Microbial life under extreme energy limitation

Key Points

  • Most of what we understand about microbial energy metabolism derives from the study of cultured organisms that poorly represent those in low-energy settings, both in phylogeny and physiological state.

  • A large fraction of bacteria and archaea on Earth live in the deep subsurface, where fluxes of energy can be orders of magnitude lower than in our surface world.

  • Organisms in low-energy environments catabolize and turn over biomass 105–106-fold more slowly than those operating near Vmax in culture, and subsist with energy fluxes 104-fold lower than culture-based estimates of maintenance energy.

  • The calculated mean turnover times of cell biomass in the sub-seafloor deep biosphere is a few hundred to a few thousand years: that is, 100–1,000 times slower than in surface sediments.

  • Mean cell-specific rates of metabolism in subsurface microbial communities scatter around 10−4 to 10−3 fmol cell−1 d−1.

  • This range of metabolic rates probably reflects the 'basal power requirement': that is, the energy turnover rate per cell or per unit biomass associated with the minimal complement of functions required to sustain a metabolically active state of the cell.

Abstract

A great number of the bacteria and archaea on Earth are found in subsurface environments in a physiological state that is poorly represented or explained by laboratory cultures. Microbial cells in these very stable and oligotrophic settings catabolize 104- to 106-fold more slowly than model organisms in nutrient-rich cultures, turn over biomass on timescales of centuries to millennia rather than hours to days, and subsist with energy fluxes that are 1,000-fold lower than the typical culture-based estimates of maintenance requirements. To reconcile this disparate state of being with our knowledge of microbial physiology will require a revised understanding of microbial energy requirements, including identifying the factors that comprise true basal maintenance and the adaptations that might serve to minimize these factors.

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Figure 1: Timescales, population sizes and biomass turnover times associated with culture-based and natural environment studies.
Figure 2: Principle of D:L amino acid racemization model for the calculation of microbial turnover in subsurface sediments.
Figure 3: Mean cell-specific rates of sulphate reduction in marine sediments from three different geographical regions.
Figure 4: Mean cell-specific carbon turnover in marine sulphate-reducing microorganisms.

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Acknowledgements

T.M.H. is supported by the NASA Astrobiology Institute and Exobiology Program, and B.B.J is supported by the Danish National Research Foundation, the German Max Planck Society and the European Research Council. The authors thank M. A. Lever, H. Røy, A. Schippers and an anonymous reviewer for helpful comments on the manuscript.

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Correspondence to Tori M. Hoehler.

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Second International Workshop on Microbial Life under Extreme Energy Limitation

Glossary

Deep biosphere

The set of ecosystems and their organisms living beneath the upper few metres of the solid earth surface.

Extended stationary phase

A phase of the batch culture life cycle characterized by the persistence of a small fraction of cells for months to years beyond the death of the majority of the culture, without new addition of substrate.

Y ATP

Cellular growth yield normalized to ATP consumption.

Basal power requirement

Energy turnover rate per cell or per unit biomass associated with the minimal complement of functions required to sustain a metabolically active state of the cell.

Mean cell-specific metabolic rates

Estimate of average cellular metabolic rate among a whole community of cells obtained by measurement of bulk metabolic process rates and cell numbers.

Primary productivity

The formation of living organic biomass from carbon dioxide through the process of photosynthesis or chemosynthesis.

Reaction-transport modelling

Calculation of metabolic process rates based on steady-state concentration-depth profiles and calculated metabolite fluxes.

Power law

A mathematical relationship between two quantities describing how one quantity, c, varies as a power of another quantity, z: for example, c = A × z−b, in which c could be cell density, z sediment depth (z> >0), and A and b constants.

Bioturbated sediment

The uppermost part of the seabed that is physically reworked by animals.

Gyre

A large system of rotating ocean currents, such as those involved with large wind movements at mid-latitudes on the northern and southern Pacific and Atlantic Ocean.

Amino acid racemization

Conversion of one stereoisomer of an amino acid to another stereoisomer that is a mirror image of the former.

Depurination

An alteration of DNA in which the purine base (adenine or guanine) is lost from the deoxyribose sugar by hydrolysis of the β-N-glycosidic link between them.

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Hoehler, T., Jørgensen, B. Microbial life under extreme energy limitation. Nat Rev Microbiol 11, 83–94 (2013). https://doi.org/10.1038/nrmicro2939

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