Oxygen Availability and Environmental Origin as dual Ecological Filters Shaping Aerobic Hydrocarbon-degrading Enrichment Microbial Communities

Abstract

Oxygen availability and environmental origin are key ecological factors jointly structuring microbial communities involved in aerobic petroleum hydrocarbon degradation. To assess their relative importance, we established parallel enrichments under aerobic (7–8 mg L⁻¹ dissolved oxygen) and microaerobic (~ 0.5 mg L⁻¹ dissolved oxygen) conditions from two contrasting environments: a human-impacted hydrocarbon-contaminated field groundwater and formation water from a crude oil well representing a natural petroleum system. Community dynamics were analysed by 16 S rRNA gene amplicon sequencing at both phylum and genus levels. Permutational multivariate analysis of variance (PERMANOVA) and distance-based redundancy analysis (db-RDA) revealed that both environmental origin (R² = 0.44, p = 0.002) and oxygen availability (R² = 0.26, p = 0.006) significantly structured community composition, with environmental origin accounting for a larger proportion of total variance. Nevertheless, oxygen availability acted as a consistent ecological filter, selecting for reproducible, redox-specific functional consortia across both source environments. At the phylum level, Actinomycetota proliferated under aerobic conditions with Dietzia emerging as a key aerobic genus, consistently suppressed under oxygen limitation. In contrast, Pseudomonas maintained a strong presence across both regimes, while Acinetobacter was largely restricted to microaerobic enrichments, where it became a major genus, underscoring its ecological role as a hydrocarbon degrader in oxygen-limited systems. Together, these findings demonstrate that hydrocarbon-degrading community assembly is governed by the interplay of environmental origin — determining baseline diversity and species-level composition — and oxygen availability, which selects for functionally coherent consortia regardless of source environment, highlighting the relevance of redox control in petroleum-impacted ecosystems.