Carbon cycle in the microbial ecosystems of biological soil crusts

Abstract

The carbon cycle (C-cycle) is the most important and complex biogeochemical cycle in soil ecosystems, but our understanding of C-cycle at the community level remains limited. Biocrusts are known ecosystem engineers and represent ideal model systems for biogeochemical cycling studies. Here, metagenomic sequencing based on five repeated collections of four types of biocrusts revealed a low abundance of genes related to light-driven inorganic carbon fixation, and high abundance of genes related to the chemical energy-driven degradation of macromolecular organic carbon (OC), fermentation, aerobic respiration, and CO oxidation. For OC decomposition, genes mediating starch/glycogen and cellulose degradation were most abundant during the initial complex OC degradation, as were genes mediating fermentation during terminal steps of OC decomposition. To assess successional changes in carbon cycle, the metagenomic data were combined with absolute quantification via GeoChip, as well as key enzyme activity measurements. Inorganic carbon fixation, fermentation, CH4 oxidation, and both starch/glycogen and peptidoglycan degradation decreased during succession. However, several high efficiency processes, as well as CO oxidation and most types of OC degradation, increased. Co-occurrence networks revealed that C-cycle in biocrusts consists of an assimilation module, akin to primary production, and a dissimilation module, comparable to secondary production; dynamic changes in the relationships between C-cycle pathways and microbial community composition occurred during succession. The two C-cycle modules were connected by the Calvin-Benson-Bassham cycle, as well as ethanol and propionate fermentation; the modules were balanced by drought and salinity. Collectively, these results improve our understanding of C-cycle pathways and regulatory mechanisms in biocrust succession, and provide a basis for future multi-omics studies of these systems.