Spatiotemporal distribution and microbial assimilation of polyamines in a mesotrophic lake

Abstract

We examined seasonal and spatial variations of dissolved free polyamines (DFPA) in the large mesotrophic prealpine Lake Zurich (Switzerland). An ion‐pairing liquid chromatography method with mass spectrometric detection was optimized for the quantification of DFPA without prior concentration or derivatization. Total DFPA concentrations varied between 0.4 nM and 11 nM in winter and spring of 2015, respectively. Polyamine concentrations were highest in the epilimnion during the phytoplankton growth phase, and reflected occurrence patterns of diatoms. Putrescine consistently dominated the DFPA pool throughout the season whereas norspermidine was detected only once in spring. Incubations with 13C‐labeled putrescine revealed concentration‐dependent uptake rates (3.2–5 nM h−1) and short turnover times (2.4–4.4 h). In contrast, incorporation rates into biomass measured with 14C‐labeled putrescine were substantially lower (0.9 nM h−1), indicating that this compound was predominantly respired. Uptake kinetics moreover suggested that putrescine in situ uptake rates were limited by low ambient concentrations. Competition assays revealed that putrescine uptake could only be inhibited by excess concentrations of another polyamine (spermidine), but not by amino acids. Bacteria affiliated with Limnohabitans and the acI lineage of Actinobacteria were identified as the taxa with the highest fraction (25–32%) of putrescine‐incorporating cells. This compound was also utilized by Alphaproteobacteria, Cyclobacteriaceae, diatoms, and cyanobacteria. Overall, our data point to fast turnover of putrescine by different microorganisms, implying the importance of this substrate as an attractive energy source.

Microbial oxidation of nitrogen supplied as selected organic nitrogen compounds in the South Atlantic Bight

“…Therefore, high‐oxidation rates of N supplied as DON at inshore stations reflect the high‐biogeochemical activity generally found in these waters regardless of whether the rapid N‐oxidation is due to direct activity of abundant Thaumarchaeota or to the combined activity of heterotrophic remineralization and NH 4 + oxidation. However, irrespective of the underlying mechanism, our data suggest that oxidation of polyamine‐N may contribute to a significant fraction of total nitrification in waters where polyamine fluxes are high, such as decaying phytoplankton blooms or productive coastal waters (Lee and Jørgensen ; Nishibori et al ; Lu et al ; Liu et al ; Krempaska et al ) and may therefore contribute significantly to DON oxidation in the coastal ocean.…”

“…They are ubiquitous in eukaryotic and prokaryotic cells where they participate in integral cellular processes such as nucleic acid synthesis and stabilization, biosilica precipitation in diatoms, and protein synthesis (Kröger et al ; Iacomino et al ). Polyamines are present at millimolar concentrations in phytoplankton and bacterial cells (e.g., Tabor and Tabor ; Nishibori and Nishijima ; Liu et al ), but their standing stocks in aquatic environments are in the low nanomolar or picomolar range, suggesting rapid biogeochemical cycling (Nishibori et al , b ; Lu et al ; Liu et al ; Krempaska et al ). Recent work has expanded our understanding of polyamine assimilation and the cycling of polyamine carbon (C) in aquatic systems (e.g., Poretsky et al ; Mou et al , ; Liu et al ; Lu et al ; Krempaska et al ), but little is known about the fate of polyamine‐N.…”

Metatranscriptomic identification of polyamine‐transforming bacterioplankton in the Gulf of Mexico

“…PAs are ubiquitous in cells of organisms of all three domains of life (Archaea, Bacteria, and Eukarya; Tabor and Tabor, ; Lee and Jørgensen, ) and are widely distributed in marine (Nishibori et al . , ) and freshwater environments (Krempaska et al ., ; Madhuri et al ., ). They have been found satisfying the growth of marine (Höfle, ; Lee and Jørgensen, ; Lu et al ., ) and freshwater (Krempaska et al .…”

“…They have been found satisfying the growth of marine (Höfle, ; Lee and Jørgensen, ; Lu et al ., ) and freshwater (Krempaska et al . ; Madhuri et al ., ) bacterioplankton as carbon, nitrogen, and/or energy sources. Concentrations of PAs in seawater range from a few nM to about 200 nM (Lee and Jørgensen, ; Lu et al ., ).…”

Homeostatic regulation of dissolved labile organic substrates by consumption and release processes in a freshwater lake

“…This conclusion appears to contrast with the concept of taxon‐specific “target substrates”, as, for example, deduced from microautoradiography analyses (Buck et al ; Eckert et al ) examining individual cells or populations. However, the uptake of many labile substrates appears to be widespread across different taxa of pelagic bacteria (e.g., Riemann and Azam ; Krempaska et al ). Thus, the coexistence of numerous populations of more or less specialized bacteria with overlapping substrate spectra (Salcher et al ) would result in exactly the type of apparently “generalist” substrate consumption pattern at the community level as observed in our experiment.…”