Microbial Interactions Drive the Complete Catabolism of the Antibiotic Sulfamethoxazole in Activated Sludge Microbiomes.

Affiliation

Qi M(1), Liang B(1)(2)(3), Zhang L(4), Ma X(1), Yan L(5), Dong W(6), Kong D(3), Zhang L(1), Zhu H(5), Gao SH(1)(2), Jiang J(4), Liu SJ(5), Corvini PF(7)(8), Wang A(1)(2)(3).
Author information:
(1)State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of Technology, Harbin 150090, China.
(2)School of Civil & Environmental Engineering, Harbin Institute of Technology
(Shenzhen), Shenzhen 518055, China.
(3)Key Laboratory of Environmental Biotechnology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China.
(4)Department of Microbiology, Key Lab of Microbiology for Agricultural Environment, Ministry of Agriculture, College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China.
(5)State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
(6)Department of Civil and Natural Resources Engineering, University of Canterbury, Christchurch 8140, New Zealand.
(7)Institute for Ecopreneurship, School of Life Sciences, University of Applied Sciences and Arts Northwestern Switzerland, Muttenz 4132, Switzerland.
(8)State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing 210023, China.

Abstract

Microbial communities are believed to outperform monocultures in the complete catabolism of organic pollutants via reduced metabolic burden and increased robustness to environmental challenges; however, the interaction mechanism in functional microbiomes remains poorly understood. Here, three functionally differentiated activated sludge microbiomes (S1: complete catabolism of sulfamethoxazole (SMX); S2: complete catabolism of the phenyl part of SMX ([phenyl]-SMX) with stable accumulation of its heterocyclic product 3-amino-5-methylisoxazole (3A5MI); A: complete catabolism of 3A5MI rather than [phenyl]-SMX) were enriched. Combining time-series cultivation-independent microbial community analysis, DNA-stable isotope probing, molecular ecological network analysis, and cultivation-dependent function verification, we identified key players involved in the SMX degradation process. Paenarthrobacter and Nocardioides were primary degraders for the initial cleavage of the sulfonamide functional group (-C-S-N- bond) and 3A5MI degradation, respectively. Complete catabolism of SMX was achieved by their cross-feeding. The co-culture of Nocardioides, Acidovorax, and Sphingobium demonstrated that the nondegraders Acidovorax and Sphingobium were involved in the enhancement of 3A5MI degradation. Moreover, we unraveled the internal labor division patterns and connections among the active members centered on the two primary degraders. Overall, the proposed methodology is promisingly applicable and would help generate mechanistic, predictive, and operational understanding of the collaborative biodegradation of various contaminants. This study provides useful information for synthetic activated sludge microbiomes with optimized environmental functions.