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Impact of Oxygen and Pesticides on Microbial Cellulose Degradation in Aerated Agricultural Soils: A Microscaled Analysis of Processes and Prokaryotic Populations
(2011)
- The polysaccharide cellulose is a major component of organic matter in terrestrial ecosystems and its mineralization drives carbon fluxes in soil. The degradation of plant-derived saccharides (e.g., cellulose, cellobiose, and glucose) is catalysed by a huge diversity of aerobic and anaerobic microorganisms (including Bacteria, fungi, and protists), but there is limited information about their phylogenetic identities and their in situ relevance in soil. Soil is a heterogeneous habitat in which oxic and anoxic microzones co-occur, and in which the distribution of O2 can change rapidly. Hence, the availability of O2 is an important factor that determines the activity of the saccharide-degrading community in microzones of aerated soil. Likewise, the accumulation of potential toxic pesticides in agricultural ecosystems might influence microbial activity. It is not resolved how active cellulolytic and saccharolytic taxa respond to rapid changes in the availabilities of O2. Furthermore, it is unclear if pesticides impact on the degradation of cellulose and cellulose-linked processes, and influence the activity of active saccharide-utilizing microorganisms. Hence, this study first identified cellulolytic and saccharolytic aerobic and anaerobic Prokaryotes that catalyzed the degradation of supplemented [13C]-labeled saccharides by 16S rRNA stable isotope probing. The metabolic response of major bacterial taxa to pesticides and fluctuating availabilities of O2 was further analyzed with taxon-specific qPCR assays. Eukaryotes that contributed to soil carbon flux were identified by targeting 18S rRNA genes by the collaborative group of Dr. A. Chatzinotas at the Helmholtz Centre (UFZ) in Leipzig. Cellulose, cellobiose, and glucose were mineralized to carbon dioxide under oxic conditions, whereas different fermentation products accumulated under anoxic conditions. Fermentations occurred concomitant with the apparent reduction of nitrate and ferric iron. The degradation of supplemented saccharides was stable under oxic and anoxic conditions. Archaea were no active constituents of the cellulose-degrading community in the investigated soil. [13C]-cellulose was mainly degraded by Kineosporiaceae (Actinobacteria), the cellulolytic taxon Cluster III Clostridiaceae (Firmicutes), and the new family-level taxon 'Cellu1-3' (Bacteroidetes) under anoxic conditions. Under oxic conditions, the new family-level taxa 'Sphingo1-4' (Bacteroidetes) and 'Deha1' (Chloroflexi), and Planctomycetaceae (Planctomycetes) were involved. Active community members in [13C]-cellobiose and [13C]-glucose treatments differed from those in [13C]-cellulose treatments, and were selectively activated by O2. Twenty-eight of the 48 labeled bacterial family-level taxa did not closely affiliate with cultured species. Labeled Eukaryotes belonged to the families Bodonidae, Eustigmataceae, Mallomonadaceae, Opistonectidae, unclassified Chrysophyceae, and unclassified Stramenopiles. These families inhabit autotrophic algae and bacteriovorus flagellates. It is likely that these active Eukaryotes were labeled by incorporation of [13C]-carbon derived from grazing on active cellulolytic and saccharolytic soil bacteria. Fungi were not labeled in stable isotope probing experiments. The pesticides Bentazon, MCPA and Nonylphenol impaired cellulose-linked microbial processes only at pesticide concentrations far above the recommended rate. The impairment was most pronounced under anoxic conditions. Planctomycetaceae and the new family-level taxon 'Sphingo1-4' were sensitive to pesticide addition under oxic conditions, whereas Cluster I Clostridiaceae and the new family-level taxon 'Cellu1-3' were reduced under anoxic conditions. Nevertheless, the impact of pesticides on the degradation of saccharides at in situ-relevant concentrations seems to be minimal. These collective findings suggest that (i) a large uncultured diversity of Bacteria was involved in the degradation of cellulose, (ii) O2 selectively activates different cellulolytic and saccharolytic taxa, (iii) Cluster III Clostridiaceae, and the new family-level taxa 'Sphingo1-4' and 'Cellu1-3' represent the major cellulolytic constituents of the microbial community in the investigated agricultural soil, whereas Cluster I Clostridiaceae, Intrasporangiaceae and Micrococcaceae are saccharolytic satellite organisms that utilize cellulose-derived carbon, and (iv) the degradation of plant-derived saccharides is a community function that is stabilized by the rapid response of active bacterial taxa and independent of fluctuating availabilities of O2 and of pesticide application.
