Pyrolyzed Substrates Induce Aromatic Compound Metabolism in the Post-fire Fungus, Pyronema domesticum

Wildfires represent a fundamental and profound disturbance in many ecosystems, and their frequency and severity are increasing in many regions of the world. Fire affects soil by removing carbon in the form of CO2 and transforming remaining surface carbon into pyrolyzed organic matter (PyOM). Fires also generate substantial necromass at depths where the heat kills soil organisms but does not catalyze the formation of PyOM. Pyronema species strongly dominate soil fungal communities within weeks to months after fire. However, the carbon pool (i.e., necromass or PyOM) that fuels their rise in abundance is unknown. We used a Pyronema domesticum isolate from the catastrophic 2013 Rim Fire (CA, United States) to ask whether P. domesticum is capable of metabolizing PyOM. Pyronema domesticum grew readily on agar media where the sole carbon source was PyOM (specifically, pine wood PyOM produced at 750°C). Using RNAseq, we investigated the response of P. domesticum to PyOM and observed a comprehensive induction of genes involved in the metabolism and mineralization of aromatic compounds, typical of those found in PyOM. Lastly, we used 13C-labeled 750°C PyOM to demonstrate that P. domesticum is capable of mineralizing PyOM to CO2. Collectively, our results indicate a robust potential for P. domesticum to liberate carbon from PyOM in post-fire ecosystems and return it to the bioavailable carbon pool.

Pyrolyzed substrates induce aromatic compound metabolism in the post-fire fungus,Pyronema domesticum

ABSTRACTWildfires represent a fundamental and profound disturbance in many ecosystems, and their frequency and severity are increasing in many regions of the world. Fire affects soil by removing carbon in the form of CO2and transforming remaining surface carbon into pyrolyzed organic material (PyOM). Fires also generate substantial necromass at depths where the heat kills soil organisms but does not catalyze the formation of PyOM.Pyronemaspecies strongly dominate soil fungal communities within weeks to months after fire. However, the carbon pool (i.e. necromass or PyOM) that fuels their rise in abundance is unknown. We used aPyronema domesticumisolate from the catastrophic 2013 Rim Fire (CA, USA) to ask ifP. domesticumis capable of metabolizing PyOM.P. domesticumgrew readily on agar media where the sole carbon source was PyOM (specifically, pine wood PyOM produced at 750 °C). Using RNAseq, we investigated the response ofP. domesticumto PyOM and observed a comprehensive induction of genes involved in the metabolism and mineralization of aromatic compounds, typical of those found in PyOM. Lastly, we used13C-labeled 750 °C PyOM to demonstrate thatP. domesticumis capable of mineralizing PyOM to CO2. Collectively, our results indicate a robust potential forP. domesticumto liberate carbon from PyOM in post-fire ecosystems and return it to the bioavailable carbon pool.IMPORTANCEFires are increasing in frequency and severity in many regions across the world. Thus, it’s critically important to understand how our ecosystems respond to inform restoration and recovery efforts. Fire transforms the soil, removing many nutrients while leaving behind both nutritious necromass and complex pyrolyzed organic matter, which is often recalcitrant. Filamentous fungi of the genusPyronemastrongly dominate soil fungal communities soon after fire. While Pyronema are key pioneer species in post-fire environments, the nutrient source that fuels their rise in abundance is unknown. In this manuscript, we used a P. domesticum isolate from the catastrophic 2013 Rim Fire (CA, USA) to demonstrate thatP. domesticummetabolizes pyrolyzed organic material, effectively liberating this complex pyrolyzed carbon and returning it to the bioavailable carbon pool. The success of Pyronema in post-fire ecosystems has the potential to kick-start growth of other organisms and influence the entire trajectory of post-fire recovery.

Cyanobacterial taxonomy, metabolism, and cyanophage association in dark and anoxic sediment

BackgroundCyanobacteria are photosynthetic ancient bacteria ubiquitous in terrestrial and aquatic environments. Even though they carry a photosynthesis apparatus they are known to survive in dark environments. Cyanophages are viruses that infect and lyse cyanobacterial cells, adding bioavailable carbon and nutrients into the environment. Here we present the first study that investigate the metabolic spectrum of cyanobacteria in dark and anoxic environments, as well as their associated cyanophages. We sampled surface sediments during April 2018 located along a water depth gradient of 60–210 m—representing oxic, hypoxic and anoxic conditions—in the largest dead zone in the world (Baltic Sea). We combined metagenomic and RNA-seq to investigate cyanobacterial taxonomy, activity and their associated cyanophages.ResultsCyanobacteria were detected at all four stations (n = 3 per station) along the sampled gradient, including the anoxic sediment. Top genera in the anoxic sediment included Anabaena (19% RNA data), Synechococcus (16%), and Cyanobium (5%). The mRNA data showed that cyanobacteria were surviving through i) anaerobic carbon metabolism indicated by glycolysis plus fatty acid biosynthesis, and ii) nitrogen (N2) fixation (likely by heterocystous Anabaena). Interestingly, in the mRNA data cyanobacteria were also transcribing photosynthesis, phytochromes, and gas vesicle genes. Cyanophages were detected at all stations, and compared to the oxic sediment had a different beta diversity in the hypoxic-anoxic sediment. Moreover, our results show that these cyanophages can infect cyanobacteria affecting the photosystem and phosphate regulation.ConclusionsCyanobacteria were found to transcribe genes for photosynthesis, phytochromes, and gas vesicles and this suggests that cyanobacteria try to ascend to the surface waters. The difference in cyanophage beta diversity between oxic and hypoxic-anoxic sediment suggests that anaerobic cyanobacteria select for specific cyanophages. Cyanobacteria are known to fuel oxygen depleted benthic ecosystems with phosphorous (so called internal loading), and our study suggests that cyanophage-controlled lysis of cyanobacteria likely provides a source of nitrogen. Our results suggest that cyanobacteria might also provide nutrients via N2 fixation and viral lysis in dark and anoxic environments.

Cyanobacterial taxonomy, metabolism, and cyanophage association in dark and anoxic sediment

Background Cyanobacteria are photosynthetic ancient bacteria ubiquitous in terrestrial and aquatic environments. Even though they carry a photosynthesis apparatus they are known to survive in dark environments. Cyanophages are viruses that infect and lyse cyanobacterial cells, adding bioavailable carbon and nutrients into the environment. Here we present the first study that investigate the metabolic spectrum of cyanobacteria in dark and anoxic environments, as well as their associated cyanophages. We sampled surface sediments during April 2018 located along a water depth gradient of 60–210 m—representing oxic, hypoxic and anoxic conditions—in the largest dead zone in the world. We combined metagenomic and total RNA sequencing to investigate cyanobacterial taxonomy, activity and their associated cyanophages. Results Cyanobacteria were detected at all four stations (n = 3 per station) along the sampled gradient, including the anoxic sediment. Top active genera in the anoxic sediment included Anabaena (19% RNA data), Synechococcus (16%), and Cyanobium (5%). The mRNA data showed that cyanobacteria were surviving through i) anaerobic carbon metabolism indicated by glycolysis plus fatty acid biosynthesis, and ii) nitrogen (N2) fixation (likely by heterocystous Anabaena). Interestingly, cyanobacteria were also actively transcribing photosynthesis, phytochromes, and gas vesicle genes. Cyanophages were also detected at all stations, and compared to the oxic sediment had a different beta diversity in the hypoxic-anoxic sediment. Moreover, our results show that these cyanophages infect cyanobacteria affecting the photosystem and phosphate regulation of cyanobacteria. Conclusions Cyanobacteria were found to transcribe genes for photosynthesis, phytochromes, and gas vesicles and this suggests that cyanobacteria are trying to ascend to the surface waters. The difference in cyanophage beta diversity between oxic and hypoxic-anoxic sediment suggests that anaerobic cyanobacteria select for specific cyanophages. Cyanobacteria are known to fuel oxygen depleted benthic ecosystems with phosphorous (so called internal loading), and our study suggests that cyanophage-controlled lysis of cyanobacteria likely provides a source of nitrogen. Photosynthetic cyanobacteria are commonly thought to have been essential in the great oxygenation event on Earth ca. 2.4 billion years ago. Our results suggest that active cyanobacteria might also provide nutrients (via N2 fixation and viral lysis) in dark and anoxic environments.

Greenland Ice Sheet exports labile organic carbon to the Arctic oceans

Runoff from small glacier systems contains dissolved organic carbon (DOC) rich in protein-like, low molecular weight (LMW) compounds, designating glaciers as an important source of bioavailable carbon for downstream heterotrophic activity. Fluxes of DOC and particulate organic carbon (POC) exported from large Greenland catchments, however, remain unquantified, despite the Greenland Ice Sheet (GrIS) being the largest source of global glacial runoff (ca. 400 km3 yr−1). We report high and episodic fluxes of POC and DOC from a large (>600 km2) GrIS catchment during contrasting melt seasons. POC dominates organic carbon (OC) export (70–89% on average), is sourced from the ice sheet bed, and contains a significant bioreactive component (9% carbohydrates). A major source of the "bioavailable" (free carbohydrate) LMW–DOC fraction is microbial activity on the ice sheet surface, with some further addition of LMW–DOC to meltwaters by biogeochemical processes at the ice sheet bed. The bioavailability of the exported DOC (26–53%) to downstream marine microorganisms is similar to that reported from other glacial watersheds. Annual fluxes of DOC and free carbohydrates during two melt seasons were similar, despite the approximately two-fold difference in runoff fluxes, suggesting production-limited DOC sources. POC fluxes were also insensitive to an increase in seasonal runoff volumes, indicating a supply limitation in suspended sediment in runoff. Scaled to the GrIS, the combined DOC (0.13–0.17 Tg C yr−1 (±13%)) and POC fluxes (mean = 0.36–1.52 Tg C yr−1 (±14%)) are of a similar order of magnitude to a large Arctic river system, and hence may represent an important OC source to the near-coastal North Atlantic, Greenland and Labrador seas.