 103.

    Elbein AD. New insights on trehalose: a multifunctional molecule. Glycobiology. 2003;13:17R–27R.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  104. 104.

    Obruca S, Sedlacek P, Koller M. The underexplored role of diverse stress factors in microbial biopolymer synthesis. Bioresour Technol. 2021;326:124767.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  105. 105.

    Ayub ND, Tribelli PM, López NI. Polyhydroxyalkanoates are essential for maintenance of redox state in the Antarctic bacterium Pseudomonas sp. 14-3 during low temperature adaptation. Extremophiles. 2009;13:59–66.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  106. 106.

    Grime JP. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat. 1977;111:1169–94.

    Article  Google Scholar 

  107. 107.

    Ho A, Kerckhof F-M, Luke C, Reim A, Krause S, Boon N, et al. Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies: Functional traits of methane-oxidizing bacteria. Environ Microbiol Rep. 2013;5:335–45.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  108. 108.

    Santillan E, Seshan H, Constancias F, Wuertz S. Trait‐based life‐history strategies explain succession scenario for complex bacterial communities under varying disturbance. Environ Microbiol. 2019;21:3751–64.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  109. 109.

    Chesson P. Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst. 2000;31:343–66.

    Article  Google Scholar 

  110. 110.

    Loreau M, de Mazancourt C. Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol Lett. 2013;16:106–15.

    PubMed  Article  PubMed Central  Google Scholar 

  111. 111.

    Geyer KM, Kyker-Snowman E, Grandy AS, Frey SD. Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry. 2016;127:173–88.

    CAS  Article  Google Scholar 

  112. 112.

    Manzoni S, Porporato A. Soil carbon and nitrogen mineralization: Theory and models across scales. Soil Biol Biochem. 2009;41:1355–79.

    CAS  Article  Google Scholar 

  113. 113.

    Schultz P, Urban NR. Effects of bacterial dynamics on organic matter decomposition and nutrient release from sediments: a modeling study. Ecol Model. 2008;210:1–14.

    CAS  Article  Google Scholar 

  114. 114.

    Torres-Dorante LO, Claassen N, Steingrobe B, Olfs H-W. Polyphosphate determination in calcium acetate-lactate (CAL) extracts by an indirect colorimetric method. J Plant Nutr Soil Sci. 2004;167:701–3.

    CAS  Article  Google Scholar 

  115. 115.

    Micić V, Köster J, Kruge MA, Engelen B, Hofmann T. Bacterial wax esters in recent fluvial sediments. Org Geochem. 2015;89–90:44–55.

    Article  CAS  Google Scholar 

  116. 116.

    Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A. Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol 2014;5:1–10.

    Article  Google Scholar 

  117. 117.

    Op De Beeck M, Troein C, Siregar S, Gentile L, Abbondanza G, Peterson C, et al. Regulation of fungal decomposition at single-cell level. ISME J. 2020;14:896–905.

    PubMed  PubMed Central  Article  Google Scholar 

  118. 118.

    Liang C, Amelung W, Lehmann J, Kästner M. Quantitative assessment of microbial necromass contribution to soil organic matter. Glob Chang Biol. 2019;25:3578–90.

    PubMed  Article  PubMed Central  Google Scholar 

  119. 119.

    Ducklow H, Steinberg D, Buesseler K. Upper ocean carbon export and the biological pump. Oceanography. 2001;14:50–8.

    Article  Google Scholar 

  120. 120.

    Wieder WR, Allison SD, Davidson EA, Georgiou K, Hararuk O, He Y, et al. Explicitly representing soil microbial processes in Earth system models: Soil microbes in Earth system models. Glob Biogeochem Cycles. 2015;29:1782–800.

    CAS  Article  Google Scholar 

  121. 121.

    Schimel J, Weintraub MN. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem. 2003;35:549–63.

    CAS  Article  Google Scholar 

  122. 122.

    Ni B-J, Fang F, Rittmann BE, Yu H-Q. Modeling microbial products in activated sludge under feast-famine conditions. Environ Sci Technol. 2009;43:2489–97.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  123. 123.

    Godwin CM, Cotner JB. Stoichiometric flexibility in diverse aquatic heterotrophic bacteria is coupled to differences in cellular phosphorus quotas. Front Microbiol 2015;6:1–15.

    Article  Google Scholar 

  124. 124.

    Camenzind T, Philipp Grenz K, Lehmann J, Rillig MC. Soil fungal mycelia have unexpectedly flexible stoichiometric C:N and C:P ratios. Ecol Lett. 2021;24:208–18.

    PubMed  Article  PubMed Central  Google Scholar 

  125. 125.

    Fatichi S, Manzoni S, Or D, Paschalis A. A mechanistic model of microbially mediated soil biogeochemical processes: a reality check. Glob Biogeochem Cycles. 2019;33:620–48.

    CAS  Article  Google Scholar 

  126. 126.

    Sistla SA, Rastetter EB, Schimel JP. Responses of a tundra system to warming using SCAMPS: a stoichiometrically coupled, acclimating microbe–plant–soil model. Ecol Monogr. 2014;84:151–70.

    Article  Google Scholar 

  127. 127.

    Lashermes G, Gainvors-Claisse A, Recous S, Bertrand I. Enzymatic strategies and carbon use efficiency of a litter-decomposing fungus grown on maize leaves, stems, and roots. Front Microbiol 2016;7:1–14.

    Article  Google Scholar 

  128. 128.

    Lee ZM, Schmidt TM. Bacterial growth efficiency varies in soils under different land management practices. Soil Biol Biochem. 2014;69:282–90.

    CAS  Article  Google Scholar 

  129. 129.

    Camenzind T, Lehmann A, Ahland J, Rumpel S, Rillig MC. Trait‐based approaches reveal fungal adaptations to nutrient‐limiting conditions. Environ Microbiol. 2020;22:3548–60.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  130. 130.

    Manzoni S, Čapek P, Mooshammer M, Lindahl BD, Richter A, Šantrůčková H. Optimal metabolic regulation along resource stoichiometry gradients. Ecol Lett. 2017;20:1182–91.

    PubMed  Article  PubMed Central  Google Scholar 

  131. 131.

    Tang J, Riley WJ. Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions. Nat Clim Chang. 2015;5:5.

    CAS  Article  Google Scholar 

  132. 132.

    Lee KS, Pereira FC, Palatinszky M, Behrendt L, Alcolombri U, Berry D, et al. Optofluidic Raman-activated cell sorting for targeted genome retrieval or cultivation of microbial cells with specific functions. Nat Protoc. 2021;16:634–76.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  133. 133.

    Günther S, Trutnau M, Kleinsteuber S, Hause G, Bley T, Röske I, et al. Dynamics of polyphosphate-accumulating bacteria in wastewater treatment plant microbial communities detected via DAPI (4′,6′-diamidino-2-phenylindole) and tetracycline labeling. Appl Environ Microbiol. 2009;75:2111–21.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  134. 134.

    Singleton CM, Petriglieri F, Kristensen JM, Kirkegaard RH, Michaelsen TY, Andersen MH, et al. Connecting structure to function with the recovery of over 1000 high-quality metagenome-assembled genomes from activated sludge using long-read sequencing. Nat Commun. 2021;12:2009.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  135. 135.

    Link H, Fuhrer T, Gerosa L, Zamboni N, Sauer U. Real-time metabolome profiling of the metabolic switch between starvation and growth. Nat Methods. 2015;12:1091–7.

    CAS  PubMed  Article  Google Scholar 

  136. 136.

    Warren CR. Altitudinal transects reveal large differences in intact lipid composition among soils. Soil Res. 2021;59:644–59.

    CAS  Article  Google Scholar 

  137. 137.

    Wilkinson J. The problem of energy-storage compounds in bacteria. Exp Cell Res. 1959;7:111–30.

    Article  Google Scholar 

  138. 138.

    Nickels JS, King JD, White DC. Poly-β-hydroxybutyrate accumulation as a measure of unbalanced growth of the estuarine detrital microbiota. Appl Environ Microbiol. 1979;37:459–65.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  139. 139.

    Murphy DJ. The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma. 2012;249:541–85.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  140. 140.

    Alvarez HM. Triacylglycerol and wax ester-accumulating machinery in prokaryotes. Biochimie. 2016;120:28–39.

    CAS  PubMed  Article  Google Scholar 

  141. 141.

    Koller M, Maršálek L, de Sousa Dias MM, Braunegg G. Producing microbial polyhydroxyalkanoate (PHA) biopolyesters in a sustainable manner. N Biotechnol. 2017;37:24–38.

    CAS  PubMed  Article  Google Scholar 

  142. 142.

    Obruca S, Sedlacek P, Slaninova E, Fritz I, Daffert C, Meixner K, et al. Novel unexpected functions of PHA granules. Appl Microbiol Biotechnol. 2020;104:4795–810.

    CAS  PubMed  Article  Google Scholar 

  143. 143.

    Roach PJ, Depaoli-Roach AA, Hurley TD, Tagliabracci VS. Glycogen and its metabolism: some new developments and old themes. Biochem J. 2012;441:763–87.

    CAS  PubMed  Article  Google Scholar 

  144. 144.

    Wang L, Wang M, Wise MJ, Liu Q, Yang T, Zhu Z, et al. Recent progress in the structure of glycogen serving as a durable energy reserve in bacteria. World J Microbiol Biotechnol. 2020;36:14.

    PubMed  Article  Google Scholar 

  145. 145.

    Ruhal R, Kataria R, Choudhury B. Trends in bacterial trehalose metabolism and significant nodes of metabolic pathway in the direction of trehalose accumulation: Trehalose metabolism in bacteria. Micro Biotechnol. 2013;6:493–502.

    Article  CAS  Google Scholar 

  146. 146.

    Kalscheuer R. Genetics of wax ester and triacylglycerol biosynthesis in bacteria. In: Timmis KN, editor. Handbook of hydrocarbon and lipid microbiology. Berlin, Heidelberg: Springer Berlin Heidelberg; 2010. p. 527–35.

  147. 147.

    Rao NN, Gómez-García MR, Kornberg A. Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem. 2009;78:605–47.

    CAS  PubMed  Article  Google Scholar 

  148. 148.

    Denoncourt A, Downey M. Model systems for studying polyphosphate biology: a focus on microorganisms. Curr Genet. 2021;67:331–46.

    CAS  PubMed  Article  Google Scholar 

  149. 149.

    Füser G, Steinbüchel A. Analysis of genome sequences for genes of cyanophycin metabolism: Identifying putative cyanophycin metabolizing prokaryotes. Macromol Biosci. 2007;7:278–96.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  150. 150.

    Watzer B, Forchhammer K. Cyanophycin: a nitrogen-rich reserve polymer. In: Tiwari A, editor. Cyanobacteria. London: InTech; 2018.

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Acknowledgements

Many thanks to Aliia Gilmullina, whose hospitality supported the initiation of this work, and to Emilia Hannula and Andreas Schweiger for their comments on early drafts. We are grateful for the critical input of three anonymous reviewers. KMJ acknowledges the Dutch Research Council (NWO) for funding of the Vital Soils project under the “Programma NWO Groen 2015” (ALWGR.2015.5) and the NWO Veni project VI.Veni.202.086. SLR acknowledges support from the National Science Foundation Graduate Research Fellowship (00039202) and a Graduate Research Opportunities Worldwide (GROW) fellowship supported by the NSF and NWO (040.15.054/6097). SM received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no. 101001608).

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Correspondence to Kyle Mason-Jones.

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The authors declare no competing interests: KMJ conceived of the work, SM undertook modeling, all authors contributed to data collection and conceptual development, KMJ, SLR, and SM drafted the paper, and all authors were involved in paper revision and have approved the final version.

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Mason-Jones, K., Robinson, S.L., Veen, G.F.(. et al. Microbial storage and its implications for soil ecology. ISME J (2021). https://doi.org/10.1038/s41396-021-01110-w

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