TY - JOUR
T1 - Integrated use of electrochemical anaerobic reactors and genomic based modeling for characterizing methanogenic activity in microbial communities exposed to BTEX contamination
AU - Yusim, Evgenia Jenny
AU - Zarecki, Raphy
AU - Medina, Shlomit
AU - Carmi, Gon
AU - Mousa, Sari
AU - Hassanin, Mahdi
AU - Ronen, Zeev
AU - Wu, Zhiming
AU - Jiang, Jiandong
AU - Baransi-Karkaby, Katie
AU - Avisar, Dror
AU - Sabbah, Isam
AU - Yanuka-Golub, Keren
AU - Freilich, Shiri
N1 - Publisher Copyright:
© 2025 Elsevier Inc.
PY - 2025/3/1
Y1 - 2025/3/1
N2 - In soil polluted with benzene, toluene, ethylbenzene, and xylenes (BTEX), oxygen is rapidly depleted by aerobic respiration, creating a redox gradient across the plume. Under anaerobic conditions, BTEX biodegradation is then coupled with fermentation and methanogenesis. This study aimed to characterize this multi-step process, focusing on the interactions and functional roles of key microbial groups involved. A reactor system, comprising an Anaerobic Bioreactor (AB) and two Microbial Electrolysis Cell (MEC) chambers, designed to represent different spatial zones along the redox gradient, operated for 160 days with intermittent exposure to BTEX. The functional differentiation of each chamber was reflected by the gas emission profiles: 50%, 12% and 84% methane in the AB, anode and cathode chambers, respectively. The taxonomic profiling, assessed using 16S amplicon sequencing, led to the identification chamber-characteristic taxonomic groups. To translate the taxonomic shift into a functional shift, community dynamics was transformed into a simulative platform based on genome scale metabolic models constructed for 21 species that capture both key functionalities and taxonomies. Representatives include BTEX degraders, fermenters, iron reducers acetoclastic and hydrogenotrophic methanogens. Functionality was inferred according to the identification of the functional gene bamA as a biomarker for anaerobic BTEX degradation, taxonomy and literature support. Comparison of the predicted performances of the reactor-specific communities confirmed that the simulation successfully captured the experimentally recorded functional variation. Variations in the predicted exchange profiles between chambers capture reported and novel competitive and cooperative interactions between methanogens and non-methanogens. Examples include the exchange profiles of hypoxanthine (HYXN) and acetate between fermenters and methanogens, suggesting mechanisms underlying the supportive/repressive effect of taxonomic divergence on methanogenesis. Hence, the platform represents a pioneering attempt to capture the full spectrum of community activity in methanogenic hydrocarbon biodegradation while supporting the future design of optimization strategies.
AB - In soil polluted with benzene, toluene, ethylbenzene, and xylenes (BTEX), oxygen is rapidly depleted by aerobic respiration, creating a redox gradient across the plume. Under anaerobic conditions, BTEX biodegradation is then coupled with fermentation and methanogenesis. This study aimed to characterize this multi-step process, focusing on the interactions and functional roles of key microbial groups involved. A reactor system, comprising an Anaerobic Bioreactor (AB) and two Microbial Electrolysis Cell (MEC) chambers, designed to represent different spatial zones along the redox gradient, operated for 160 days with intermittent exposure to BTEX. The functional differentiation of each chamber was reflected by the gas emission profiles: 50%, 12% and 84% methane in the AB, anode and cathode chambers, respectively. The taxonomic profiling, assessed using 16S amplicon sequencing, led to the identification chamber-characteristic taxonomic groups. To translate the taxonomic shift into a functional shift, community dynamics was transformed into a simulative platform based on genome scale metabolic models constructed for 21 species that capture both key functionalities and taxonomies. Representatives include BTEX degraders, fermenters, iron reducers acetoclastic and hydrogenotrophic methanogens. Functionality was inferred according to the identification of the functional gene bamA as a biomarker for anaerobic BTEX degradation, taxonomy and literature support. Comparison of the predicted performances of the reactor-specific communities confirmed that the simulation successfully captured the experimentally recorded functional variation. Variations in the predicted exchange profiles between chambers capture reported and novel competitive and cooperative interactions between methanogens and non-methanogens. Examples include the exchange profiles of hypoxanthine (HYXN) and acetate between fermenters and methanogens, suggesting mechanisms underlying the supportive/repressive effect of taxonomic divergence on methanogenesis. Hence, the platform represents a pioneering attempt to capture the full spectrum of community activity in methanogenic hydrocarbon biodegradation while supporting the future design of optimization strategies.
KW - AB-MEC bioreactor system
KW - Acetoclastic methanogens
KW - BTEX
KW - Dynamic flux balance analysis
KW - Hydrogenotrophic methanogens
KW - Metabolic modeling
KW - Microbial functional groups
KW - Soil pollution
UR - http://www.scopus.com/inward/record.url?scp=85214296587&partnerID=8YFLogxK
M3 - Article
C2 - 39746623
AN - SCOPUS:85214296587
SN - 0013-9351
VL - 268
JO - Environmental Research
JF - Environmental Research
M1 - 120691
ER -