Microbial nitrogen removal versus recycling in the redox transition zone of a meromictic lake and its coupling to sulfur

Abstract

Organotrophic denitrification is an important nitrogen (N) removal process in lakes, but alternative N reduction processes such as lithotrophic sulfur (S)-oxidizing denitrification may be greatly underappreciated. We studied the redox transition zone (RTZ) in the meromictic water column of the North Basin of Lake Lugano (Switzerland) to characterize N transformation pathways coupled to the S and carbon (C) cycles. Incubations with 15N-labeled and unlabeled nitrate showed low denitrification rates and a general limitation of organic electron donors. The most accessible fractions of exported primary production biomass may have been largely consumed in the oxic water column during sedimentation, and did not reach the RTZ at [~]100 m. Conversely, sulfide (H2S) and methane (CH4), major end products of anaerobic degradation of the more recalcitrant organic matter fractions in the sediment, represent a continuous source of energy to the RTZ, fostering the establishment of a community of S- and CH4-dependent nitrate reducers, dominated by Sulfuritalea and Candidatus Methylomirabilis over several years of observation. Anoxic incubation experiments with H2S amendments revealed a strong stimulation of dissimilatory nitrate reduction to ammonium (DNRA), but not denitrification. High relative abundances of the archaeal ammonia oxidizer Candidatus Nitrosopumilus and bacterial nitrifiers indicate intense nitrate regeneration by nitrification in the upper RTZ. The potential interaction between nitrification and S-driven DNRA is unclear. However, their importance in close proximity suggests that, at least under conditions of carbon limitation, N recycling between the nitrate and ammonium pools, predominates over N removal via complete denitrification in the Lake Lugano North Basin.