Core taxa, co-occurrence pattern, diversity, and metabolic pathways contributing to robust anaerobic biodegradation of chlorophenol

Ming Lin; Chenhui Pan; Chenyi Qian; Fei Tang; Siwen Zhao; Jun Guo; Yongming Zhang; Jiaxiu Song; Bruce E Rittmann

doi:10.1016/j.envres.2023.117591

Core taxa, co-occurrence pattern, diversity, and metabolic pathways contributing to robust anaerobic biodegradation of chlorophenol

Environ Res. 2024 Jan 15:241:117591. doi: 10.1016/j.envres.2023.117591. Epub 2023 Nov 4.

Authors

Ming Lin¹, Chenhui Pan¹, Chenyi Qian¹, Fei Tang¹, Siwen Zhao¹, Jun Guo², Yongming Zhang¹, Jiaxiu Song³, Bruce E Rittmann⁴

Affiliations

¹ School of Environmental and Geographical Sciences, Shanghai Normal University, Shanghai, 200234, PR China; Yangtze River Delta Urban Wetland Ecosystem National Field Scientific Observation and Research Station, Shanghai, 200234, PR China.
² School of Environmental and Geographical Sciences, Shanghai Normal University, Shanghai, 200234, PR China; Department of Environmental Science and Engineering, Fudan University, Shanghai, 200238, PR China.
³ School of Environmental and Geographical Sciences, Shanghai Normal University, Shanghai, 200234, PR China; Yangtze River Delta Urban Wetland Ecosystem National Field Scientific Observation and Research Station, Shanghai, 200234, PR China. Electronic address: songjiaxiu@shnu.edu.cn.
⁴ Biodesign Swette Center for Environmental Biotechnology, Arizona State University, Tempe, AZ, 85287-5701, USA.

PMID: 37926226
DOI: 10.1016/j.envres.2023.117591

Abstract

It is hard to achieve robustness in anaerobic biodegradation of trichlorophenol (TCP). We hypothesized that specific combinations of environmental factors determine phylogenetic diversity and play important roles in the decomposition and stability of TCP-biodegrading bacteria. The anaerobic bioreactor was operated at 35 °C (H condition) or 30 °C (L condition) and mainly fed with TCP (from 28 μM to 180 μM) and organic material. Metagenome sequencing was combined with 16S rRNA gene amplicon sequencing for the microbial community analysis. The results exhibited that the property of robustness occurred in specific conditions. The corresponding co-occurrence and diversity patterns suggest high collectivization, degree and evenness for robust communities. Two types of core functional taxa were recognized: dechlorinators (unclassified Anaerolineae, Thermanaerothrix and Desulfovibrio) and ring-opening members (unclassified Proteobacteria, Methanosarcina, Methanoperedens, and Rubrobacter). The deterministic process of the expansion of niche of syntrophic bacteria at higher temperatures was confirmed. The reductive and hydrolytic dechlorination mechanisms jointly lead to C-Cl bond cleavage. H ultimately adapted to the stress of high TCP loading, with more abundant ring-opening enzyme (EC 3.1.1.45, ∼55%) and hydrolytic dechlorinase (EC 3.8.1.5, 26.5%) genes than L (∼47%, 10.5%). The functional structure (based on KEGG) in H was highly stable despite the high loading of TCP (up to 60 μM), but not in L. Furthermore, an unknown taxon with multiple functions (dechlorinating and ring-opening) was found based on genetic sequencing; its functional contribution of EC 3.8.1.5 in H (26.5%) was higher than that in L (10.5%), and it possessed a new metabolic pathway for biodegradation of halogenated aromatic compounds. This new finding is supplementary to the robust mechanisms underlying organic chlorine biodegradation, which can be used to support the engineering, regulation, and design of synthetic microbiomes.

Keywords: Co-occurrence network; Dechlorination; Diversity; Microbiome; Robustness; Trichlorophenol.

MeSH terms

Anaerobiosis
Bacteria / metabolism
Biodegradation, Environmental
Chlorophenols*
Phylogeny
RNA, Ribosomal, 16S / genetics

Substances

Chlorophenols
RNA, Ribosomal, 16S