Temperature dependence of metabolic rates for microbial growth, maintenance, and survival

Abstract

Our work was motivated by discoveries of prokaryotic communities that survive with little nutrient in ice and permafrost, with implications for past or present microbial life in Martian permafrost and Europan ice. We compared the temperature dependence of metabolic rates of microbial communities in permafrost, ice, snow, clouds, oceans, lakes, marine and freshwater sediments, and subsurface aquifer sediments. Metabolic rates per cell fall into three groupings: (i) a rate, μ g(T), for growth, measured in the laboratory at in situ temperatures with minimal disturbance of the medium; (ii) a rate, μ m(T), sufficient for maintenance of functions but for a nutrient level too low for growth; and (iii) a rate, μ s(T), for survival of communities imprisoned in deep glacial ice, subsurface sediment, or ocean sediment, in which they can repair macromolecular damage but are probably largely dormant. The three groups have metabolic rates consistent with a single activation energy of ≈110 kJ and that scale as μ g(T):μ m(T):μ s(T) ≈ 10 6:10 3:1. There is no evidence of a minimum temperature for metabolism. The rate at -40°C in ice corresponds to ≈10 turnovers of cellular carbon per billion years. Microbes in ice and permafrost have metabolic rates similar to those in water, soil, and sediment at the same temperature. This finding supports the view that, far below the freezing point, liquid water inside ice and permafrost is available for metabolism. The rate μ s(T) for repairing molecular damage by means of DNA-repair enzymes and protein-repair enzymes such as methyltransferase is found to be comparable to the rate of spontaneous molecular damage.