Bacteriophage–prokaryote dynamics and interaction within anaerobic digestion processes across time and space

Junyu Zhang, Qun Gao, Qiuting Zhang, Tengxu Wang, Haowei Yue, Linwei Wu, Jason Shi, Ziyan Qin, Jizhong Zhou, Jiane Zuo, Yunfeng Yang

Bacteriophage-prokaryote dynamics and interaction are believed to be important in governing microbiome composition and ecosystem functions, yet our limited knowledge of the spatial and temporal variation in phage and prokaryotic community compositions precludes accurate assessment of their roles and impacts. Anaerobic digesters are ideal model systems to examine phage-host interaction, owing to easy access, stable operation, nutrient-rich environment, and consequently enormous numbers of phages and prokaryotic cells. Equipped with high-throughput, cutting-edge environmental genomics techniques, we examined phage and prokaryotic community composition of four anaerobic digesters in full-scale wastewater treatment plants across China. Despite the relatively stable process performance in biogas production, phage and prokaryotic groups fluctuated monthly over a year of study period, showing significant correlations between those two groups at the α- and β-diversity levels. Strikingly, phages explained 40.6% of total variations of the prokaryotic community composition, much higher than the explanatory power by abiotic factors (14.5%). Consequently, phages were significantly (P < 0.010) linked to parameters related to process performance including biogas production and volatile solid concentrations. Association network analyses showed phage-prokaryote pairs were shallowly conserved since they were detected only within small viral clades. Those results collectively demonstrate phages as a major biotic factor in controlling prokaryotic composition and process performance. Therefore, phages may play a larger role in shaping prokaryotic community dynamics and process performance of anaerobic digesters than currently appreciated.