Selective Pressure of Temperature on Competition and Cross-Feeding within Denitrifying and Fermentative Microbial Communities

Abstract

In coastal marine sediments, denitrification and fermentation are important processes in the anaerobic decomposition of organic matter. Microbial communities performing these two processes were enriched from tidal marine sediments in replicated, long term chemostat incubations at 10 and 25°C. Whereas denitrification rates at 25°C were more or less stable over time, at 10°C denitrification activity was unstable and could only be sustained either by repeatedly increasing the amount of carbon substrates provided or by repeatedly decreasing the dilution rate. Metagenomic and transcriptomic sequencing was performed at different time points and provisional whole genome sequences (WGS) and gene activities of abundant populations were compared across incubations. These analyses suggested that a temperature of 10°C selected for populations related to Vibrionales/Photobacterium that contributed to both fermentation (via pyruvate/formate lyase) and nitrous oxide reduction. At 25°C, denitrifying populations affiliated with Rhodobacteraceae were more abundant. The latter performed complete denitrification, and may have used carbon substrates produced by fermentative populations (cross-feeding). Overall, our results suggest that a mixture of competition—for substrates between fermentative and denitrifying populations, and for electrons between both pathways active within a single population –, and cross feeding—between fermentative and denitrifying populations—controlled the overall rate of denitrification. Temperature was shown to have a strong selective effect, not only on the populations performing either process, but also on the nature of their ecological interactions. Future research will show whether these results can be extrapolated to the natural environment.

Effect of Temperature on Oxygen Profiles and Denitrification Rates in Freshwater Sediments

“…The weaker temperature effect indicates that other drivers besides temperature are of importance in controlling denitrification rates. This corroborates the findings of Brin et al (2015) and Hanke et al (2015), who both showed that availability of organic carbon is another key determinant controlling denitrification and its response to warming. In our experiment nitrate concentrations were set at 1 mg N l −1 at the start of the denitrification measurements.…”

“…For example, in enrichment bioreactors which contained communities derived from marine sediments, warming resulted in changed denitrification activity and community shifts, from a community where fermenters and organisms capable of nitrous oxide reduction were the dominant organic matter degraders at 10 degrees, to a system dominated by denitrifying populations, performing the complete denitrification pathway, at 25 degrees (Hanke et al 2015). Thus, Hanke et al (2015) show that temperature effects on denitrification rates are not only controlled by oxygen, but also by organic carbon, driven by changed interactions between fermenting and denitrifying bacteria. Effects of warming may also depend on the successional stage of microbial communities, as was observed in freshwater biofilms , in which young biofilms showed increased denitrification rates with warming, whereas denitrification rates in older biofilms decreased.…”

“…In these ecosystems, denitrification -the microbial conversion of nitrate (NO 3 − ) or nitrite (NO 2 − ) via nitric oxide (NO) and nitrous oxide (N 2 O) to dinitrogen gas (N 2 ) -can remove more than half of the nitrogen i nfluxes, ma kin g it a crucial process counteracting eutrophication (de Klein and Koelmans 2011;Veraart 2012). However, because denitrification on average produces 1-5% of its gaseous end product in the form of N 2 O, enhanced denitrification rates can also pose a strong, yet understudied, positive feedback on global warming Hanke et al 2015). Denitrification is a major sink for inorganic nitrogen in freshwater ecosystems, however, several studies in the past two decades have demonstrated that anaerobic ammonium oxidation (anammox) can also significantly contribute to N removal (Risgaard-Petersen et al 2003;Seitzinger et al 2006).…”

Seasonal variation in the biocontrol efficiency of bacterial wilt is driven by temperature‐mediated changes in bacterial competitive interactions

“…; Hanke et al . ), the survival of the biocontrol agent (Hu et al . ) and the interactive effects within microbiomes (Thomas & Sekhar ).…”

Hidden in plain sight: The importance of cryptic interactions in marine plankton

“…In a meromictic lake, microbial iron oxidizers and reducers were found concomitant with high rates of iron oxidation but no detectable iron oxides, suggesting rapid reduction (Berg et al ). Evidence of carbon substrate sharing between fermenters and denitrifiers was shown in a mixed culture from marine sediments (Hanke et al ). Also in marine sediments, recycling of nitrite contributed to higher‐than‐expected rates of sulfide oxidation (Rios‐Del Toro and Cervantes ).…”