Coordinated plant and microbial transcriptional responses to oil-sands process-affected water

Constructed wetland treatment systems (CWTSs) are promising options for treating oil-sands process-affected water (OSPW), which contains toxic naphthenic acid fraction compounds (NAFCs). However, the molecular mechanisms underlying NAFCs attenuation by plants and root microbes remain poorly resolved. In our previous mesocosm study, Typha latifolia increased NAFC removal 2.5-fold relative to unplanted controls without reducing plant growth. Here, using RNA from that same experimental system, we applied metatranscriptomics to 40 root samples collected over 60 days to characterize plant and active microbial responses to OSPW exposure. The active root-associated microbial community was dominated by Pseudomonadota, and Burkholderiales remained the most active order, although Flavobacteriaceae (Bacteroidota) activity increased with time when exposed to OSPW. Microbial community composition shifted with both time and water type, and 42 genes with potential roles in NAFC or related organic-compound transformation were differentially expressed in OSPW mesocosms. These responses were dominated by oxidoreductases affiliated mainly with Burkholderiales and Rhizobiales. The host plant also responded strongly to OSPW, up-regulating genes encoding oxidoreductases, transporters, and glycosyltransferases associated with xenobiotic stress and detoxification. Together, these results revealed coordinated plant and microbial transcriptional responses in a system where enhanced NAFC attenuation had already been demonstrated chemically. The observed patterns, however, likely reflect the broader OSPW mixture rather than NAFCs alone.