Isotope pool dilution reveals rapid turnover of small quaternary ammonium compounds

Abstract

Studies of how nitrogen (N) becomes available have tended to focus on depolymerisation of proteins and subsequent uptake of amino acids, yet amino acids and their polymers are not the only organic N compounds in soil. For example, concentrations of small quaternary ammonium compounds in the extracellular fraction of soil are often comparable to those of amino acids. We know that there is rapid turnover of amino acids in the extracellular fraction of soil, but there are no comparable data for small quaternary ammonium compounds. The most common function of small quaternary ammonium compounds is as intracellular osmolytes, which leads to the hypothesis that at constant osmolarity microbes would neither efflux nor take up osmolytes and thus there would be negligible flux of quaternary ammonium compounds through the extracellular fraction of soil. To test this hypothesis isotope pool dilution was used to compare gross fluxes of three quaternary ammonium compounds (betaine, carnitine and hercynine) with gross fluxes of two amino acids (glycine, alanine) in three different soils. Contrary to our hypothesis extracellular pools of betaine, carnitine and hercynine were highly dynamic and turned over rapidly. For example, in one soil the mean residence times of all quaternary ammonium compounds varied between 6 and 14 min such that pools would have turned over 100 to 240 times per day. Mean residence times of quaternary ammonium compounds were notably longer in soils from two other sites, yet remained shorter than 60 min such that pools would turnover many tens of time per day. Gross fluxes of betaine, carnitine and hercynine through the extracellular pool were 3–75 times slower than for the amino acid alanine, and thus fluxes of small quaternary ammonium compounds likely account for only a small fraction of the bio-available N that is produced and consumed. The combination of small concentrations and short residence times suggest there is intense microbial competition and active uptake of betaine, carnitine and hercynine from the extracellular fraction of soil.