Coupled nitrogen fixation and substrate stabilization drive ecological strategy shifts during microbial succession

ABSTRACT:

Background:

Primary succession is predicted to proceed through shifts from stress-tolerant to competitive to cooperative ecological strategies as resource availability increases, yet molecular evidence for these transitions in microbial systems remains limited. Here, we used an integrated multi-omics approach to investigate how microbial functional traits and chemical outputs change across early ecosystem development using experimental basaltic hillslopes spanning succession from bare rock through biocrust to moss-dominated communities.

 

Results:

Genome-resolved analyses revealed stress-tolerant pioneer communities enriched in oxidative and temperature stress-response genes on nitrogen-limited and physically unstable basalt. These communities were replaced by competitive nitrogen-fixing cyanobacteria that formed biocrusts enriched in carbon and nitrogen fixation pathways while stabilizing substrates through exopolysaccharide production. This stabilization enabled the establishment of functionally diverse moss-associated communities characterized by complete biogeochemical cycling and cooperative metabolic interactions. Metabolomic profiling linked these functional transitions to distinct chemical signatures across succession. Early stages were enriched in organic nitrogen- and sulfur-containing compounds, intermediate stages accumulated nucleosides and organic acids, and later stages were characterized by complex lipids and secondary metabolites. Metabolites discriminated successional stages with substantially higher accuracy than taxonomic markers, indicating that functional outputs in this system more reliably capture ecosystem state than community composition. While microbial community assembly shifted from stochastic to deterministic processes over succession, metabolite assembly remained predominantly deterministic throughout.

 

Conclusions:

Integration across genomic and metabolomic data demonstrates that cyanobacterial nitrogen fixation coupled with substrate stabilization alleviates nutrient limitation and modifies physical habitat conditions, driving successional progression through ecological strategy shifts. These results advance succession theory by showing that biogeochemical and physical processes operate in tandem rather than sequentially. These molecular insights provide the first comprehensive evidence for predicted ecological strategy shifts at the molecular level and offer a framework for ecosystem monitoring and restoration, with stage specific metabolic signatures serving as quantitative biomarkers for assessing recovery trajectories.

INSTRUMENT(S): Liquid Chromatography MS - positive - reverse-phase, Direct infusion MS - negative, Liquid Chromatography MS - negative - hilic

PROVIDER: MTBLS14041 | MetaboLights | 2026-03-12

REPOSITORIES: MetaboLights