Investigating the effect of temperature on growth and microbial biomass accumulation during winter

It is well documented that microbial biomass increases during winter in cold mountain or tundra ecosystems, but the cause and mechanism of such accumulation is unclear. Results from a grassland in Iceland demonstrated that the microbial biomass carbon (MBC, measured by the fumigation-extraction method) increased in winter, while microbial DNA content remained constant. We thus hypothesized that this accumulation of microbial biomass during the cold season is driven by the decrease in temperature, that increases the carbon storage of individual cells, but not by an increase in microbial cell numbers.

To test this hypothesis, we conducted a laboratory incubation experiment with soils from a grassland in Iceland sampled before the onset of winter in early October (around 9 °C). We then exposed the soils to decreasing temperatures (0.5 °C, 3 °C, 6 °C and 9 °C) over five months. We analyzed microbial biomass carbon (MBC) and quantified the DNA content. Over the course of five months, we found higher MBC values at cool temperatures compared to warm conditions. As expected, cooling did not affect the DNA content, leading to a significantly higher MBC to DNA ratio when soils were incubated at 0.5 °C compared to 9 °C. This indicates that numbers of microbial cells did not change across temperatures, but that microbes at lower temperatures stored more carbon. We also found similar patterns in soils collected at different time points in the field. Furthermore, we estimated microbial DNA production, i.e., growth rates, by measuring the incorporation of ¹⁸O from labelled water into DNA. We observed lower microbial growth rates under field conditions in winter, indicating that increasing biomass carbon was not due to increased growth and that growth and turnover was balanced at all temperatures. Instead, we suggest that carbon uptake (which was decreased at lower temperatures) was less affected by cold temperatures than growth, so that microbial carbon could accumulate. We also verified this pattern in growth and carbon uptake rates with decreasing temperatures in the laboratory incubation experiment.

Decreasing growth (cell division) and turnover rates with decreasing temperatures, at a lower but sustained carbon uptake rate, suggest that the cell size of soil microorganisms may increase when exposed to cooling. We will show and discuss first results from measurements with a suspended microchannel resonator (SMR), that, together with microscopic imaging allows to assess the mass (size) of individual cells of microorganisms at different temperatures.