Processing of grassland soil C-N compounds into soluble and volatile molecules is depth stratified and mediated by genomically novel bacteria and archaea

Abstract

Soil microbial activity drives the carbon and nitrogen cycles and is an important determinant of atmospheric trace gas turnover, yet most soils are dominated by organisms with unknown metabolic capacities. Even Acidobacteria, among the most abundant bacteria in soil, remain poorly characterized, and functions across groups such as Verrucomicrobia, Gemmatimonadetes, Chloroflexi, Rokubacteria are understudied. Here, we resolved sixty metagenomic, and twenty proteomic datasets from a grassland soil ecosystem and recovered 793 near-complete microbial genomes from 18 phyla, representing around one third of all organisms detected. Importantly, this enabled extensive genomics-based metabolic predictions for these understudied communities. Acidobacteria from multiple previously unstudied classes have genomes that encode large enzyme complements for complex carbohydrate degradation. Alternatively, most organisms we detected encode carbohydrate esterases that strip readily accessible methyl and acetyl groups from polymers like pectin and xylan, forming methanol and acetate, the availability of which could explain high prevalences of C1 metabolism and acetate utilization in genomes. Organism abundances among samples collected at three soil depths and under natural and amended rainfall regimes indicate statistically higher associations of inorganic nitrogen metabolism and carbon degradation in deep and shallow soils, respectively. This partitioning decreased in samples under extended spring rainfall indicating long term climate alteration can affect both carbon and nitrogen cycling. Overall, by leveraging natural and experimental gradients with genome-resolved metabolic profiles, we link organisms lacking prior genomic characterization to specific roles in complex carbon, C1, nitrate, and ammonia transformations and constrain factors that impact their distributions in soil.

Niche differentiation is spatially and temporally regulated in the rhizosphere

“…Using these guilds, we determined the prevalence of three d-CAZy transcriptional strategies in the rhizosphere, and found that rhizosphere organisms upregulate decomposition transcripts in addition to increasing population sizes. Further, these populations used both primary and breakdown products, and supports recent observations that metabolic handoffs link together interacting members of microbial communities (79)(80)(81). Guilds dynamics of carbohydrate depolymerization during rhizosphere succession provides a key step towards developing microbially-constrained models to predict the fate of soil carbon.…”

“…Genome-resolved metagenomic analyses indicate the importance of metabolic byproduct handoff in linking together interacting members of microbial communities (80,81). The breadth of carbohydrate degradation pathways that Rhizosphere and Detritusphere guilds engage in may be a potential explanation for the stable, positive and repeatable interaction networks in the rhizosphere that we observed in a previous study (82).…”

“…xylan degradation, but also their breakdown products. Recent work suggests that facilitative processes such as cross-feeding in large networks can act to stabilize coexisting competitors for resources (79)(80)(81).…”

Soil bacterial communities associated with stony soils influence the tuber size of Tetrastigma hemsleyanum

“…These groups are widely distributed in ne earth, most of them showing a positive correlation with pH and a negative relationship with nutrient elements, such as soil organic carbon, TN, and available phosphorus [35,36]. The genomes of Acidobacteria encode large enzyme complements for degrading complex carbohydrates, which, in turn, impacts on the carbon distribution in the soil [37]. The bacteria from Chloro exi and WPS-2 were strongly associated with physicochemical soil properties, such as pH, AS, and TN, and Chloro exi were able to scavenge organic matter like sucrose, glucose, and N-acetyl-glucosamine under anoxic conditions [38,39].…”

“…The genomes of bacteria from the Verrucomicrobia and Rokubacteria contain some of the earliest dissimilatory sul te reductases to induce sul te/sulfate reduction, and thus play an important role in the global sulfur cycle [44]. The genome of Rokubacteria also exhibits an extensive capacity to biosynthesize diverse small organic molecules that promote mineral dissolution [37]. This may explain why stony soils were richer in nutrients than non-stony soils in both the BS and RZS samples ( Table 2).…”